Tony Anh-Khôi

Lisa Bảo-Anh

Dr Yvan Rahbé

Prof François Verheggen

Yvan Capowiez

Dr Anne-Violette Violette Lavoir

Eric Wajnberg

Lucie Monticelli

María Concepción

Sylvain Benhamou

Morgane Canovas

Maria

Awawing, Yanyan, Yusha, Christine, Mateus, Marianne, Sylla, Wenyen, Liu, Rihem Eva Ali

Thu Ha Le

Nguyen

Edwige Amiens-Desneux

Chen Luo

George E Heimpel

Jean-Luc Gatti

Nicolas Desneux
email: nicolas.desneux@inra.fr

Le-Thu-Ha Nguyen

Christiane Métay-Merrien

Preference-performance relationship in host use by generalist parasitoids

Keywords: host specificity, preference-performance hypothesis, tritrophic interactions, water limitation, biological control Host range, generalist parasitoids, specialization, preference-performance hypothesis, aphid host range, oviposition, tritrophic interactions, abiotic stress, drought

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The pursuit of knowledge and the wind of change brought me to INRA to start this Ph.D.

Table of Contents

Tables

 Table 1.Specialists vs generalists: pros and cons in biological control. Table 2. Bottom-up effects of abiotic factors including water supply, nutrient supply, light, and temperature. Table 3. Articles on the subject: "Impacts of water stress on the tritrophic plant-aphidparasitoid system." Table 4. Biotic and abiotic factors affecting the host specificity of aphid parasitoids Table 5. Articles on the subject: "Impacts of abiotic stress on the tritrophic plant-aphidparasitoid system". Table 6. Lists of study using Aphidius ervi as biological models.

List of abbreviations

Résumé de la thèse en français

La lutte biologique (LB) ou l'utilisation d'ennemis naturels pour lutter contre les ravageurs (espèces nuisibles pour l'intérêt humain telles que les arthropodes herbivores dans les systèmes agricoles) est une pratique agricole traditionnelle millénaire [START_REF] Van Den Bosch | The History and Development of Biological Control. An Introduction to Biological Control[END_REF] (et ce même si le concept de lutte biologique en lui même a était introduit en 1868 par les travaux de Riley en Californie). La pratique de la LB s'est transmise à travers les âges et continue encore aujourd'hui. Parce que les méthodes des LB sont durables, respectueuses de l'environnement et potentiellement rentables, elles sont aujourd'hui une approche systémique et post-pesticide qui permet aussi de limited l'apparition de résistances aux pesticides dans les populations d'espèces ciblées. Les trois approches principales de LB sont la lutte classique (libération d'ennemis naturels exotiques pour contrôler les ravageurs éxotiques envahissants), la lutte par augmentation (augmentation des populations d'ennemis naturels indigènes) et la lutte par conservation (aménagement des habitats pour favoriser les populations d'ennemis naturels pour réguler les ravageurs).

L'efficacité de ces approches dépend de l'efficacité de l'agent de lutte biologique (ALB) qui dépend elle-même de plusieurs facteurs dont leurs caractéristiques biologiques et leurs interactions avec l'environnement). L'utilisation des ALB nécessite donc une connaissance écologique du fonctionnement des écosystèmes i.e. des facteurs biotiques et abiotiques qui interagissent dans l'environnement. Les critères les plus pertinents prennent en compte la biodiversité, la spécialisation écologique (l'utilisation des ressources et les rôles des espèces dans les réseaux écologiques) ainsi que les interactions et les forces qui régulent les écosystèmes.

Les pucerons sont des parasites végétaux qui causent des pertes importanes de rendement (Valenzuela et Hoffmann 2014), soit par dommages directs en se nourrissant sur les plantes de cultures, soit indirectement via la transmission de virus (van Emden et Harrington 2007).

En outre, ils résistent à plusieurs types d'insecticides [START_REF] Bass | Insecticide resistance in the peach potato aphid, Myzus persicae, Part 2: Metabolic mechanisms and host adaptation[END_REF], Bass et al., 2014). Par conséquent, l'approche LB contre les pucerons apparaît comme une méthode de lutte à fort potentiel.

Parmi les ennemis naturels des pucerons, les parasitoïdes sont couramment utilisés comme ALB aussi bien dans les serres qu'en plein champs. Les parasitoïdes sont des espèces dont les larves se développent en se nourrissant dans le corps de leur hôte, généralement des insectes. En raison de cette stratégie d'alimentation spécifique, les parasitoïdes s'adaptent à leurs hôtes et co-évoluent strictement avec eux. Grâce à leur haute spécificité, les parasitoïdes sont largement utilisés en LB en tant qu'agents contre les ravageurs des cultures.

Pour choisir un ALB parasitoïde potentiel, les scientifiques doivent évaluer leur spécificité d'hôte et l'efficacité d'utilisation de leur hôte à différentes échelles. De plus, les informations sur l'écosystème où un ALB est relâché, pourraient aider à prédire ses réponses sur le terrain.

L'étude de la spécificité hôte du parasitoïde contribue à (1) comprendre les mécanismes qui structurent les communautés hôtes-parasitoïdes, et [START_REF] Calvo | The performance of an aphid parasitoid is negatively affected by the presence of a circulative plant virus[END_REF] [START_REF] Power | Top-down and Bottom-up Forces in Food Webs -Do Plants Have Primacy[END_REF].

Dans ce contexte, on peut se demander si les forces environnementales ascendantes qui régulent les réseaux écologiques pourraient affecter le contrôle descendant, c'est-à-dire l'efficacité des parasitoïdes en modulant leur spécificité d'hôte. L'étude des effets ascendants d'un facteur abiotique, ici la limitation en eau, sur le système tritrophique 'plante-puceronparasitoïde' pourrait aider à prédire l'efficacité d'un ACB parasitoïde sur le terrain. Cet objectif est rappelé et détaillé dans le chapitre 3.

Pour y répondre, nous avons tout d'abord appliqué les méthodes de test de la gamme d'hôtes et calculé les deux paramètres, indice de spécificité de l'hôte et corrélation préférenceperformance, pour évaluer la spécificité hôte de trois parasitoïdes de pucerons (chapitre 4).

Ces deux paramètres ont été testés dans l'idée de voir s'ils étaient plus pertinents et précis pour classer les parasitoïdes au sein du continuum de spécialistes -généralistes. La gamme d'hôtes fondamentale de ces trois parasitoïdes a été déterminée par expérimentations en conditions de laboratoire permettant de calculer l'indice de spécificité de l'hôte et d'analyser la relation préférence-performance (article 1). La gamme d'hôtes fondamentale a ensuite été comparée à la gamme d'hôtes sur le terrain, rapportée dans la littérature. Enfin, l'indice de spécificité et la relation préférence-performance se sont révélés comme étant des paramètres appropriés à appliquer dans les schémas futurs de test de gamme d'hôtes, notamment dans le cadre de la LB. Dans cette étude, Diaeretiella rapae et Aphelinus abdominalis sont généralistes et peuvent se développer sur une large gamme d'hôtes. A. ervi est une espèce intermédiaire spécialisée dont les femelles attaquaient toutes les espèces de pucerons à des taux élevés, mais était capable de se développer avec succés que sur quelques espèces de pucerons.

Dans un deuxième temps, nous avons testé les effets ascendants d'un facteur abiotique sur la spécificité d'hôte d'un parasitoïde (chapitre 5). Pour se faire, nous avons choisi d'utiliser Aphidius ervi (Hymenoptera: Braconidae: Aphidiinae), identifié comme spécialiste intermédiaire dans l'étude précédente. Les femelles d'A. ervi ont attaqué toutes les espèces de pucerons proposées à des taux élevés mais n'ont pu se développer complétement que sur quelques hôtes, tous appartenant à la tribu des Macrosiphini. Sa position médiane dans le continuum spécialiste-généraliste favorisait nos chances de voir un effet de modulation du facteur environnemental sur sa gamme d'hôte i.e. le parasitoïde est-il toujours capable d'évaluer la même espèce hôte, potentiellement de qualité différente dans un environnement différent ? S'il y a impact, que se passe-t-il aux niveaux trophiques inférieurs (plantes et pucerons) qui pourrait expliquer les variations de la gamme d'hôte ? Nous avons tout d'abord réalisé une étude bibliographique pour identifier les facteurs abiotiques susceptibles d'influencer la préférence et la performance des parasitoïdes par effet bottomup. Cette étude nous a permis d'identifier la limitation en eau comme étant un stress abiotique pertinent pour l'étude des effets bottom-up sur la modulation de la gamme d'hôte.

Nous avons ainsi testé l'impact de la limitation en eau sur la préférence et la performance du parasitoïde A. ervi sur deux de ses meilleurs hôtes i.e. deux espèces de pucerons dans lequel il se développe bien (article 2). Les effets observés nous ont poussé à étudier d'autres complexes plante-puceron (six en tout) représentant des hôtes plus ou moins bons pour A. ervi (article 3). Nous avons utilisé la même méthode que dans le chapitre 4 pour évaluer et comparer la spécificité d'hôte d'A. ervi. i.e. nous avons calculé son indice de spécificité d'hôte et analysé la corrélation préférence-performance en conditions optimales vs limitées d'apport en eau pour la plante. De plus, les modifications induites par la limitation en eau chez la plante et les pucerons ont été mesurées pour (1) confirmer l'impact de nos traitements et [START_REF] Calvo | The performance of an aphid parasitoid is negatively affected by the presence of a circulative plant virus[END_REF] proposer des pistes sur les mécanismes potentiels.

La corrélation positive préférence-performance ainsi que le signal phylogénétique des hôtes pucerons sur la performance des parasitoïdes ont bien été retrouvés en conditions optimales conformément aux expériences précédentes (chapitre 4). Mais dans les conditions stressées, la corrélation est perdue car la préférence et la performance des parasitoïdes ont été affectées. La limitation en eau a diminué la qualité nutritionnelle des plantes, ce qui s'est traduit par une faible performance des pucerons sur les plantes hôtes, ce qui a diminué la capacité des parasitoïdes. Ces effets de la limitation en eau sur la préférence et la performance étaient cependant espèces-dépendant. Dans l'ensemble, cette preuve de l'effet ascendant de la limitation de l'eau du sol sur la spécificité de l'hôte parasitoïde soulève une préoccupation pour les parasitoïdes en tant que BCA. Les plantes et les pucerons peuvent tolérer une limitation modérée et à long terme de l'eau, même si leurs performances ont été négativement affectées. Les populations de pucerons pourraient être maintenues sur des plantes stressant l'eau pendant plusieurs semaines sans extinction dans cette étude. Cependant, la mortalité des parasitoïdes sur les hôtes des pucerons a augmenté de manière significative, de 60% sous un apport d'eau optimal à 94,5% en eau limitée sur les hôtes M. persicae. Ainsi, le niveau trophique supérieur avec un degré élevé de spécialisation alimentaire comme les parasitoïdes pourrait souffrir plus que les niveaux trophiques inférieurs. D'autres études devraient être menées pour confirmer cette affirmation, par exemple en étudiant la dynamique des populations de parasitoïdes chez les pucerons hôtes se nourrissant de plantes stressées par l'eau.

En cas d'impacts ascendants négatifs confirmés des facteurs abiotiques sur les parasitoïdes, faut-il libérer ces BCA sous contraintes abiotiques ? Cela pourrait être une perte économique. Dans l'application sur le terrain, les praticiens pourraient augmenter l'efficacité de la sélection des hôtes parasitoïdes par des méthodes telles que (1) l'apprentissage antérieur, comme les exposer à des hôtes de faible qualité avant ou en induisant des composés végétaux volatils pour localiser les hôtes; (2) l'application d'un mélange d'ennemis naturels, par ex. spécialiste ALB sur les pucerons hôtes partagés; (3) l'utilisation d'une combinaison de plante-puceron résistante au stress abiotique pour soutenir l'ALB. Il est bien connu que les réponses des organismes sont très différentes pour chaque type de stress hydrique ou de leur intensité, durée et moment (Huberty et Denno 2004). Il pourrait être intéressant de tester toutes sortes de régimes de limitation de l'eau ou de stress abiotique combiné, par exemple, la limitation de l'eau et l'apport d'engrais sur des systèmes tri-trophiques similaires pour optimiser les régimes d'eau.

Cette étude des facteurs modulant la spécificité de l'hôte des parasitoïdes de pucerons suggère non seulement les rôles significatifs des contraintes abiotiques sur l'ACB, mais aussi contribue à une compréhension plus approfondie de la spécialisation des parasitoïdes.

Mots-clés : spécificité de l'hôte, hypothèse de préférence-performance, interactions tritrophiques, limitation de l'eau, lutte biologique, agents de lutte biologique

Summary

Biological control (BC) including the use of natural enemies to control arthropod herbivore pests in agricultural systems has been a traditional agriculture practice for hundred of years (notably in China) despite being formally developed by Riley in 1868 in California (van den [START_REF] Van Den Bosch | The History and Development of Biological Control. An Introduction to Biological Control[END_REF]. As BC methods are sustainable, environmentally friendly, and costeffective, they are nowadays a possible approach to limit the increase of pesticide resistances in targeted species (resulting from overuse of chemical pesticides). The three main BC strategies are (1) the classical method: the release of exotic natural enemies to control invasive pests; [START_REF] Calvo | The performance of an aphid parasitoid is negatively affected by the presence of a circulative plant virus[END_REF] the augmentative: increasing the populations of indigenous natural enemies; and (3) the conservative: enhancing natural enemy efficiency in regulating pest populations by using methods such as landscape management.

Through these approaches, the efficiency, and the ecological risks for non-target species of the biological control agent (BCA) must be assessed (Roderick et al. 2012). These characteristics can be influenced by several factors, including BCA traits and their interactions with the surrounding environment. BCA use needs ecological knowledge of the ecological specialization such as the diversity of resources that can be used and how the ecosystem is regulated by interactions and forces. The most unpredictable aspect is how the species specialization changes within a new or disturbed environment (Poisot et al. 2011).

Ecological specialization is a process whereby species adapt to their niche to survive. There are two opposite specialization tendencies (1) narrow their resource breadth becoming a specialist or [START_REF] Calvo | The performance of an aphid parasitoid is negatively affected by the presence of a circulative plant virus[END_REF] broaden their resource breadth becoming a generalist. Environmental constraints might increase specialization and variation in abiotic components of the environment might favor generalists. However, the effects depend on interactions between life-history and preference traits (Poisot 2011).

Predators and parasitoids are two main types of BCA to control herbivore pests. Predators are considered generalists in compare to parasitoids because they could feed on prey of different phylogenetic families (Symondson et al. 2002). Parasitoids are species whose larvae develop by feeding on the bodies of their host, usually insects (Godfray 1994). They adapt and co-evolve with their hosts which belong to few families. Thanks to their high specificity, parasitoids are widely used as BCA against crop pests. The study of host specificity of parasitoids contributes to (1) understanding ecological and evolutionary mechanisms driving ecosystems and (2) evaluating the efficiency of BCA and the ecological risks for non-target species.

Aphids are pests which cause massive yield loss which could economically damage up to 500 million dollars per year (Valenzuela and Hoffmann 2014), either directly by feeding on plants, or indirectly via virus transmission (van Emden and Harrington 2007). BC strategies are essential against aphids mostly because they are resistant to several kinds of insecticides (Bass et al. 2014) and their control by chemical compounds may not be carried through.

Among natural enemies of aphids, parasitoids are common BCA both in greenhouses and in the field. To choose a potential BCA parasitoid, scientists must evaluate host specificity and host use efficiency under laboratory conditions and on the field. Moreover, information about the ecosystem where a BCA is released, e.g. the abiotic and biotic environment, should be considered to predict its field efficacy.

This study focused on parasitoid host specificity in the context of the plant-aphid-parasitoid tritrophic system. Chapters 1 and 2 are respectively a literature review on host specificity and the bottom-up effect of water limitation on host specificity. In chapter 1, the ecological context of the host range testing method is provided and involves the ecological specialization concept. The presence of decade-long opposite ideas reveals the complexity of the ecological specialization issue. Therefore, the first question is: from what threshold could a specialist vs. generalist species be defined? Secondly, between specialists and generalist species, who would be dominant and/or evolutionarily favored? The dominants could be at each degree of the specialization continuum, or specialists and generalists could equally co-exist in nature.

Empirical supports exist for each hypothesis and depend on the environment. Principles and applications of host range testing methods have also been presented. However, there is much room for method improvement, e.g. find out characteristics representing the degree of specialization or how to separate specialists/generalists. The two criteria defined and used were parasitoid host specificity index and the correlation between preference and performance, i.e. behavioral and physiological traits, respectively.

Chapter 2 describes the possible effects of environmental factors in an ecological network.

The impacts of abiotic or biotic factors cascade up and down food chains and consist of bottom-up or top-down forces. Bottom-up forces mean resources at the bottom of trophic networks which control the upper trophic consumers. Top-down forces mean higher trophic consumers control lower trophic resources [START_REF] Wollrab | Simple rules describe bottom-up and topdown control in food webs with alternative energy pathways[END_REF]. Similar to the specialization issue, the debate on which forces dominate an ecosystem is still ongoing. Empirical supports exist for contrary hypotheses. Different theories of the dominant forces and the contextdepend outcomes have been presented. The primacy of the control and mediation of plants during bottom-up and top-down regulation [START_REF] Power | Top-down and Bottom-up Forces in Food Webs -Do Plants Have Primacy[END_REF]) have been pointed out. In this context, our hypothesis was that bottom-up forces from environmental stress, precisely soil water limitation, could affect the top-down control, i.e. parasitoid efficiency, through trophic interactions. The study of bottom-up effects of abiotic factors on the tritrophic plant-aphidparasitoid could help predict the real efficacy of a parasitoid BCA in the field conditions. Under environmental stress, especially water limitation, the whole ecosystem might be affected and could lose the ability to recover (Schwalm et al. 2017), and parasitoids in the field under such conditions could be altered behaviorally, physiologically, and genetically.

With this in mind, two main objectives have been defined (chap 3): The first one was to find some relevant indexes to determine the degree of parasitoid host specificity (chap 4). In the second part, the plant-mediated impact of an environmental abiotic stress (water limitation) to the whole tri-trophic system, namely bottom-up effect, has been studied (chap 5). To do so, factors from the three trophic levels that affect parasitoid host exploitation have been recorded such as plant species and quality, aphid species and quality, parasitoid behavior, and physiology under laboratory conditions. Using the data gathered, the host range testing method has been applied to evaluate parasitoid host specificity.

Chapter 4 focuses on parasitoid host specificity. The host range testing method was used to calculate the host specificity index and the preference-performance correlation to evaluate the host specificity of three aphid parasitoids on a broad range of host species. The three parasitoids Diaeretiella rapae, Aphelinus abdominalis and Aphidius ervi have been considered generalists in literature as they have a broad host range in both the Aphidini and Macrosiphini tribes. Their degree of host specificity has been tested using these methods; so, whether the method is suitable to assess parasitoid host specificity and what is needed to improve future schemes of host range testing have been discussed.

In chapter 5, the bottom-up effects of water limitation on parasitoid specificity have been assessed. The same method in chapter 4 has been used to evaluate and compare parasitoid host specificity tested on aphid-plant complexes under water limitation and optimal water supply conditions. Among the three evaluated parasitoids in chap 4, the intermediate specialist Aphidius ervi widely used as an ecological model and a commercial BCA has been chosen to carry out these experiments. The cascade impacts of water limitation on A. ervi host specificity have been analyzed on six plant-aphid combinations. Furthermore, water limitation-induced modifications in plant and aphid life-history traits have also been monitored. Both preference and performance of parasitoids have been affected by water limitation. Our hypotheses were: (1) the stress will alter the quality of plants and aphids which in turn will impact the parasitoid host specificity; (2) the impacts of water limitation will differ according to plant-aphid combinations.

Chapter 1.

Host range testing: biological control practice requiring ecological understanding

Biological control of pests in the ecological context

Then God said, "I give you every seed-bearing plant on the face of the whole earth and every tree that has fruit with seed in it. They will be yours for food." Genesis 1:29 | NIV |

The importance of biological control

Crop losses caused by pests challenge crop protection efforts. Pests throughout the world are destroying about 35% of all crop production [START_REF] Pimentel | Diversification of Biological-Control Strategies in Agriculture[END_REF][START_REF] Oerke | Crop losses to pests[END_REF]). Among them, insect pests cause an estimated 13% crop loss, plant pathogens 12%, and weeds 10% (Cramer, 1967). Crop protection measures could play essential roles in preventing both pre-and postharvesting loss. Since 1942, the discovery of new chemical pesticides gave rise to their golden era where they integrate into many foods, fiber, and fuel production systems. Agricultural producers spent around 40 billion-worth for pesticides per year worldwide for estimated 2.5

x 106 tons of pesticides; these numbers increase annually [START_REF] Pimentel | Diversification of Biological-Control Strategies in Agriculture[END_REF]Popp et al. 2012).

At the first time, pesticides (in this context understood as chemical ones) were efficiency against pests as they protected up to 70% of potential crop yields [START_REF] Oerke | Crop losses to pests[END_REF]). However, intensive overuse of chemical products places a heavy burden on ecology, environment, and human health in the long term and threaten the overall future of agriculture. Pesticide residues were present in surface waters, aquatic sediments, and groundwater in more than 2500 sites in 73 countries [START_REF] Stehle | Agricultural insecticides threaten surface waters at the global scale[END_REF]. They diminish soil biodiversity and spoil soil function by killing beneficial organisms, and indirectly cause soil erosion [START_REF] Fao | Natural Control of Cereal Aphids (Homoptera, Aphididae) by Entomopathogenic Fungi (Zygomycetes, Entomophthorales) and Parasitoids (Hymenoptera, Braconidae and Encyrtidae) on Irrigated Spring Wheat in Southwestern Idaho[END_REF]. Residues of pesticides can also be found in a tremendous variety of everyday foods and beverages, including cooked meals, water, wine, fruit juices, refreshments, and animal feeds [START_REF] Nicolopoulou-Stamati | Chemical Pesticides and Human Health: The Urgent Need for a New Concept in Agriculture[END_REF]. Adverse effects associated with chemical pesticides upon animal or human health include dermatological, gastrointestinal, neurological, carcinogenic, respiratory, reproductive, and endocrine effects (Bonner and Alavanja, 2017; [START_REF] Kim | Exposure to pesticides and the associated human health effects[END_REF]. To confront these deleterious effects, the governments of the countries like USA, EU, Canada, India, China have regulated or restricted the use of several types of pesticides (United Nations, 2009). Since the publication of "Silent Spring" (Rachel [START_REF] Carson | Silent Spring[END_REF], the growing public concern increases the pressure on replacing chemical measures by more sustainable and "green" methods.

Most of all, pesticide application is not omnipotent, as many pest problems in agriculture root in drastic changes in the crop agroecosystem [START_REF] Pimentel | Diversification of Biological-Control Strategies in Agriculture[END_REF]. Despite an apparent increase in pesticide use, crop losses have not significantly decreased during the last 40 years [START_REF] Oerke | Crop losses to pests[END_REF]). In the years of '90 in the US, corn losses to rootworm pests average 12% [START_REF] Pimentel | Diversification of Biological-Control Strategies in Agriculture[END_REF] despite the application of 14 x 10 6 kg insecticide per year. However, in 1945, before the invention of synthesized pesticides, corn losses to these insects averaged only 3.5% (USDA, 1954). Different mechanisms could explain the inefficiency of chemical methods. [START_REF] Pimentel | Diversification of Biological-Control Strategies in Agriculture[END_REF]. Therefore, pest problems and crop protection must be approached by holistic strategies.

Under such circumstance, the concept of Integrated Pest Management (IPM) is developed and implemented at the global scale for over 20 years [START_REF] Fao | Natural Control of Cereal Aphids (Homoptera, Aphididae) by Entomopathogenic Fungi (Zygomycetes, Entomophthorales) and Parasitoids (Hymenoptera, Braconidae and Encyrtidae) on Irrigated Spring Wheat in Southwestern Idaho[END_REF]. IPM is a knowledgeintensive process of decision making that combines various strategies such as biological, cultural, physical, and chemical methods and regular field monitoring of the crops. IPM focuses on the reduction of pesticide use to sustainably manage dangerous pests [START_REF] Fao | Natural Control of Cereal Aphids (Homoptera, Aphididae) by Entomopathogenic Fungi (Zygomycetes, Entomophthorales) and Parasitoids (Hymenoptera, Braconidae and Encyrtidae) on Irrigated Spring Wheat in Southwestern Idaho[END_REF].

As an ecological approach, IPM promotes biological control (BC) methods in pest prevention and suppression among other strategies (Figure 1).

Figure 1. The concept of Integrated Pest Management

BC or the use of natural enemies to control pests has been a traditional agriculture practice up to now (van den [START_REF] Van Den Bosch | The History and Development of Biological Control. An Introduction to Biological Control[END_REF]. However, BC practices are still limited. Over 67000 pest species in the world, 300 pest species targeted to BC; among which only around 120 pest species have been controlled efficiently [START_REF] Pimentel | Diversification of Biological-Control Strategies in Agriculture[END_REF]. Different types of natural enemies used as biological control agents (BCA) include predators, parasitoids (insects that lay eggs inside or on pests and eventually kill them), pathogens (such as fungi and bacterial toxins) and soil predatory nematodes (Heimpel and Mills, 2017) (Figure 2). BC has several advantages in compares to the chemical approach. Firstly, BC associate with few risks on environmental and public health [START_REF] Fao | Natural Control of Cereal Aphids (Homoptera, Aphididae) by Entomopathogenic Fungi (Zygomycetes, Entomophthorales) and Parasitoids (Hymenoptera, Braconidae and Encyrtidae) on Irrigated Spring Wheat in Southwestern Idaho[END_REF]. Secondly, as BCA are highly specific to few targeted pests in compare to pesticides, the efficiency of BCB are promising. Furthermore, BC could have sustainable effects as the released agents are self-powered, self-sufficient, and self-regulating and could permanently establish in the new environment. In such cases, further investments in BC are not required in contrast to the obligate annual applications of pesticides. Examples of other pest species that have been permanently controlled are numerous (Sweetman, 1958;DeBach, 1964;Huffaker, 1980). For example, the introduction of beetle predators in California (USA) has provided effective control of the cottony scale for over 100 years (Simmonds et al., 1976;[START_REF] Pimentel | Diversification of Biological-Control Strategies in Agriculture[END_REF]. Three main strategies of BC are (1) importation or classical BC consists of the introduction of an exotic BCA to regulate a pest species. Over the past 120 years, more than 2000 exotic BCAs were released worldwide to try to control pests in a new area (Bale et al. 2008). ( 2) Augmentative BC consists of inundative or inoculative releases of BCA and their genetical enhancement; (3) Conservation BC includes in managing the agricultural landscape to favor BCA [START_REF] Debach | Biological Control by Natural Enemies[END_REF]) (Figure 3). BC contribute up to US$5.4 billion per year in the USA (Losey and Vaughan, 2006) et al., 2008;[START_REF] Schowalter | Chapter 16 -Application to Sustainability of Ecosystem Services. Insect Ecology[END_REF]. BC within the IPM practice is nowadays a post-pesticide-era approach to counteract the increase of pesticide resistance on targeted species and are a path toward sustainable agriculture. nematodes (Heimpel and Mills 2017).

Figure 3. Spatial and temporal scales of the four main approaches of the BC process (from Klinken 1999)

The risks of BC and requirements for BC practices

Despite all outstanding advantages, BC does not come without risks. The use of BCA also implies ecological risks, e.g. the extinction of non-target native species, or the unpredictable evolution of the BCA in a new environment [START_REF] Kaser | Linking risk and efficacy in biological control hostparasitoid models[END_REF]Roderick et al. 2012).

Most of all, invasive alien species are considered among the most significant threats to global biodiversity. Exotic species once released could benefit from the lack of their natural enemies or the defensive systems of their food species and become dominant in the ecosystem through intra-guild predation (when one of two species (or both) competing for the same host or prey also consumes its competitor) [START_REF] Roy | From biological control to invasion: the ladybird Harmonia axyridis as a model species[END_REF]. As a result, the native biodiversity reduces. The rapid increase in introduced exotic species worldwide and the potential of these species to become invasive have ecological and evolutionary consequences (Olden and Poff 2004;Olden et al. 2006). Secondly, in many cases, the efficiency and the costeffective of BC has been questioned. Many accidentally or intentionally introduced species fail to establish in their new range. Unlike chemical compounds, BCAs are sensible to many biotic and abiotic factors from the ecosystem and from the rearing conditions through ecological interactions. Therefore, the BCA efficiency is not thoroughly predictable. Thirdly, of those alien species that do manage to establish many have negligible effects and some species, often those introduced with agriculture and forestry, are even considered beneficial and desirable (Williamson 1999). Lastly, when the BCA are parasites or parasitoids, the selective pressure upon pest hosts by parasite populations can cause rapid evolution in the pest hosts [START_REF] Lamichhane | Networking of integrated pest management: A powerful approach to address common challenges in agriculture[END_REF]. Therefore, BC practices require a deep understanding of the ecosystem.

BC comes with the concept of keeping pests at an economically acceptable threshold. Often, low levels of populations of some pests are needed to keep natural enemies in the field, and IPM aims to reduce pest populations to avoid damage levels that cause yield loss. Therefore, IPM strategies, mainly BC requires understanding the crop ecosystem as a basis for right crop management decisions and are specific to each crop variety, country, region, and location [START_REF] Fao | Natural Control of Cereal Aphids (Homoptera, Aphididae) by Entomopathogenic Fungi (Zygomycetes, Entomophthorales) and Parasitoids (Hymenoptera, Braconidae and Encyrtidae) on Irrigated Spring Wheat in Southwestern Idaho[END_REF]. The efficiency of the BCA depends on several factors including (1) their biological traits ( 2) interactions with their surrounding environmental conditions, the so-called species niche, and (3) their specificity toward the ecosystem they are released in (Roderick et al.

2012

). Also, risk assessment is an essential component in the development of any biological control strategy [START_REF] Roy | From biological control to invasion: the ladybird Harmonia axyridis as a model species[END_REF]. The prior study of a potential BCA focuses on its BC efficiency and safety. Both parameters could be predicted through the initial evaluation of the BCA host specificity.

Aphid parasitoids as biological control agents

1.2.1. Aphids: biology, agricultural importance, and natural enemies

Aphid biology

Aphids (Hemiptera: Aphididae) are soft-bodied insects of less than 10 mm in length. Their body parts consist of a head, thorax, an abdomen, siphunculus, antenna, and cauda (Figure 4). They can secrete protective liquid, alarm pheromones, and honeydew. Aphids excrete honeydew, which are food resources for several insects such as ants and parasitoids to reduce the osmotic pressure of ingested phloem sap or host plant toxins (Auclair 1963). Among around 4300 aphid species, aphid pests belong mostly to the sub-family Aphidinae of two tribes: Aphidini and Macrosiphini [START_REF] Byeon | Life History Parameters and Temperature Requirements for Development of an Aphid Parasitoid Aphelinus asychis (Hymenoptera: Aphelinidae)[END_REF]. Many aphid species reproduce sexually only under specific environmental conditions, such as during winter. Their parthenogenetic combined with "Russian dolls" reproduction whereby a mother aphid carries both her daughters and their granddaughters allows populations of aphids to increase rapidely [START_REF] Stern | Aphids[END_REF]. The Buchnera provides its host with essential amino acids and obtains nonessential amino acids from the host (van Hemden, 2007).

A. Wingless aphids B. Winged aphids

Agricultural importance of aphids

Aphid crop damage is among the most serious of agricultural and horticultural problems. Aphids cause damage mostly by feeding and transmitting viruses. For example, effects of aphid feeding and associated virus injury on grain crops in Australia resulted in potential economic costs of $241 and $482 million/year, respectively (Valenzuela and Hoffmann, 2015).

Aphid-feeding effects may remove plant sap to plant death, and through salivary secretion, they could manipulate the plant's physiological functions to their advantages (Figure 5). Over 200 aphid species are known to be virus vectors. Their saliva secretion is phytotoxic, causing opportunist plant diseases and make them powerfully prevalent vectors (van Hemden, 2007;[START_REF] Stern | Aphids[END_REF]. Aphids could develop rapid resistance to pesticides (Bass et al., 2014;[START_REF] Herron | Can resistance management strategies recover insecticide susceptibility in pests?: a case study with cotton aphid Aphis gossypii (Aphididae: Hemiptera) in Australian cotton[END_REF]. IPM of aphids aims to promote BCA and minimize the BCA effects on nontarget species. Strategies include cultural control methods, for example, decreasing ant populations, using ultraviolet-reflecting films to repel winged aphids, or interplanting pollen and nectar source plants among crop rows to promote natural enemies [START_REF] Sorensen | Chapter 8 -Aphids A2 -Resh, Vincent H. Encyclopedia of Insects[END_REF].

Natural enemies

Natural enemies of aphids are mainly predators and parasitoids. Predators include ladybird beetles (Coccinellidae), lacewings (Neuroptera), hoverflies (Syrphidae), gall midges (Cecidomyiidae), and predatory bugs (Anthocoridae). Parasitoids include wasps of the large family Aphidiidae and several genera of Aphelinidae (van Hemden, 2007).

Aphid parasitoids: biology and application in biological control

Insect parasitoids, their phytophagous hosts, and their host plants compose a significant proportion of the world's biodiversity (Hawkins, 1994). They represent one of the most critical and best-investigated groups because of their vital role in biocontrol as natural enemies of aphids [START_REF] Zikic | Host range patterning of parasitoid wasps Aphidiinae (Hymenoptera: Braconidae)[END_REF].

Parasitoids are parasite species whose larvae develop by feeding on the bodies of other arthropods, usually insects (its hosts) (Godfray 1994). Hymenoptera is by far the most speciesrich insect order concerning the number of parasitoids (La Salle & Gauld, 1992). Among them, the subfamily Aphidiinae includes more than 400 described species worldwide, all of them parasitizing aphids (Hemiptera: Aphididae; Sanchis et al., 2001;Petrović et al., 2014). This group is extensively studied due to its essential role in biological control of agricultural pests, e.g. Hawkins & Cornell (1994);de Conti et al. (2008). However, their identification remains problematic as several species within genera have high morphologic plasticity or are phylogenetically close, and consequently difficult to identify (Kavallieratos et al., 2001;Tomanović et al., 2003Tomanović et al., , 2007;;Stanković et al. 2015). Indeed, [START_REF] Derocles | Are generalist Aphidiinae (Hym. Braconidae) mostly cryptic species complexes?[END_REF] suggested aphid parasitoids are cryptic complex by comparing the morphology and the genetic distances based on COI gene sequences of various generalist parasitoids.

Parasitoid biology

The entire development of immature aphid parasitoids in the Aphidiinae and the Aphelinidae group occurs within the host aphid. Aphid parasitoids are considered in the middle of the "predator-parasite" spectrum because of their feeding mode shift during their life cycle. From egg to larvae, they adopt a parasitic mode by feeding on a live host. From larva to mummy stages, they take a predator mode by eating their host. During oviposition, the female lay eggs inside the aphid. The egg then hatches and get through three larval instars (O'Donnell 1987).

During the second instar, the larva spins its silk cocoon and turns into a pupa; during that period the cuticle of the aphid hardens and dried and leaves an exoskeleton called mummy (Quicke 1997). The parasitoid only kills the aphid host during its last larval instar by consuming all tissue inside the aphid. The emerging parasitoid adult cut a hole to escape from the mummy.

Upon emergence, the female parasitoid mates and starts to search for aphid hosts. They may attack aphids on the same patch or the same plant where they were emerged (Weisser and Völkl 1997). If host density is low, she may disperse in search of a new aphid colony. In most species, the females search for hosts within a few meters (Weisser and Völkl 1997;Langhof et al. 2005). However, some species may disperse over 100 km in a year (Cameron et al. 1981).

Aphid parasitoids locate potential hosts in responding to signals from host and host plants (Royer and Boivin 1999). These cues for host finding could be visual, sensory or volatiles.

Visual and volatile signals from plants induced by aphid feeding serve as long-range cues to locate aphid patches. Once an aphid colony has been located, the female aphid parasitoids adjust their level of exploitation based on several short-range cues associated with aphids such as sensory cues, color, or kairomones [START_REF] Powell | Strategies involved in the location of hosts by the parasitoid Aphidius ervi Haliday (Hymenoptera : Braconidae : Aphidiinae)[END_REF]. Aphid parasitoids show clear preferences towards specific aphid species and aphid instars, which is based on host quality (Barrette et al. 2009). Patch residence time depends on aphid colony quality such as the size (Pierre et al. 2003), the distance between potential resources (Tentelier et al. 2006) and the presence of competitors (Le Lann et al. 2011, Wajnberg 2006).

Life-cycle of juvenile parasitoids inside aphid hosts

The parasitoid wasp (in our example is Aphidius ervi) lay the egg in the haemocoel of the host aphids ( The larval midgut of the hymenopteran parasitoid Aphidius ervi transport nutrients from aphid organ to the haemocoel, provide most of the organic molecules necessary for rapid insect development, especially L-amino acids in general, and leucine [START_REF] Fiandra | Leucine transport by the larval midgut of the parasitoid Aphidius ervi (Hymenoptera)[END_REF].

A. B.

Co-evolution of parasitoids and aphid hosts

The Red Queen hypothesis (RQH) [START_REF] Van Valen | A new evolutionary law[END_REF] indicating that antagonist species would co-evolve in an arms race between consumer attack and prey defenses as counterresponses, was proved by several studies [START_REF] Agrawal | Insect Herbivores Drive Real-Time Ecological and Evolutionary Change in Plant Populations[END_REF]. For instance, plant-aphidparasitoid coevolve through their defense/virulence traits and specialize their strategies:

plant against pest and aphid against parasitoids [START_REF] Martinez | Specificity of Multi-Modal Aphid Defenses against Two Rival Parasitoids[END_REF]. The alternative RQH [START_REF] Lapchin | Asymmetry in host and parasitoid diffuse coevolution: when the red queen has to keep a finger in more than one pie[END_REF]Ibanez et al. 2012) state that the co-evolution is unequal within a pair of consumer -prey; the prey's defenses often cost expensive and require compromise, so the higher trophic species likely win the race. This characteristic, called asymmetric are also observed on the host-parasite (Dybdahl and Lively 1998) and plantpathogen pairs (Clay and Kover 1996).

Parasitoid suffers strong selection pressures from the resistance of aphid hosts. They strictly co-evolve with their hosts as they must face the full host immune response (Error! Reference source not found.). The host-parasitoid model hence provides the insight of species interactions at both molecular, ecological, and evolutionary levels.

The significance of parasitoid host specificity in biological control

The roles of parasitoids in biological control are well stated in the literature [START_REF] Boivin | Aphid parasitoids in biological control[END_REF][START_REF] Nega | Review on Concepts in Biological Control of Plant Pathogens[END_REF]van Emden and Harrington 2007). They are essential ecosystem service providers and mainly help to regulate pest populations (Godfray 1994;Godfray & Shimada, 1999).

Parasitoids are used widely in the BC because they could target specific host species [START_REF] Bass | Insecticide resistance in the peach potato aphid, Myzus persicae, Part 2: Metabolic mechanisms and host adaptation[END_REF]. However, the release of exotic parasitoids could increase the extinction risk for indigenous species [START_REF] Jervis | Insects as Natural Enemies: A Practical Perspective[END_REF]. As a result, both efficiency and risk of a potential BCA must be assessed before being released. These characteristics depend on host specificity of parasitoids. For example, specialist parasitoid agents are anticipated to be efficient in host use pattern, to be safe for the environment and to establish well in the context they are released following classical BC approach [START_REF] Gagic | The Effects of Aphid Traits on Parasitoid Host Use and Specialist Advantage[END_REF]Klinken 1999) (see more chapter 1.1.9).

Ecology of host specificity

The study of host specificity in model host-parasitoid models is important considering the ecological services provided by parasitoids as BCA (see chapter 1.1). Understanding of the ecological specialization of parasitoids provides a solid background for the design of BCA risk and efficiency assessments, and the prediction of impacts of the potential BCA on an ecosystems. In return, the study of host specificity plays a key role within the theme of ecological specialization, which is one of the fundamental concepts of evolutionary ecology and the most studied question in the XX th century (Sutherland et al. 2013). Aphid parasitoids co-evolve with their hosts, which in turn co-evolve with host plants because aphids themselves are plant parasites (see chapter 1. 2.3, Boivin 2012). The model plant-aphidparasitoid could shed light on how organisms interact and evolve, as well as the impacts of these interactions, e.g. bottom-up and top-down forces on ecosystems, which is also a fundamental question in ecology (Sutherland et al. 2013, see chapter 2.3).

Ecological specialization concept

Ecological niches are a set of biotic and abiotic conditions in which a species can persist and maintain stable population sizes [START_REF] Futuyma | The evolution of ecological specialisation[END_REF]Moreno 1988, Devictor 2009). Ecological specialization means the pattern of one species adaptation or resource utilization in its niche.

Ecological specialization holistically describes the 'niche breadth' (or 'niche width') of one species. This concept disentangles the roles of one species in interactions with its surrounding, answers questions like why and how one species fit its environment, what happens next in case of perturbation. Understanding of ecological specialization shed light on mechanisms by which communities shaped from collections of species assemble [START_REF] Mouillot | Is the abundance of species determined by their functional traits? A new method with a test using plant communities[END_REF]; to predict outcomes of organism responses threaten by environmental fluctuation (Wiens 2016); the direction of community shift and impacts of community shift on the ecosystem (Devictor et al. 2010a[START_REF] Nock | Functional Traits[END_REF].

The fundamental niche, as known as "potential specificity," represents the total multidimensional ecological space in which a species could persist [START_REF] Futuyma | The evolution of ecological specialisation[END_REF].

Potential specificity is determined by interactions between species genotype and environment (Poisot et al. 2012). The realized niche, as known as "realized specificity," is the ecological space in which a species persists [START_REF] Futuyma | The evolution of ecological specialisation[END_REF]. The realized specificity reflects the impact of ecology, chance events and history on potential specificity [START_REF] Bolnick | The ecology of individuals: incidence and implications of individual specialization[END_REF]Devictor et al. 2010;Poisot et al. 2012). These concepts in host specificity assessment correspond to different scales of these tests where laboratory tests give information of fundamental host range and field tests give information of realized host range (see chapter 1.4.4).

1.3.2.

Shades of ecological specialization: specialist vs. generalist species

The degree of specialization of one species, (as known as the specificity) is evaluated by its niche breadth, as known as or spectrum of resources they can use [START_REF] Futuyma | The evolution of ecological specialisation[END_REF] and niche relatedness (phylogenetical or geographical clusters) [START_REF] Jorge | An integrated framework to improve the concept of resource specialisation[END_REF]. A specialist occupies a narrow niche, and a generalist fills a large niche. As ecological niches are multidimensional, i.e. consisting of habitat, diet breadth, etc; the degree of specialization one species could be different at each dimension. For example, one parasitoid could be habitat specialist and host generalist (Vet and Dicke 1992). However, the concept of specialist and generalist is also relative and context-dependent. Comparing host specificity of a predator and a parasitoid as BCA, a predator is relatively generalist because it could feed on prey from different families, but a parasitoid attacks hosts from only one family [START_REF] Jervis | Insects as Natural Enemies: A Practical Perspective[END_REF]). Among predators, omnivores are considered more generalist than carnivores. Among parasitoids, the one attacks over 20 host species is a generalist in compare to the one attack only one host species [START_REF] Zikic | Host range patterning of parasitoid wasps Aphidiinae (Hymenoptera: Braconidae)[END_REF]. Therefore, the term host specialist/generalist in this study is applied in a pairwise comparison among species share same food items: (relative) specialists and

(relative) generalists. Specificity also depends on the measured dimensions such as habitat and patch. The habitat is the location of plant hosts on which suitable aphid hosts occur.

Similar to the definition of host specialist or generalist, habitat specialists exploit few habitats when generalists can detect and forage several [START_REF] Stilmant | Host specialization in habitat specialists and generalists[END_REF]). The patch is the location of aphid hosts on plant hosts. A patch generalist shows the same fitness in one patch or another, while a patch specialist shows similar fitness in its specific patch compare to others (Rosenzweig 1981). The specificity of each dimension could be different, e.g. one parasitoid could be: (1) host and habitat specialist, (2) host specialist but habitat generalist, (3) host generalist but habitat specialist and (4) host and habitat generalist (Vet and Dicke 1992).

Specialization can also be viewed at different levels of biological organization, e.g. among species in a community or individuals within populations. As such, the processes of specialization can involve the diversity of populations in different environments or the variety of genotypes within a population on same environment types (fig. 7Error! Reference source not found., Poisot et al. 2012).

The debate about specialist/generalist raises the need for re-defining these terms. Also, the measurement of ecological specialization should be clarified in specific contexts, e.g.

individual-or population-level. Given the multidimensional and context-depended characteristics, the definition, analyses, and evaluation of species specialization are hence indispensable and are indeed central stones of various studies (Devictor et al. 2010a;[START_REF] Dennis | The generalismspecialism debate: the role of generalists in the life and death of species[END_REF][START_REF] Loxdale | The 'generalism' debate: misinterpreting the term in the empirical literature focusing on dietary breadth in insects[END_REF]Krasnov et al. 2011;Straub et al. 2011). The relation between different degrees of multidimensional specificity of parasitoids is still unknown and could be interesting to study.

1.3.3.

The continuum of specialization patterns: specialist -generalist "The one who eats everything must not treat with contempt the one who does not, and the one who does not eat everything must not judge the one who does, for God has accepted them." Romans 14:3 | NIV |

In any network, both hypotheses of dominant generalists and dominant specialists exist and are supported by empirical evidence. Among those hypotheses, one could prevail over others depending on the ecological networks, and new evidence found. Moreover, the criteria of "specialist" or "generalists" is not clear due to three reasons. Firstly, the concepts of specialist or generalist are context-dependent and multidimensional (Loxdale, 2010). Secondly, in each dimension, there is indeed a continuous spectrum of the degree of specialization without clear cut between specialist/generalist [START_REF] Krakos | Generalist versus specialist pollination systems in 26 Oenothera (Onagraceae)[END_REF]. Thirdly, ecological specialization is not static but dynamic. Species could evolve through two directions under environmental pressures, specialism to become more specialists, and generalism to be more generalists. The situation raises the importance of host specificity study and the necessity of having clear, quantifiable criteria for being specialist or generalist and possible evolutionary tendency of specialism/generalism.

Efficiency vs. plasticity, specialist vs. generalist

To survive and adapt to a specific niche, one organism must possess the ability of exploit specific resources, which is called efficiency; and the flexibility to change according to the environment, called plasticity. There are different paradigms which predict how the two competencies evolve in specialists and generalists. Debate histories and evidence for specialization hypotheses are listed as following.

In the host-parasitoid network, the popular paradigm of "the jack-of-all-trades is master of none" assumes one species faces a trade-off between its ability to exploit a broad range of resources and its efficiency to use a specific resource [START_REF] May | Niche Overlap as a Function of Environmental Variability[END_REF]. In other terms, the 'trade-off' model forecasts generalists are less efficient but more flexible than specialists. The 'resource-breadth' paradigms assume the ability to exploit a broad range of resources supports the efficiency to use a specific resource [START_REF] Brown | On the Relationship between Abundance and Distribution of Species[END_REF]. The 'resource breadth' model predicts generalists are both more efficient and flexible than specialists. As a result, generalists are more competent and abundant because they have more choice of food in both quantity and species diversity. [START_REF] Krasnov | Ectoparasitic "jacks-of-all-trades": Relationship between abundance and host specificity in fleas (Siphonaptera) parasitic on small mammals[END_REF][START_REF] Williams | Niche breadth and geographical range: ecological compensation for geographical rarity in rainforest frogs[END_REF][START_REF] Rader | Isotopic niches support the resource breadth hypothesis[END_REF][START_REF] Hawro | Landscape structure and agricultural intensification are weak predictors of host range and parasitism rate of cereal aphids[END_REF]. Finally, the alternative hypothesis states evolution not necessarily involves trade-off [START_REF] Morand | Distribution and abundance of parasite nematodes: ecological specialisation, phylogenetic constraint or simply epidemiology?[END_REF] or "trade-off," and "resource-breadth" are context-dependent (Fry et al. 1996;[START_REF] Forister | Revisiting the evolution of ecological specialization, with emphasis on insect-plant interactions[END_REF][START_REF] Pinheiro | Trade-offs and resource breadth processes as drivers of performance and specificity in a host-parasite system: a new integrative hypothesis[END_REF]).

In the predator-prey network, "the rich get richer" paradigm suggest generalist predators are more abundant than specialists as they can optimize nutrient intake in reducing accumulation of toxic compounds [START_REF] Freeland | Strategies in Herbivory by Mammals -Role of Plant Secondary Compounds[END_REF][START_REF] Pulliam | Diet Optimization with Nutrient Constraints[END_REF][START_REF] Karban | Herbivore offense[END_REF][START_REF] Stohlgren | The rich get richer: patterns of plant invasions in the United States[END_REF][START_REF] Weise | The role of body size in individual-based foraging strategies of a top marine predator[END_REF]). The "body size" principle argues generalist consumers are at the lower abundance and rarer in the community because they are at higher trophic levels and eat hosts/preys of a broader range of body size [START_REF] Cohen | Body sizes of hosts and parasitoids in individual feeding relationships[END_REF]).

In the mutualistic networks, e.g. pollinators-plants, the "trade-off" between pollinator effectiveness and resource breadth prevail. Specialist pollinators are believed to be more efficient in their duty but more sensitive to environmental perturbation than generalist flower visitors (Larsson 2005). However, [START_REF] Ashworth | Why do pollination generalist and specialist plant species show similar reproductive susceptibility to habitat fragmentation?[END_REF] found evidence against this prediction that under habitat fragmentation, both generalists and specialist are similarly susceptible. Among pollinators, plant generalist pollinators have been believed to be more abundant (Raguso 2008). Recently in a review, [START_REF] Krakos | Generalist versus specialist pollination systems in 26 Oenothera (Onagraceae)[END_REF] found a continuum of specialists and generalists among flower visitors in 26 Oenothera taxa.

Who would win in nature and evolutionary races, specialists or generalists?

Overall, in the host-parasitoid network, the trade-off paradigm is more popular and widely accepted (Straub et al. 2011). The trade-off model based on arguments that specialist organisms physically and behaviorally adapt to few hosts, so they must be more efficient than generalists. The trade-off also means that specialist species can only tolerate a limited range of environmental conditions. Consequently, due to disturbance caused by climate change and human activities, specialists face a higher risk of extinction under environmental perturbation as they fail to switch hosts (MacKinney 1997;Devictor et al. 2008Devictor et al. , 2010;;[START_REF] Colles | Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches[END_REF][START_REF] Christian | More species, fewer specialists: 100 years of changes in community composition in an island biogeographical study[END_REF]Chacón and Heimpel 2010) and could be highly constrained by a heterogeneous habitat [START_REF] Gagic | The Effects of Aphid Traits on Parasitoid Host Use and Specialist Advantage[END_REF]. Under the weight of evidence of the evolutionary dead-end of specialists, specialist abundancy has nowadays considered an indicator of sustainability [START_REF] Fanelli | Range of Species Occupancy, Disturbance and Generalism: Applying Hemeroby Metrics to Common Breeding Birds from a Regional Atlas[END_REF]. In the classical BC, generalist species are thought to have several advantages over specialists such as establishing better in a new landscape, surviving in lowabundant resources, tolerating environmental stresses and thriving in a large number of habitats (Raymond et al. 2015). However, a recent meta-analysis proved that specialists establish in their native hosts more successfully than generalists even in a new environment [START_REF] Rossinelli | Higher establishment success in specialized parasitoids: support for the existence of trade-offs in the evolution of specialization[END_REF]. The results could be explained by the fact that even though generalists could exploit a more extensive range of resources, their adaptation to homogeneous habitats, such as monocultures, is not so easy [START_REF] Kassen | The experimental evolution of specialists, generalists, and the maintenance of diversity[END_REF]Duffy 2007). Specialism is claimed to be an evolutionary dead-end, or more positively their extinction gives rise to generalists [START_REF] Colles | Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches[END_REF][START_REF] Day | Is specialization an evolutionary dead end? Testing for differences in speciation, extinction and trait transition rates across diverse phylogenies of specialists and generalists[END_REF]). On the contrary, Loxdale et al. (2011) claim that generalism does not even exist because species must morphologically, behaviorally and genetically tolerate their niches under natural selection pressure; generalism is not favored in nature, or some generalist species are indeed cryptic or sequential specialists [START_REF] Derocles | Are generalist Aphidiinae (Hym. Braconidae) mostly cryptic species complexes?[END_REF][START_REF] Desneux | Cryptic species of parasitoids attacking the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in Asia: Binodoxys communis Gahan and Binodoxyx koreanus Stary sp. n. (Hymenoptera: Braconidae: Aphidiinae)[END_REF][START_REF] Joppa | Reciprocal specialization in ecological networks[END_REF][START_REF] Kaartinen | Revealing secret liaisons: DNA barcoding changes our understanding of food webs[END_REF][START_REF] Mitrovski-Bogdanović | Identification of Two Cryptic Species within the Praon abjectum Group (Hymenoptera: Braconidae: Aphidiinae) using Molecular Markers and Geometric Morphometrics[END_REF]. Combined those ideas, [START_REF] Dennis | The generalismspecialism debate: the role of generalists in the life and death of species[END_REF] argued specialism be driven by environmental fragmentation and generalism by heterogeneity. The two main forces affecting specialization are fundamental biological constraints and the covariance between genes and environment (from Poisot et al. 2011).

Interestingly
Generalization may also occur at various levels. [START_REF] Bolnick | The ecology of individuals: incidence and implications of individual specialization[END_REF] Overall, phylogenetic data prove that theory based on pure genetic trade-offs in host use not enough to explain the evolutionary picture. Multitrophic interactions are the necessary framework for understanding specialization that reveals the bidirectionality in transitions between generalist and specialist lineages [START_REF] Forister | Revisiting the evolution of ecological specialization, with emphasis on insect-plant interactions[END_REF].

How to evaluate the host specificity of aphid parasitoids?

Here we present terms related to host specialization of one parasitoid by [START_REF] Klinken | Host specificity testing: Why do we do it and how we can do it better. Host specificity testing of exotic Arthropod Biological Control Agents -The biological basis for improvement in safety from Forest Health Technology Entreprise Team in[END_REF]  Host: suitable aphid for the reproduction of a parasitoid  Host range: the sum of all hosts  Host range breadth: host range, counting on taxonomy diversity among those hosts  Host specificity: = host range breadth x host relative acceptability (and/or) suitability Host specificity could be evaluated under different dimensions (Figure 8), first of all, is evaluated by the number of aphids one parasitoid can attack and develop on [START_REF] Stary | On the Strategy, Tactics and Trends of Host Specificity Evolution in Aphid Parasitoids (Hymenoptera, Aphidiidae)[END_REF].

For example, the Aphidiinae subfamily comprises numerous specialist species parasitizing few aphid hosts, but some generalists can parasitize dozens of aphid species (Kavallieratos et al., 2004;Starý 2006;Tomanović et al., 2009;Benelli et al., 2014).

Figure 8. Multi-dimensions of the host specificity

The definition of host specificity is broadened to consider the phylogenetical distance between aphid hosts, as the phylogenetically broader host ranges (Error! Reference source not found.) (Poulin and Mouillot 2005). Moreover, the field host ranges are also reflected parasitoid behavioral and physiological traits. Parasitoid behavioral traits (preference) are subsequent actions leading to host acceptance or rejection and measured by parameters such as the oviposition rate or preference index (Cock, 1978). Physiological host range (performance) are the number and taxonomy diversity of species that the agent could complete development on if attacked. Parasitoids are proved to show a preference for some hosts, regardless of host availability or their performance on these hosts. The performance on aphid hosts, e.g. survival rate, parasitism rate, emergent rate, sex ratio, offspring size [START_REF] Jervis | Insects as Natural Enemies: A Practical Perspective[END_REF]) could reflect the host quality for parasitoid development. Both these behavioral and physiological traits could determine parasitoid population on a specific host species and therefore their specificity toward hosts (Error! Reference source not found.) [START_REF] Klinken | Host specificity testing: Why do we do it and how we can do it better. Host specificity testing of exotic Arthropod Biological Control Agents -The biological basis for improvement in safety from Forest Health Technology Entreprise Team in[END_REF].

Host specificity index

Host specificity index for parasite-host interaction

In a review of host specificity indexes, [START_REF] Skoracka | Measuring the host specificity of plant-feeding mites based on field data -a case study of the Aceria species[END_REF] identified two host specificity indices as valuable to evaluate the fundamental host specialization, which is the taxonomic index of specificity (Poulin and Mouillot 2005) and the Rohde index [START_REF] Rohde | How to measure ecological host specificity[END_REF]) as listed below.

Taxonomic index of specificity (Poulin & Mouillot 2005):

where: STD*staxonomic index of specificity of species s, ωij -taxonomic distinctness between host species i and j (the number of taxonomic steps required to reach a node common to both), Psi, Psj -prevalence (the frequency of hosts that are parasitized) of species s on host species i and j, respectively.

This index measures the average taxonomic distinctness of all host species used by a given parasitoid species. The value of this index is inversely proportional to specificity:

the greater the taxonomic distinctness between host species, the higher the values of the index.

Rohde index of specificity [START_REF] Rohde | How to measure ecological host specificity[END_REF]):

where: Ss -Rohde index of specificity of species s, h -number of all examined host species, Psi -mean prevalence of species s on i th host, rsi -rank of host species i (the species with the highest prevalence has rank 1).

This index considers the uneven distribution of parasites across different hosts. In the numerator of this index, prevalence is weighted by the inverse rank (hosts which are less used contribute less to the sum). Thus, the value of the index is more stable and less affected by accidental or ephemeral occurrences of parasite species. The higher the value of this index, the higher the host specificity. The Rohde index allows evaluating relative host prevalence and compares the specialization level between parasitic species encountering different host ranges, either by experiments, and either by geographical observations. [START_REF] Rohde | How to measure ecological host specificity[END_REF].

The two indices reflect different dimensions of the specificity concept. The taxonomy index of specificity for one parasite species is calculated primarily by the taxonomic distinctness among hosts in considering the prevalence of the parasite in these different hosts (Poulin and Mouillot 2005). It thus accords to the most widely accepted definition of the "host specificity" concept [START_REF] Skoracka | Measuring the host specificity of plant-feeding mites based on field data -a case study of the Aceria species[END_REF]. The Rhode index is measured by the prevalence of the parasites but not the phylogenetic difference among hosts [START_REF] Rohde | How to measure ecological host specificity[END_REF]. It could be a complement to the taxonomy index in case the tested hosts are phylogenetically close, e.g. aphid hosts on the same subfamily have the same taxonomic distinctness values so the taxonomic index could be similar.

1.4.2.

Host specificity specter of Aphidiinae parasitoids [START_REF] Zikic | Host range patterning of parasitoid wasps Aphidiinae (Hymenoptera: Braconidae)[END_REF] develop from the classification of Aphidiidae host specificity groups (Starý, 1981a) to a spectrum of host specificity of Aphidiinae parasitoids, which mostly relies on aphid phylogeny and phylogenetic relations among aphid hosts (Error! Reference source not found., Error! Reference source not found.3). The spectre is: 1) monophagous: a single host species, (2) narrow oligophagous: two or more species of the same aphid genus, (3) moderate oligophagous: species of two or more genera of the same aphid subfamily, (4) broad oligophagous: species of two or more genera of two or more subfamilies of the same aphid family, ( 5) polyphagous: species of several genera of two or more aphid families. [START_REF] Zikic | Host range patterning of parasitoid wasps Aphidiinae (Hymenoptera: Braconidae)[END_REF]).

A 1 1 1 1-1-1 B 1-12 1-2 1 4-1-1 C 2-11 1-4 1-2 3-2-1 D 5-
The study of [START_REF] Zikic | Host range patterning of parasitoid wasps Aphidiinae (Hymenoptera: Braconidae)[END_REF] provides criteria to classify aphid parasitoids by their host ranges, which now remains challenging due to high specificity of parasitoids.

1.4.3.

The optimal foraging behavior: correlation preference-performance.

The parasitism process includes several steps from host finding until successful adult emergence (Desneux et al. 2009a[START_REF] Desneux | Cryptic species of parasitoids attacking the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in Asia: Binodoxys communis Gahan and Binodoxyx koreanus Stary sp. n. (Hymenoptera: Braconidae: Aphidiinae)[END_REF] (Vet and Dicke 1992). The second step is host evaluation, when the female encounters the potential host, evaluates it with antennae and ovipositor probing. The cues for host evaluation could be host color, shape, and texture, chemical and sensory signals [START_REF] Rehman | Host selection behaviour of aphid parasitoids (Aphidiidae: Hymenoptera)[END_REF]. If an aphid is accepted as a host, the female parasitoid will decide to oviposit and deposit an egg at the third step of host acceptance. In the case of Aphelinidae family, the parasitoid will determine to feed or oviposit on hosts. Sometimes aphid movements or defense could trigger the attack of parasitoid (Desneux et al. 2009a[START_REF] Desneux | Cryptic species of parasitoids attacking the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in Asia: Binodoxys communis Gahan and Binodoxyx koreanus Stary sp. n. (Hymenoptera: Braconidae: Aphidiinae)[END_REF], figure 12Error! Reference source not found.).

Host detection -recognition

Host acceptance Successful sting The success in the control of a pest is dependent upon parasitoid behavior of host selection and their host suitability. Overall, the 'optimal foraging strategy' stands as a central paradigm of host selection pattern (Jaenike 1978). This hypothesis states that "mothers know best" -females try making best choices for the sake of their offspring -and is applied to multidimensions of specialization. The optimal foraging pattern is determined by the correlation between parasitoid preference and performance (Desneux et al. 2009a). The correlation preference-performance could be a criterion of effective BCA because it proves that parasitoids have a good host selection capacity, which is essential in BCA assessment. For example, in classical BC, parasitoids with the optimal foraging will tend to have the preference on targeted aphids (which are high in density) will lead to higher suppression of the pest and success in biological control. However, on augmentative BC, parasitoid host choice of hosts to maximize offspring fitness will lead to the refusal of small size aphids and the patch leave before the pest has been suppressed to the desired level [START_REF] Mills | Optimal Foraging Behavior and Efficient Biological Control Methods[END_REF].

The pattern of the correlation of preference (adult oviposition) -performance (of offsprings)

is not universal in all parasitic species such as aphids or parasitoids which means that other factors than mere host quality could drive parasitoid behaviors. There are examples of no correlation (Chesnais et al. 2015;[START_REF] Rivero | The costs and benefits of host feeding in parasitoids[END_REF] or positive one (e.g. [START_REF] Singer | Heritability of Oviposition Preference and Its Relationship to Offspring Performance within a Single Insect Population[END_REF][START_REF] Ode | Oviposition vs. offspring fitness in Aphidius colemani parasitizing different aphid species[END_REF]Desneux et al. 2009a;[START_REF] Moiroux | Temperature influences host instar selection in an aphid parasitoid: support for the relative fitness rule[END_REF] or both in one study [START_REF] Mayhew | Adaptive patterns of host-plant selection by phytophagous insects[END_REF]. This non-conclusive correlation is shaped by behavioral strategies of specialists/generalists, as specialists are behaviorally more selective than generalists (Gripenberg et al. 2010;Thompson 1988a;b). This non-correlation could also be determined by food quality, i.e. when food quality is low, the female might be less choosiness [START_REF] Karban | Herbivore offense[END_REF][START_REF] Price | Insect herbivore population dynamics on trees and shrubs : new approaches relevant to latent and eruptive species and life table development[END_REF]). Another reason for the non-correlation is the capacity of host selecting, as specialists are more efficient in evaluating hosts than generalists (Straub 2011).

The host specificity testing process in biological control

The host specificity testing scheme of a BCA (Error! Reference source not found.) is now mandatory in BC industry and regulatory schemes. The assessment occurs at various scales (1) small area no-choice laboratory test (one parasitoid -one test species at a time; naïve females); ( 2) large arena choice test (one female -two or more species at a time, simultaneously or sequentially); (3) field test (release natural enemies in a non-target habitat with non-target species) (van [START_REF] Lenteren | Host range testing[END_REF][START_REF] Sands | Guidelines for testing host specificity of agents for biological control of arthropod pests[END_REF]. The BCA host specificity must be tested at the laboratory, greenhouse and field scales on both preference and performance on a wide range of aphid hosts including non-target and indigenous aphids. Only when the non-target impacts of the BCA are low, or the benefice outweighs the damage on nontargeted species that the BCA is recommended. The no-choice assays in step 1 provide information on the parasitoid fundamental host range as well as its behaviors when encountering aphid hosts. On the choice assays in step 2, the info shows learning mechanisms of parasitoids. In complementary by the understanding of a specific environment of applying the agent, the test results help to predict post-release outcomes such as the realized host range, the preference, the non-targeted hosts, and the ability of host switching (van Lenteren 2010, figure 14). NT stands for non-targeted species Figure 15. The comparison between fundamental host range tested in the laboratory and the realized host range in the field (Klinken 1999).

Among those steps, laboratory host specificity testing, which estimates the physiological host range of a BCA (Error! Reference source not found.5) provides perhaps the most crucial evidence used to predict post-release host range, i.e. the ecological host range within the region of importation. However, given the physiological host range can include species that are not preferred but are suitable to complete development for the agent; the laboratory test can overestimate the agent's field host range and misinterpret its arranged risk/benefit. (Gilbert and Webb, 2007;Pemberton, 2000;Van Driesche and Reardon 2004;van Lenteren et al., 2006[START_REF] Haye | Does fundamental host range match ecological host range? A retrospective case study of a Lygus plant bug parasitoid[END_REF]. The host distribution, the lack of experience or the host preference and host density could also result in the difference between realized host range and the fundamental host range (Klinken 1999).

The host specificity testing outcomes occupy both description and assay roles. In one hand, the outcomes describe the parasitoid intrinsic host specificity, particularly the fundamental host range, the host preference ranking, the relative host preference/performance and their learning ability. In the other hand, parasitoid field efficiency, i.e. their field host range and behaviors could be predicted from the testing outcomes given information of the ecosystem such as plant and host density, plant and host quality, and abiotic factors (Klinken 1999, Error! Reference source not found.6).

Figure 16. The implication of host specificity testing in biological control (Klinken 1999).

Chapter 2.

Bottom-up and top-down forces in ecological network

Ecological networks and interactions

Ecological networks are composed of the nexus of interactions among organisms. Ecological networks can be subdivided into three broad types: 'traditional' food webs, mutualistic networks and host-parasitoid networks (Ings et al. 2009[START_REF] Hagen | Biodiversity, Species Interactions and Ecological Networks in a Fragmented World[END_REF]. Traditional food webs consist of trophic interactions (who eat who, i.e. predator-prey and primary consumerbasal resource relationship) and are backbones of an ecosystem (Hall & Raffaelli 1993). Hostparasitoid networks also contain trophic interactions. However, they concentrate on the particular types of feeding relationships between parasitoids and their hosts. Parasitoids are insects that lay eggs on or in the body of other insects, their hosts (Godfray and Shimada 1999). When the egg hatch, the larva consumes its hosts either immediately or after a delay during which the hosts are still alive. In the early stage, larva parasitoid has a close relationship to its host, similarly to parasitism. Finally, they always kill their hosts by feeding equally to predation. Mutualistic networks are non-consume networks. Three mutualistic networks receiving particular attention are (1) pollination between plants-pollinators, ( 2) frugivore networks between plants-seed dispensers, (3) ants-plants (Ings et al. 2009). Besides trophic interactions, non-trophic interactions also play significant roles in the composition and stability of an ecological network [START_REF] Muller | Predators and mutualists influence the exclusion of aphid species from natural communities[END_REF][START_REF] Charles | Parasitoids[END_REF]van Veen et al. 2006;[START_REF] Sanders | Indirect commensalism promotes persistence of secondary consumer species[END_REF][START_REF] Terborgh | Toward a trophic theory of species diversity[END_REF][START_REF] Frost | Apparent competition drives community-wide parasitism rates and changes in host abundance across ecosystem boundaries[END_REF][START_REF] Mougi | The roles of amensalistic and commensalistic interactions in large ecological network stability[END_REF].

Interactions are the interplay of organisms with these biotic and abiotic factors. [START_REF] Olff | Parallel ecological networks in ecosystems[END_REF] classify six main types of interactions in ecosystems. They are:

- 2) microbial detrivores and (3) consumers at higher trophic levels (from [START_REF] Olff | Parallel ecological networks in ecosystems[END_REF].

(1) consumer-resource interactions, - (2
Ecological interactions may be characterized according to parameters such as consume or nonconsume, positive or negative/antagonistic effects on other organisms, reciprocal or unilateral, direct or indirect, obligatory or facultative, intraspecific or interspecific (Table 4).

Annex 1. A summary of direct and indirect interactions (adapted from [START_REF] Olff | Parallel ecological networks in ecosystems[END_REF], Han Peng Ph.D. thesis 2014).

Sub-types of interaction Effects on other organisms Examples References

Consume-resource

Trophic cascades (higher trophic consumers suppress the abundance or alter the behavior of their prey, thereby releasing the next lower trophic level from their consumers)

-positive -indirect -unilateral Carpenter et al. 2008 In an ecosystem, forces are factors that have the power to affect the interactions and characteristics, e.g. population, the behavior of other species. Depending on their influences, forces could be driven, organizational or structural. Bottom-up forces are the influence of organisms at the lower trophic level, e.g. soil conditions or resources, to higher trophic forms (consumers). Top-down forces are the influence of higher trophic forms to lower trophic forms. For example, the predation has the force to control or suppress herbivore's population and imply cascade impact on plants, as they create a "free enemy space" for plants. Ecological interactions are also characterized by the direction of the forces.

One of the critical issues of a network study is to measure the strength of forces and interactions controlling network's structure, which are essential in applying such as BC or conservation [START_REF] Agrawal | Filling key gaps in population and community ecology[END_REF][START_REF] Evans | Biodiversity, ecosystem functioning, and classical biological control[END_REF]. Among six types of interaction, the external forcing of abiotic factors has not yet fully mentioned in the study of ecological networks [START_REF] Olff | Parallel ecological networks in ecosystems[END_REF]). However, changing environment could disrupt an ecological network through interactions, e.g. mediated by plants [START_REF] Power | Top-down and Bottom-up Forces in Food Webs -Do Plants Have Primacy[END_REF]. In reverse, ecological interactions could alleviate or aggravate the forces. The context such as species density and distribution, intraand inter-competition, e.g. sharing hosts/prey, superparasitism or indirect interactions influence or even reverse the outcomes of forces. For instance, mutualism, i.e. rhizobacteria and plants could buffer impacts of environmental stresses across multi-trophic levels [START_REF] Lescano | Bottom-up effects may not reach the top: the influence of ant-aphid interactions on the spread of soil disturbances through trophic chains[END_REF][START_REF] Marquis | Insect mutualisms buffer warming effects on multiple trophic levels[END_REF]) and drive the outcomes of trophic cascades [START_REF] Morales | Allee dynamics generated by protection mutualisms can drive oscillations in trophic cascades[END_REF]. Antagonism could evolve to mutualism under tolerance strategy of the lower trophic level, if the antagonistic risk is weak and the cost of tolerance is acceptable (for example the ant-aphid interactions (Oliver et al. 2009). The reverse of mutualism becoming antagonism also happens, e.g. among aphids and their facultative bacterial symbionts [START_REF] Zytynska | The natural occurrence of secondary bacterial symbionts in aphids[END_REF].

Ecologists measure interaction strengths by different parameters of (1) an individual link, e.g. specific maximum feeding rates, biomass flow along on a link, or (2) the impact of a change in the properties of one link or of a set of links, e.g. all links to and from a given species, on the dynamics of other species or on the functioning of the whole system [START_REF] Olff | Parallel ecological networks in ecosystems[END_REF]). On the host-parasitoid networks, one parameter measures the strength of parasitism is the frequency of hosts that are parasitized called parasite prevalence (Berlow et al. 2004).

Bottom-up versus top-down forces

Among the dominant forces which influence the structure of an ecological network, bottomup and top-down process are two primary control forces. In a bottom-up process, resources provide energy flow for the ecosystem against trophic levels. In a top-down process, consumers determine the distribution of energy flow at each trophic level [START_REF] Montoya | Ecological networks and their fragility[END_REF]Bukovinszky et al. 2008). Like the debate specialist/generalist, the debate of which forces control an ecological network, the bottom-up or top-down ones also endure in ecology.

Substantial evidence supports both hypotheses, and no model entirely fit observation. The 'bottom-up' hypothesis states resources are primary control from bottom-up because resources are limited [START_REF] Lindeman | The Trophic-Dynamic Aspect of Ecology[END_REF][START_REF] Mcqueen | Trophic Relationships in Fresh-Water Pelagic Ecosystems[END_REF][START_REF] Montoya | Species' response patterns to habitat fragmentation: do trees support the extinction threshold hypothesis?[END_REF]. Plants have apparent primacy in food webs; their primary productivity is a fundamental control of higher trophic levels. Other plant attributes, such as architecture (e.g. Bernays and Graham 1988;Kareiva and Sahakian 1990) or chemical constituents (e.g. [START_REF] Price | Interactions Among Three Trophic Levels: Influence of Plants on Interactions Between Insect Herbivores and Natural Enemies[END_REF]Price and Clancy 1986) also have substantial effects on the performances and interactions of higher trophic levels. These other attributes, however, are often molded or constrained by plant growth rates, in either physiological or evolutionary time (Bloom et al. 1985;Coley et al. 1985;Oksanen 1990;[START_REF] Power | Top-down and Bottom-up Forces in Food Webs -Do Plants Have Primacy[END_REF]. 'Top-down' hypothesis states consumers at the top of trophic levels dominantly shape the network structure through regulation of plant consumers [START_REF] Hairston | Community Structure, Population Control, and Competition[END_REF][START_REF] Menge | Species-Diversity Gradients -Synthesis of Roles of Predation, Competition, and Temporal Heterogeneity[END_REF][START_REF] Sanders | The loss of indirect interactions leads to cascading extinctions of carnivores[END_REF]. Invasive species could also control a new ecosystem through top-down forcing. Exotic species are favorized by the absence of their traditional enemies as stated the 'enemy release hypothesis' (Keane and Crawley,2002) and/or their novice defensive chemistry -the 'novel weapons hypothesis' [START_REF] Callaway | Novel weapons: invasive success and the evolution of increased competitive ability[END_REF]. Once successfully integrating into the network, they could shift their host range and the community structure [START_REF] Harvey | Interactions between invasive plants and insect herbivores: A plea for a multitrophic perspective[END_REF]). The "exploitation ecosystems" hypothesis emphasizes on context-dependence of the bottom-up and top-down processes as control forces [START_REF] Oksanen | The Logic and Realism of the Hypothesis of Exploitation Ecosystems[END_REF], e.g. the resource availability.

Bottom-up forces prevail in the ecosystem if resource deficiency is important. Given adequate resources, top-down predators control herbivore populations thus indirectly support plant productivity (Hunter and Price 1992). The strength of forces will weaken along food chains or when resources are opulent [START_REF] Mcqueen | Trophic Relationships in Fresh-Water Pelagic Ecosystems[END_REF][START_REF] Terborgh | Toward a trophic theory of species diversity[END_REF]. The dominant forces also depend on the community, i.e. above-or underground networks. In a forest ecosystem, [START_REF] Schuldt | Belowground top-down and aboveground bottom-up effects structure multitrophic community relationships in a biodiverse forest[END_REF] found a significant top-down effect of the below-ground community (pathogens, symbionts, decomposers), which, in their turn, imply a strong bottom-up effect on aboveground species (herbivores, predators, parasites), the all mediated by the plant. On the contrary, abiotic factors had a strong plant-mediated bottom-effects on the aboveground community but not on the belowground one. Overall, these theories seem to complement mutually but not exclusive [START_REF] Hunter | Estimating the relative roles of topdown and bottom-up forces on insect herbivore populations: A classic study revisited[END_REF]. Further meta-analysis in the subject could be realized to compare between ecosystems and give hints about the control forces. Moreover, plants could change parasitoid behaviors as their volatiles and color served as cues for host location [START_REF] Kaplan | Trophic Complexity and the Adaptive Value of Damage-Induced Plant Volatiles[END_REF][START_REF] Zepeda-Paulo | Adaptive evolution of a generalist parasitoid: implications for the effectiveness of biological control agents[END_REF]. Plant toxins could indirectly harm to parasitoids if they are sequestered by aphids (Ibanez et al. 2012). The presence of plant mutualists, e.g. soil arbuscular mycorrhizal fungi, combined with aphid mutualists, can have subtle -but significant -effects on plant fitness and insect success. The evidence is the counteract of two mutualist systems -soil fungi and aphid endosymbiont in a tri-trophic plant Solanum -aphid Macrosiphum euphorbiae -parasitoid Aphidius ervi could both benefit and harm to parasitoids [START_REF] Bennett | Plant and insect microbial symbionts alter the outcome of plant-herbivore-parasitoid interactions: implications for invaded, agricultural and natural systems[END_REF]Martinez et al. 2014;McLean and Godfray 2017;[START_REF] Sanders | Defensive insect symbiont leads to cascading extinctions and community collapse[END_REF].

Plant defensive strategies and possible mechanisms

Under constraint conditions, each species can resist, tolerate or avoid stress. While resistance refers to traits that reduce the amount of damage, tolerance refers to traits that reduce the impact of damage to species fitness. Several paradigms are proposed to explain and predict the plant "choice" of defensive strategies under specific circumstances. The "biochemical coevolution theory" of Ehrlich and Raven (1964) states one plant family acquire a complex of defenses that exclude all but specialist herbivores. The "plant apparency theory" (Feeny 1976) hypotheses that when the risk of herbivory is high, i.e. plants are apparent to herbivores), plants invest on quantitative defenses such as expensive constitutive toxins that are effective against all generalist as specialist herbivores. Unapparent plants should invest in less-costly toxins (qualitative, induced) that are effective to most herbivores except specialists (Error!

Reference source not found.20). Regarding the trade-off plant nutritional quality vs. defense, the "resource availability theory" (Coley 1985) predicts that fast growing plants on abundant nutrient soils should invest less in defenses because the damage costs of herbivory are low and plant loss is less important. The "growth-defense trade-off" states that high resource investment in defenses means lower resource availability for growth and higher herbivory resistance. The 'slow-growth-high-mortality' SG-HM hypotheses that plants repulsive shields, e.g. tannins, fiber, and toughness, which only delay the development but do not kill herbivores, are useful only when plants interact with the third trophic level. Indeed, the slower growth of herbivores exposes them more to natural enemies, which increase their probability to be parasitized or eaten (Benrey and Denno 1997). Plant tolerance strategies include exible rates of photosynthesis and nutrient uptake, and plasticity in allocation patterns and developmental rates (Nunez-Farfan 2007). Arrow size: the probable strength of the effect; the double-headed arrows: the co-evolution.

+ or signs: posi ve or nega ve e ects of plant toxins on higher trophic levels, respec vely" (From Ibanez et al. 2012).

How could aphid traits mediate bottom-up and top-down forces?

Effects of multiple aphid traits on parasitoid specialization were demonstrated in the review of [START_REF] Gagic | The Effects of Aphid Traits on Parasitoid Host Use and Specialist Advantage[END_REF]. Firstly, parasitoids rely on cues from aphid hosts to locate them [START_REF] Rehman | Host selection behaviour of aphid parasitoids (Aphidiidae: Hymenoptera)[END_REF]. Those cues could be aphid odors like alarm signaling pheromones or kairomones (Outreman et al. 2010). In one study, Aphidius ervi refused wet aphid hosts, which could result from the parasitoids being unable to detect the host kairomones [START_REF] Weinbrenner | Oviposition behaviour of the aphid parasitoid, Aphidius ervi: Are wet aphids recognized as host?[END_REF]. Female A. ervi were found to show active oviposition attempts to object with the color similar to those reflected by its primary host, the aphid Acyrthosiphon pisum (Battaglia et al. 2000). Aphid texture, shape and aphid body liquid are evaluated by parasitoid antennal and ovipositor probing [START_REF] Rehman | Host selection behaviour of aphid parasitoids (Aphidiidae: Hymenoptera)[END_REF]. Secondly, aphids are both food resource and developmental environment of parasitoids. The host nutritional quality could be constraints for parasitoid survival. Female's diet might impact the fitness of their juvenile offspring [START_REF] Martinez-Ramirez | Nutrient uptake and allocation capacity during immature development determine reproductive capacity in Diachasmimorpha longicaudata (Hymenoptera: Braconidae: Opiinae), a parasitoid of tephritid flies[END_REF]. A. ervi offspring performance depends on host nutritional quality (Sequeira and Mackauer 1992). Host body size [START_REF] Cohen | Body sizes of hosts and parasitoids in individual feeding relationships[END_REF] and host ages [START_REF] Trotta | Plastic responses of some life history traits and cellular components of body size in Aphidius ervi as related to the age of its host Acyrthosiphon pisum[END_REF] correlates with parasitoid body size, as parasitoid larval development is restricted by limited developmental volumes of aphid hosts, so do their adult sizes.

Aphid defense/counterdefenses -In the tri-trophic system, aphids must multilaterally defend against parasitism and counter-defend against plant immune system for their feeding. The

Figure 19. Aphid immunity interactions

Aphid immunity interaction with the host plant, the primary and secondary symbionts, as well as the pathogens or parasitoids [START_REF] Poirie | The evolutionary ecology of aphid immunity[END_REF].

2.3.3.

How abiotic stresses level-up to parasitoids through the tri-trophic interaction?

In the field, plants simultaneously face several stressors such as combined abiotic stresses (e.g. drought and heat, drought and cold), combined biotic stresses (e.g. leaf-chewing and sap-feeding insects), or combined abiotic and biotic stresses (e.g. drought and herbivores).

The response of plants to stress combinations is unique and cannot be directly estimated from the impacts of each stress (Suzuki et al. 2014). Overall, when facing combined stresses plants could have one of three strategies: (1) well-developed tolerance and poor defense, (2) welldeveloped defense and poor tolerance, or (3) something between these two extremes (van der Meijden et al. 1988;[START_REF] Cipollini | Costs of Resistance in Plants: From Theory to Evidence[END_REF].

The herbivore fitness (Price 1991, Huberty andDenno 2004). At the same time, the hardened structure of plants, the stomatal closure or the increase of plant trichomes under stress may cause difficulty for herbivores in foraging [START_REF] Couture | Elevated temperature and periodic water stress alter growth and quality of common milkweed (Asclepias syriaca) and monarch (Danaus plexippus) larval performance[END_REF]. In term of plant immune system, the exposure to mild drought could activate the plant induced defenses such as trehalose and abscisic acid (ABA). Both regulators can increase the pathogen resistance of plants [START_REF] Ramegowda | The interactive effects of simultaneous biotic and abiotic stresses on plants: Mechanistic understanding from drought and pathogen combination[END_REF]. Nevertheless, the trade-off between droughttolerance and defense in the mustard lead to a decrease in levels of glucosinolate toxins function in defense against generalist herbivores [START_REF] Alsdurf | Drought-induced transgenerational tradeoff between stress tolerance and defence: consequences for range limits?[END_REF]) and potentially reduce the mortality rate of natural enemies feeding those herbivores. Overall, one external force of abiotic stresses could change the interactions and the efficiency of each organism. The strength and result of abiotic bottom-up forces could be different to each plant-aphidparasitoid complex.As a conclusion, organism traits that influence interactions and might be influence by bottom-up forces in a tritrophic plant-aphid-parasitoid system are:

-Plant traits include species, nutritional quality, defenses against herbivores, mutualism with soil bacteria or fungi.

-Aphid traits include species, nutritional quality, defenses against parasitoids and counterdefenses against plants, mutualism with bacterial symbionts.

-Parasitoid traits include species, states (egg load and age), food resources, and counterdefenses against aphids (figure 23). (1) In host generalist parasitoids, there is no correlation between their preference for and performance on aphid hosts. The correlation and host specificity index could be combined to find a cut between specialist and generalist parasitoids.

(2) The preference and performance of parasitoids could be impacted both negatively and positively by bottom-up effects of abiotic factors, depending on the plant-aphid complexes.

(3) Host specificity could modify in both direction: parasitoids could become either more generalist or more specialist. Chapter 4.

Aphid-parasitoid host specificity

The choice of one or an assemblage of BCA against pests based on their host range is crucial as it determines the BCA's efficiency. In classical and augmentative BC strategies, host specialist BCA is preferred as they attack and achieve high performance on targeted pests; they promise to be more efficient and do not attack non-targeted species comparing to shared-host generalists. The thriving questions are where the cut is being specialist or generalist and how to evaluate the host range of a BCA.

Two approaches are available to evaluate the host range of a potential BCA and complete each other: the laboratory host range testing and the observations from the field (Van Driesche and Reardon, 2004). The laboratory approach describes the 'fundamental host range' of each parasitoid genotype/phenotype at small scales, which often overestimate the real host range or 'field host range' observed in the field (Klinken 1999). The field host range reflects the realized host range under particular environmental conditions at significant scale.

However, field host ranges could be the sum of host ranges of different biotypes of one species due to the misidentification of both parasitoids and their associated hosts. The reasons could be (1) parasitoids have high plasticity; they can adapt their performance, morphology and behavior to their niche (Zepeda-Paulo et al. 2013) and ( 2) parasitoid populations could be composed of cryptic or sub-species species [START_REF] Derocles | Are generalist Aphidiinae (Hym. Braconidae) mostly cryptic species complexes?[END_REF]. The field host range could also miss some host species due to technical problems, i.e. sample collections (Van Driesche and Reardon, 2004).

Furthermore, to approach the reality, the information of the classical parasitoid host range (the number of aphid hosts) should be accompanied by information such as the host taxa closeness, the parasitoid behavioral decision during host selection process (including search and oviposition on host) and the performance of parasitoids (the suitability of aphid hosts for parasitoid larval development). All these characteristics shape parasitoid host specificity.

These parameters might be estimated through the calculation of the host specificity index and the analysis or the preference-performance relationship.

We calculated two specificity indexes: the taxonomic specificity index (STD*) (Poulin and Mouillot 2005) and the Rhode indexes of specificity (SS) (Rhode and Rhode, 2008) (see chapter 1.1.1) to compare the value. As STD* are more sensible to the taxonomic distance among hosts and SS are more sensible to parasitism rates, the two indexes could provide a hint of where and when should an index be applied and the pros/cons of each index.

The behavior of parasitoids (so-called preference, i.e. deciding for host oviposition)

determines the successful implementation of a BCA [START_REF] Mills | Optimal Foraging Behavior and Efficient Biological Control Methods[END_REF]. The host suitability for larval parasitoid (so-called performance) also plays a crucial role. The optimal foraging hypothesis (Jaenike 1978) states that parasitoids tend to oviposit on most suitable hosts for their offspring. Indeed, Desneux et al. (2009a) proved that parasitoid preference positively correlates with its performance on one host in the case of a specialist parasitoid.

Our question is whether such correlation exists for host generalist parasitoids. Does the

Biological materials -parasitoids

Aphidiinae parasitoids comprise numerous specialist species, but some generalists can parasitize dozens of aphid species (Kavallieratos et al., 2004;Starý, 2006;Tomanović et al., 2009;Benelli et al., 2014). We used three Eurasian generalist parasitoids (Error! Reference source not found.) including Aphelinus abdominalis (Aphelinidae: Aphelininae), Aphidius ervi (Braconidae: Aphidiinae) and Diaeretiella rapae (McIntosh) (Braconidae: Aphidiinae). They have broad field host ranges, i.e. more than ten host species as described previously for host generalist parasitoids [START_REF] Dassonville | FresaProtect and BerryProtect: mixes of parasitoids to control all common aphid species on protected soft fruit crops Product development and case studies from three years of experience. Fruits and Roots: A Celebration and Forward Look[END_REF], Kavallieratos et al. 2004[START_REF] Zikic | Host range patterning of parasitoid wasps Aphidiinae (Hymenoptera: Braconidae)[END_REF]. In contrast, the fundamental host ranges of these three parasitoids have not been yet reported. Aphelinus abdominalis -is considered as polyphagous (Honek et al. 1998). However, there was no publication of their full field host ranges. A. abdominalis primarily parasitized big aphids, A. solani, M. euphorbiae, and Myzus species. In the laboratory and semi-field conditions, A. abdominalis parasitizes efficiently ten aphid species: Aphis craccivora, A. fabae, (Gazmer et al. 2015;[START_REF] Tena | Parasitoid nutritional ecology in a community context: the importance of honeydew and implications for biological control[END_REF]. A. abdominalis is synovigenic (low egg load, high longevity). They can lay 5-10 eggs/day and can directly feed on early-stage aphids. They have a relatively long life (several weeks) and are more robust than Aphidius species [START_REF] Shrestha | Preference and life history traits of Aphelinus abdominalis (Hymenoptera: Aphelinidae) when offered different development stages of the lettuce aphid Nasonovia ribisnigri (Hemiptera: Aphididae)[END_REF]. Both the physiological trait of egg load and the behavioral trait of host feeding affect host selection, i.e. time-constraint females tend to accept low-quality hosts [START_REF] Deas | Egg and time limitation mediate an egg protection strategy[END_REF]Hopper et al. 2013[START_REF] Jervis | Life-history strategies in parasitoid wasps: a comparative analysis of 'ovigeny[END_REF].

Biological materials -aphid host species and their plant host

Based on our estimation of field host ranges of A. The optimal foraging model was statistically analyzed to find the correlation between parasitoid preference and performance, where preference is the acceptance of an aphid as host, i.e. parasitoid attack and oviposit on) and performance is the survival ratio of parasitoids during each step of its immature life cycle.

Results & discussion -The continuum specialist-generalist

Among six parasitoids (Figure 28), their taxonomic specificity indexes (STD*) range from 1.17 Similarly, we saw a relevance between field host range, laboratory host range and the optimal oviposition pattern. The field host range of A. ervi, A. abdominalis, and D. rapae are 14, more than 10 and 98 species; their (STD*) are 2.21, 2.37 and 2.55, respectively. From all information, we concluded that the taxonomic specificity index and the correlation preference-performance should be used to predict the host specificity of one parasitoid. The taxonomic indexes, in that case, are sensible enough to classify parasitoid host specificity based on taxonomic distance. The Rhode indexes are not relevant in that case probably because it excludes the phylogenetical difference among hosts. The results prove our hypothesis of selective strategies of specialist parasitoids. We proved that the strains of A.

ervi we had in the laboratory are intermediate specialists/generalists, whereas A. abdominalis and D. rapae are generalists. Also, we reported the three-parasitoid fundamental host specificity. The results mean specialist parasitoid accept hosts with good quality for their offspring development, while generalist parasitoids are less choosy. This result is consistent with the statement of host specificity from [START_REF] Colles | Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches[END_REF] that at the individual-choice level, one organism 'decide' to be a specialist (choosy) if they can afford the selection, i.e.

capable of using different resources, no search-time constraint). The study confirms the optimal reproduction hypothesis in ecology on specialist parasitoids and supports current studies on mechanisms of specialization and resistant evolution of A. ervi as a biological model.

Based on the specificity index and the correlation preference-performance pattern, we could define parasitoid assemblages adapted for biocontrol (Klinken 1999;Poulin and Mouillot 2003;[START_REF] Mills | Optimal Foraging Behavior and Efficient Biological Control Methods[END_REF]. For instance, specialist parasitoids are chosen to release in classical and augmentation biocontrol strategies. However, in conservation biocontrol aiming to enhance natural enemy activities by landscape managing, practitioners should consider mix specialist and generalist assemblage (Raymond et al. 2015). Parasitoids with optimal patterns would adapt well in case of classical BC, but that characteristic could be a trade-off with host suppression at the local level in inundative BC [START_REF] Mills | Optimal Foraging Behavior and Efficient Biological Control Methods[END_REF]. Host specificity index and behavioral patterns, therefore, plays a vital role in predicting non-target effects of potential agents and host use efficiency in the field.

To go further -Evaluation of the "cryptic species" hypothesis

Natural populations of parasitoid adaptation to their local environment and differentiation in host specificity (host species and host exploitation efficiency) are common phenomena [START_REF] Takada | A comparison between two strains from Japan and Europe of Aphidius ervi[END_REF][START_REF] Henry | Host-range evolution in Aphidius parasitoids: Fidelity, virulence and fitness trade-offs on an ancestral host[END_REF]. Moreover, most of the analyzed generalist morpho-species were composed of subgroups related to the aphid host, some of them revealed cryptic species [START_REF] Derocles | Are generalist Aphidiinae (Hym. Braconidae) mostly cryptic species complexes?[END_REF]. There are hypotheses of cryptic species within the population of both A. ervi [START_REF] Pennacchio | Host Recognition and Acceptance Behavior in 2 Aphid Parasitoid Species -Aphidius-Ervi and Aphidius-Microlophii (Hymenoptera, Braconidae)[END_REF] We also compared the results from our experiments to other studies on the field and in the laboratory in different geographical areas to test the hypothesis of cryptic species within this population. Results are quite similar between various studies in the field and under laboratory conditions. Among our three parasitoids, D. rapae has a higher specificity index (2.55) than A.

abdominalis (2.37), which are proved to be highly generalists, and A. ervi (2.21), which are shown to be an intermediate specialist. However, when A. abdominalis and A. ervi expressed generalist behavior, i.e. they accepted and attacked all hosts at a high rate (more than 40% of successful oviposition for both species even on low-quality hosts (fig. 30). Regarding A. ervi, our results are quite similar to different studies both in the field and under laboratory conditions in various regions (Zepeda-Paulo et al. 2013, Bilodeau et al. 2013, Kavallieratos et al. 2004[START_REF] Milne | The Release and Establishment of Aphidius-Ervi Haliday (Hymenoptera, Ichneumonoidea) in Lucerne Aphids in Eastern Australia[END_REF]). These shreds of evidence proved that A. ervi life history traits are well conserved at geographical levels. Additionally, [START_REF] Henry | Host-range evolution in Aphidius parasitoids: Fidelity, virulence and fitness trade-offs on an ancestral host[END_REF] stated that host specificity is strictly genetically related. [START_REF] Derocles | Are generalist Aphidiinae (Hym. Braconidae) mostly cryptic species complexes?[END_REF] found that among seven generalist species, only A. ervi do not have morphological substructure specific to their natal hosts (fig. 31). Moreover, in our study A. ervi are instead an intermediate specialist. A. ervi populations are therefore less likely to be composed of cryptic species.

A. Aphelinus abdominalis

INTRODUCTION

Specialization in parasitoid species is defined as a narrow pattern of hosts selected and suitable for offspring development [START_REF] Futuyma | The evolution of ecological specialisation[END_REF][START_REF] Muller | Predators and mutualists influence the exclusion of aphid species from natural communities[END_REF], Straub et al. 2011, Desneux et al. 2012). Multiple characteristics related to biological, ecological and phylogenetic traits are normally used to classify parasitoids as specialists or generalists.

However, all these traits are scarcely documented for most parasitoid species, and the number of host species successfully parasitized has been used largely as an endpoint for describing host specificity [START_REF] Futuyma | The evolution of ecological specialisation[END_REF]Moreno 1988, Shaw 1994). On the one hand, specialists usually show fitness values that are higher, when using one or few particular resources, than fitness values showed by generalists that use all resources available [START_REF] Levins | Theory of Fitness in a Heterogeneous Environment. I. The Fitness Set and Adaptive Function[END_REF][START_REF] Levins | Evolution in changing environments[END_REF]). On the other hand, generalists can rely on a wider range of resources and are more tolerant to environmental changes as well as to poorly diversified systems, e.g.

agricultural habitats (Futuyama and Moreno 1988).

Host specificity, and more broadly diet breath, has been described by the preferenceperformance hypothesis of Jaenike (1978). It predicts a positive relationship between the choice of adult females (preference) and the degree of successful development of offspring (performance). More widely, female preference tends to correlate with host quality for offspring development (Jaenike 1978[START_REF] Thompson | Evolutionary Ecology of the Relationship between Oviposition Preference and Performance of Offspring in Phytophagous Insects[END_REF], Desneux et al. 2009a). Various studies stressed the occurrence of such relationship for specialized phytophagous arthropods [START_REF] Craig | A Strong Relationship Between Oviposition Preference and Larval Performance in a Shoot-Galling Sawfly[END_REF][START_REF] Nylin | Ovi position preference and larval performance in Polygonia calbum (Lepidoptera: Nymphalidae): the choice between bad and worse[END_REF]Gripenberg et al. 2010) as well as for both specialized predators [START_REF] Sadeghi | Individual variation in oviposition preference, and its interaction with larval performance in an insect predator[END_REF] and parasitoids (Driessen 1991[START_REF] Brodeur | Effects of Pieris host species on life history parameters in a solitary specialist and gregarious generalist parasitoid (Cotesia species)[END_REF], Desneux et al. 2009a). By contrast, such relationships shall not be famous in case of generalist arthropods (Eben et al. 2000, Gripenberg et al. 2010, Chesnais et al. 2015) notably presumably owing to their weaker choosiness when encountering different hosts.

Indeed, the behavioral selection of host by parasitoids involves the detection of physical and/or chemical cues from the other trophic levels (like host species and/or host plants) [START_REF] Vinson | The behaviour of parasitoids[END_REF], Vet and Dicke 1992, Mackauer and Michaud 1996), and the specificity of parasitoids may be mainly shaped by info chemicals (Afsheen et al. 2008). Specialist parasitoids more efficiently use specific cues related to their hosts [START_REF] Barbosa | Natural enemies and herbivore-plant interactions: influence of plant allelochemicals and host specificity[END_REF], Vet and Dicke 1992[START_REF] Mccormick Clavijo | The specificity of herbivore-induced plant volatiles in attracting herbivore enemies[END_REF]. For example, for Microplitis croceipes use host kairomones from a variety of host-related sources, e.g. frass, hemolymph, and salivary secretions [START_REF] Jones | Host seeking stimulants for parasite of corn earworm: isolation, identification and synthesis[END_REF][START_REF] Alborn | Host-specific recognition kairomone for the parasitoid Microplitis croceipes (Cresson)[END_REF]. By contrast, generalist parasitoids often use more general cues to identify potential host species (Vet and Dicke 1992). For example, the generalist parasitoid Aphaereta minuta does not use host-derived chemical signals to select host fly larvae and attacks almost all hosts that are present in encountered decaying materials (Vet and Dicke 1992). Such a generalist behavior (low selectivity when facing various hosts) is associated with parasitoid fitness, i.e. performance, mostly dictated by hosts suitability for parasitoid offspring development, which may lead to an overall lack in the preference-performance relationship in generalist parasitoids. However, several studies did report positive preference-performance relations in case of generalist parasitoids [START_REF] Brodeur | Effects of Pieris host species on life history parameters in a solitary specialist and gregarious generalist parasitoid (Cotesia species)[END_REF], Henry et al. 2005[START_REF] Li | The influence of prior experience on preference and performance of a cryptoparasitoid Scleroderma guani (Hymenoptera: Bethylidae) on beetle hosts[END_REF], Kos et al. 2012). Still, these studies (i) tested a few host species only (up to 3), and (ii) the host species belonged to the same tribes or genus representing a possible bias in assessing preference-performance correlation (Poulin and Mouillot in 2005). Such reported positive relationships may be false positive as these studies were not designed per se to evaluate the link between the preference of females and the performance of offspring in the context of the preference-performance hypothesis (Gripenberg et al. 2010).

In this study, we assessed under laboratory conditions the preference (behavioral host range)-performance (physiological host range) relationship in three generalist aphid parasitoids attacking a broad phylogenetic range of hosts. For this, we calculated a host specificity index (Poulin and Mouillot 2005) to classify the parasitoids tested depending on their host specificity and to identify an indicator of the quantifying where these species in a generalist-specialist continuum. For this, we considered previously published results on specialist parasitoids generated by our research group. Also, some side factors modulating preference and/or performance of parasitoids such as endosymbionts or host plants. This is why, twelve aphid species spread over six different host plants were tested and all aphid species were screened for the presence of 9 endosymbionts species.

MATERIAL AND METHOD

Biological materials

Three Eurasia generalist parasitoids were tested: Aphelinus abdominalis (Aphelinidae:

Aphelininae), Aphidius ervi (Braconidae: Aphidiinae) and Diaeretiella rapae (Braconidae:

Aphidiinae). These endoparasitoid species are koinobiont of many aphid species (Honek et al. 1998, Kavallieratos et al. 2004). The description of the aphid species, their color, hosts rapae. Before experiments, the parasitized aphids at the mummy stage were retrieved and isolated in plastic Petri dishes. After the adult emergence, females were mated and fed with the honey solution (50 % water + 50 % honey) for at least 24 hours. The experiments were carried out using 24-48 hour-old parasitoid females.

Experiment 1: preference.

Parasitoid behavioral host ranges were established observing their behavior when they encountered different aphid species. Three parasitoid behavioral steps were identified: detection, acceptance, and oviposition (parasitoids attack). Detection was described as the contact between aphid and parasitoid followed by antenna analysis. Acceptance was defined as the parasitoid abdomen bent underneath its thorax in the direction to the aphid for A. ervi and D. rapae while for A. abdominalis, it was described as movement's right and left behind the aphid. Oviposition was defined as the introduction of the ovipositor in the aphid followed by an egg deposition. Aphid defensive behaviors were also recorded, and three reactions were considered as defensive ones: the kick, cornicle secretion (sticky secretion) and/or escape. For the analyses, all defensive behaviors were grouped.

For each replicates, one leaf of one host plant was placed upside down under a binocular magnifier (8x). One aphid was placed on the leaf with a fine brush. After 5 minutes of the establishment, one mated female parasitoid was introduced. When the parasitoid touched the leaf, the experiment began, and the parasitoid behavior was noted during 5 minutes for A. ervi and D. rapae (short stinging time) and during 10 minutes for A. abdominalis (long stinting time, [START_REF] Wahab | Observations on the biology and behaviour of Aphelinus abdominalis Dalm. (Hym., Aphelinidae), a parasite of aphids[END_REF]. The preference experiment was stopped after the 5 or 10 minutes or when the parasitoid introduced the ovipositor in the aphid suggesting an egg deposition. Each parasitoid and aphid species was tested randomly every experimental day.

Aphid size is known to have an impact on parasitoid host selection process [START_REF] Wyckhuys | Parasitism of the soybean aphid, Aphis glycines by Binodoxys communis: the role of aphid defensive behaviour and parasitoid reproductive performance[END_REF]. Hence, the aphids used in the experiment were all of the equivalent sizes of 2 nd instar A. pisum for A. abdominalis and A. ervi and an equivalent of 4 th instar B. brassicae for D.

rapae, i.e. known instar preferred by parasitoid for oviposition (Sequeira andMackauer 1994, Hafez 1961). PCR amplification. Diagnostic PCR reactions with a species-specific primer (Sup material 1)

were conducted in 1.5 % agarose gel stained with ethidium bromide and visualized with UV light to test the presence of facultative symbiont. Each symbiont was tested with a positive control (DNA from infected species) and two negative controls (two pea aphid genotypes with only primary endosymbiont Buchnera aphidicola). Furthermore, the quality of the extraction was tested by PCR on the primary endosymbiont: B. aphidicola. Finally, bands showing a signal were removed from the gel, purified (with Min Elute PCR purification kit)

and sequenced to check the symbiont identity (validated when the sequence was at least 95% similar).

Index of host specificity (STD*).

The STD* considers the taxonomic and ecological information, and calculates a value for each parasitoid species (Poulin and Mouillot 2005). This index is inversely proportional to

Data analysis

All statistical analyses were carried out using R version 3.2.2. A generalized linear model (GLM) with a binomial distribution and followed by a multi-comparison test (Tukey, package 'multcomp') was used to (i) compared each parasitoid behavior recorded (detection, acceptance and stinging rate) on the rearing host with the parasitoid behavior on all other aphid species, (ii) analyzed the effect of the aphid colors, the aphid host plants, the aphid tribe and the presence of secondary endosymbiont on the proportion of stung aphids by each parasitoid species in each aphid species, (iii) compared the parasitoid mortality among the different stage (egg, larvae, mummy and adult) in every aphid species, and (iv) analyzed the relationship between parasitoid stinging rate and (1) the aphid defensive behavior or [START_REF] Calvo | The performance of an aphid parasitoid is negatively affected by the presence of a circulative plant virus[END_REF] the parasitoid physiological hosts range (emergence rate). The deviation from a 0.5 sex ratio was tested with permuted Fisher's Exact test (with the Bonferonni adjustment method).

RESULTS

Experiment 1: Preference.

For A. abdominalis, the proportion of aphids detected in each aphid species was not significantly different than the proportion of A. pisum (the rearing host) detected, (X 2 13 = 15.53, P > 0.05) (Table 2). The proportion of detected aphids in each aphid species ranged from 0.91 to 1.00. Two aphid species (A. fabae and A. gossypii) were less accepted compared to the proportion of A. pisum accepted (X 2 13 = 112.47, P < 0.001). The proportion of aphids accepted in each aphid species ranged from 0.31 to 1.00. These species being less accepted were also less stung by the parasitoids compared to the proportion of A. pisum stung (X 2 13 = 93.37, P < 0.001). The proportion of stung aphid species ranged from 0.25 to 0.94. Due to the low number of A. fabae and A. gossypii stung by A. abdominalis, these aphid species were not used in experiment 2.

For A. ervi, the proportion of aphid species detected in each aphid species was not significantly different than the proportion of A. pisum (the rearing host) detected (X 2 13 = 31.76, P < 0.01 but there were no differences between the proportion of rearing host detected and the proportion of the other aphid species in the multi-comparison test, Table 2). Aphidius ervi detected a proportion of aphids in each aphid species that ranged from 0.91 to 1.00. Four aphid species (A. craccivora, A. fabae, B. brassicae and R. padi) were less accepted compared to the rearing host (X 2 13 = 155.84, P < 0.001). The proportion of accepted aphids in each aphid species ranged from 0.48 to 0.95. The same four less accepted species were also less stung compared to the rearing host (X 2 13 = 144.89, P < 0.001) and their proportions ranged from 0.42 to 0.95.

For D. rapae, the proportion of aphid species detected in each aphid species was not significantly different than the proportion of B. brassicae (the rearing host) detected (X 2 13 = 72.05, P < 0.001 but there were no differences between the proportion of rearing host detected and the proportion of the other aphid species in the multi-comparison test, Table 2). The detection proportion ranged from 0.58 to 1.00. Six aphid species (A. craccivora, A.

fabae, A. gossypii, M. euphorbiae (T and P), M. dirhodum and R. padi) were less accepted compared to the rearing host (X 2 13 = 157.68, P < 0.001) and the proportion of aphids accepted in each aphid species ranged from 0.30 to 0.98. These six less accepted aphid species and two other aphid species (A. nerii and M. persicae red clone) were less stung compared to the rearing host (X 2 13 = 190.94, P < 0.001). M. dirhodum, A. craccivora, and A.

fabae were not used in experiment 2 due to the insufficient number of stung aphids.

When all aphid defensive behaviors were grouped, there was a negative relationship between the proportion of aphid species stung by A. abdominalis and the proportion of aphid defenses (X 2 1= 34.42, P < 0.01, dispersion parameter: 4.8) (Figure 1). There was no relationship between the proportion of stung aphid species by A. ervi and D. rapae and the proportion of aphid defenses (X 2 1 = 20.48; 6.49, dispersion parameter = 9.5; 13.5, P > 0.05, respectively). The aphid defensive behavior varied depending on the parasitoid species and the aphid species (X 2 2 = 270.94, = P <0.01 and X 2 13 = 101.26, P < 0.001, respectively).

Specifically, D. rapae induced the highest aphid defensive rate (on average 62% species of the aphid reacted), followed by A. abdominalis (on average 45% of the aphid species reacted) and A. ervi (on average 20% of the aphid species reacted).

Experiment 2: Performance.

The highest adult survival rate for A. abdominalis was in A. pisum, M. euphorbiae (potato and tomato plants), M. dirhodum, M. persicae (green and red clones), R. padi and S. avenae and the proportions of adults emerged ranged from 0.61 to 0.9 (Figure 2,A). The other aphid species could be separated by the stages at which the parasitoid development failed.

Firstly, a lower proportion of parasitoid eggs were deposited in A. craccivora compared to the rearing host (P < 0.01). Then, a high parasitoid mortality was observed between egg and larval stage when A. abdominalis developed on A. nerii (P < 0.01) and the proportion of larvae in this aphid species was different compared to the proportion of larvae in the rearing host (P < 0.01). The parasitoid mortality between the larval and the mummy stage was observed in B. brassicae and S. graminum, (all P < 0.01) and the proportions of mummies were significantly different compared to the proportion in the rearing host (all P <0.01).

Finally, in S. avenae, parasitoid mortality was observed after aphid mummification (P = 0.023). However, the proportion of adult parasitoids emerged from this aphid species was not different compared to the proportion emerged from the rearing host. The A.

abdominalis sex ratio varied from the 50:50 depending on the aphid species. It was malebiased on M. dirhodum, M. persicae green and red clones and R. padi (all P < 0.001) and female-biased in M. euphorbiae on tomato (P < 0.05) (Table 3). We found no relationship between the preference (sting rate) of A. abdominalis and its performance (emergence rate) persicae green and red clone, parasitoid mortality was observed after aphid mummification (P = 0.01) and the proportion of adults emerged from these species was significantly different than the proportion of adults emerged from the rearing host (P < 0.01). The A. ervi sex ratio was similar from 50:50 in all aphid species (all P > 0.05) (Table 3). We found a positive relationship between the A. ervi preference (sting rate) and its performance (emergence rate) (X 2 1 = 33.89, dispersion parameter = 4.8, P < 0.01, Figure 3 andS1, B).

(
The highest adult survival rate of D. rapae was observed in A. gossypii, B. brassicae, M.

persicae (green and red clones), R. padi and S. avenae and the proportions of adults emerged from these species ranged from 0.38 to 0.61 (Figure 2,C). The other aphid species could be separated by the stages at which the parasitoid development failed. Firstly, a significant parasitoid mortality was observed between egg and larval stage in A. pisum and M. euphorbiae (on potato and tomato plants) (all P < 0.01) and the proportion of parasitoid larvae in these aphid species was different than the proportion of parasitoid larvae in the rearing host (P < 0.01). The parasitoid mortality between the larval and the mummy stage was observed in A. nerii and S. graminum (all P < 0.01) and the proportion of mummies was significantly different than the mummy proportion in the rearing host (P < 0.01). Finally, the parasitoid mortality was observed after the aphid mummification in B. brassicae, M.

persicae green and R. padi (all P < 0.04). However, their proportion of adults was not significantly different than the proportion of emerged adult in the rearing host (P > 0.05 for the three aphid species). The D. rapae sex ratio was similar from 50:50 in all aphid species (all P > 0.05) (Table 3). We found no relationship between the preference (sting rate) of D.

rapae and its performance (emergence rate) (X 2 1 = 11.49, dispersion parameter = 9.56, P > 0.05, Figure 3 and S1, C).

Experiment 3: Presence of secondary endosymbionts in aphids.

The primary endosymbiont Buchnera aphidicola was found in all aphid samples.

Arsenophonus, PAXS, Rickettsia, Rickettsiella, Serratia symbiotica, Spiroplasma, and Wolbacchia were not found in the aphid species screened. Hamiltonella defensa was found 6 times out of 6 in A. fabae (6/6) and 4 times out of 6 in M. dirhodum (4/6), and Regiella insecticola was found 6 times out of 6 in M. dirhodum (6/6).

Index of host specificity.

Binodoxys communis and B. koreanus were the most specialized species considered in our study, and they stung only the Aphis genus (STD* are respectively 1.17 and 1.32) (figure 4).

Lysiphlebus testaceipes (France and USA origin) stung more aphid species, but they only came from the Aphidini tribes (STD* are respectively 1.75 and 1.83). A. ervi stung the Macrosiphini tribes and some species with small prevalence in Aphidini tribes and its STD* is 2.21. A. abdominalis and D. rapae stung almost the same quantities of species in both tribes with high prevalence, and their STD* are 2.37 and 2.55, respectively.

DISCUSSION

In this study, we tested the preference-performance relationship for three generalist parasitoids on twelve aphid species and used previous results on specialist parasitoids. We showed no relationship for A. abdominalis and D. rapae while a significant relationship was found for A. ervi. Overall, the three parasitoid species showed a low behavioral selectivity (preference traits) whereas their performances, and specifically for A. ervi, were strongly parasitoids (Desneux et al. 2009a(Desneux et al. , 2009b, unpublished data), unpublished data).

Preference traits

As expected for generalist parasitoids, the three species tested showed low host selectivity, and they stung mostly all aphid species encountered at high rates. However, preference was modulated by different factors (1) A. abdominalis and A. ervi had less stung the black aphids compared to the other aphid colors (respectively, X 2 3 = 49.44; 69.4, dispersion parameter = 4.3; 7.1, P < 0.02), ( 2) A. abdominalis and A. ervi stung mainly the aphids from the macrosiphini tribe (respectively, X 2 1 = 31.86; 55.36, dispersion parameter = 4.9; 7.75, P < 0.01) and (3) A. abdominalis had less stung the aphids on squash (X 2 3 = 60.5, dispersion parameter = 4.32, P = 0.03). The presence of endosymbiont did not modulate the parasitoid preference (respectively for A. abdominalis, A. ervi and D. rapae X 2 1 = 14.24; 2.21; 32.9, dispersion parameter = 6.88; 10.9; 11.6, P > 0.05). Aphid defensive behaviors are known to potentially affect oviposition behavior of various aphid parasitoids and reduce the parasitoid host range [START_REF] Kouamé | Influence of aphid size, age and behaviour on host choice by the parasitoid wasp Ephedrus californicus: a test of host-size models[END_REF][START_REF] Wyckhuys | Parasitism of the soybean aphid, Aphis glycines by Binodoxys communis: the role of aphid defensive behaviour and parasitoid reproductive performance[END_REF], Desneux et al. 2009a). In line with these studies, no relationship was found between aphid stung rates by A. ervi and D. rapae and the proportion of aphid defenses observed, suggesting that their 'quick' sting syndrome avoid aphid defenses (Desneux et al. 2009c, Bilodeau et al. 2013,). By contrast, there was a negative relationship between the proportion of aphid species stung by A.

abdominalis and the proportion of aphid defensive behaviors. Aphelinus abdominalis showed stinging time ranging between 20 and 60 seconds, so about four times more than the two other parasitoid species tested. This behavioral pattern suggests that aphid defensive behaviors may disturb females during their stinging event (De Farias andHopper 1999, Wahab 1985). Secondly, the success of aphid defenses depends on the relative size of attacking parasitoid vs. aphid. A. abdominalis is two times smaller than A. ervi and D. rapae which may attack aphids more easily (Le Ralec et al. 2010). Finally, A. abdominalis did not show a particular behavior enable to lower occurrence of aphid defenses, as observed in several other aphid parasitoid species, e.g. antennal tapping mimicking the behavior of aphid-mutualistic ants [START_REF] Völkl | Effects of adult mortality risks on parasitoid foraging tactics[END_REF].

Performance traits

The three generalist parasitoids showed higher host specificity index values compared to the specialized species considered in this assessment. Indeed, Binodoxys communis and B. ervi could be considered as an intermediate specialist-generalist, i.e. it has the same host range than a generalist one but differ in their relative performance [START_REF] Klinken | Host specificity testing: Why do we do it and how we can do it better. Host specificity testing of exotic Arthropod Biological Control Agents -The biological basis for improvement in safety from Forest Health Technology Entreprise Team in[END_REF].

Different physiological and ecological factors could give aphid resistance against immature parasitoids and modify parasitoid host range. The primary sources of resistance are poor parasitoid ability to control the host metabolism, the presence of secondary endosymbionts in aphids, and the aphid ability to sequester toxic compounds and/or the host quality itself.

Generalist organisms have a successful development in a wide host range through phenotypic plasticity, i.e. the ability to express different phenotypes depending on the environment [START_REF] Agrawal | Phenotypic Plasticity in the Interactions and Evolution of Species[END_REF]) and transgenerational phenotypic plasticity, i.e. the offspring would be primed to develop in the host in which their mother developed (Mousseau and Fox 1998). The generalist behavior of the three parasitoid species in association with their phenotypic plasticity may rapidly develop an adaptation to novel host species (Fox and Mousseau 1998). However, becoming acclimated to its host may be costly for the parasitoids (Uller 2008).

The facultative endosymbionts present in aphids may compromise the successful development of parasitoids and reduce their host ranges [START_REF] Ferrari | Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance[END_REF][START_REF] Oliver | Variation in resistance to parasitism in aphids is due to symbionts not host genotype[END_REF], McLean and Godfray 2015). Specifically, Hamiltonella defensa and Regiella insecticola are known to protect aphids against different natural enemies such as parasitoids (Oliver et al. 2003[START_REF] Von Burg | Genetic variation and covariation of susceptibility to parasitoids in the aphid Myzus persicae: no evidence for trade-offs[END_REF]. In this study, A. abdominalis was not impacted by the presence of secondary endosymbionts in aphids and had 84% of successful parasitism in M.

dirhodum. Aphid ability to sequester toxic secondary metabolites when feeding on toxic plants [START_REF] Mooney | Coexisting congeners: demography, competition, and interactions with cardenolides for two milkweed-feeding aphids[END_REF][START_REF] Pratt | Accumulation of Glucosinolates by the Cabbage Aphid Brevicoryne brassicae as a Defense Against Two Coccinellid Species[END_REF]) might also impact the parasitoid host range [START_REF] Helms | Effects of variation among plant species on the interaction between a herbivore and its parasitoid[END_REF] (Bruce et al. 2008, Kavallieratos et al. 2004[START_REF] Colinet | Host age and fitness-related traits in a koinobiont aphid parasitoid[END_REF], suggesting that the aphid genotype could be involved in this failure (Bilodeau et al. 2013). Aphid ability to sequester the toxic compounds from their plant requires a high specialization of these aphid species [START_REF] Mooney | Coexisting congeners: demography, competition, and interactions with cardenolides for two milkweed-feeding aphids[END_REF]) and only a few (up to four) parasitoid species can parasite A. nerii and B. brassicae (Kavallieratos et al. 2004); suggesting that robust circumventing mechanisms are needed for a parasitoid to adapt to aphid defense. Furthermore, by contrast with endosymbionts, this is a general aphid defensive against natural enemies in general and not only against parasitoids [START_REF] Omkar | Preference-performance of a generalist predatory ladybird: A laboratory study[END_REF]Mishra 2005, Toft and[START_REF] Thompson | Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects[END_REF], general defenses confer a stronger protection against generalist parasitoids compared to the specialized defenses.

Finally, host quality could also contribute to a reduction in aphid parasitoid host range (high mortality of the older parasitoid larvae until emergence) or at least modulate their sex ratio (male-biased) (Thompson 1985, Mackauer 1986[START_REF] Kouamé | Influence of aphid size, age and behaviour on host choice by the parasitoid wasp Ephedrus californicus: a test of host-size models[END_REF], Godfray 1994). The host species and the host's age are the two main components of host quality for parasitoid development. However, generalist parasitoids have a weaker choosiness when encountering different hosts as shown in the behavioral results of this study. For example, S.

graminum caused a high larval mortality of the three parasitoid species (consistent with Desneux et al. 2009a) and a high value of un-emerged parasitoids of A. ervi were observed in R. padi despite they are stung mainly by the parasitoids, indicating S. graminum and R. padi to be poor hosts for these parasitoid species. Furthermore, some parasitoids tend to place male eggs in unfavorable hosts (King 1990, Kochetova 1978). For example, the sex ratios of Aphidius colemani emerging adults were more male-biased from R. padi than from the three other aphid species (M. persicae, S. graminum, and A. gossypii), suggesting that R. padi is a poor-quality host for A. colemani [START_REF] Ode | Oviposition vs. offspring fitness in Aphidius colemani parasitizing different aphid species[END_REF]. In A. abdominalis, a male-biased sex ratio was observed in M. dirhodum, M. persicae (green and red), R. padi and S. graminum;

but no link among the host plant, the presence of endosymbiont, the color or the host size could explain these results except the low quality of these hosts for A. abdominalis.

The preference-performance relationship in generalist parasitoids

The meta-analysis of Cripenberg et al. (2010) of the preference-performance relationship in phytophagous insects described a relationship between the preference and the performance of specialists and intermediate specialists / generalists and no relationship for generalists and these results are consistent with those obtained in our study, there was no relationship between the preference and the performance of A. abdominalis and D. rapae whereas a strong relationship was observed for A. ervi. The phenotypic plasticity is more critical in generalist parasitoids as well as the transgenerational phenotypic plasticity, and these abilities could explain the lack of the preference-performance relationship in A. We demonstrated that the preference-performance relationship does occur for specialist and intermediate specialist-generalist parasitoids but not for true generalist ones; likely owing to combined effects of low selectivity and the phenotypic plasticity in generalist parasitoids. The generalists are less affected by specific aphid defenses against them (such as endosymbionts) whereas they are strongly affected by general ones that are used against natural enemies, e.g. aphid ability to sequester the toxic compounds (Desneux et al. 2009a).

The preference of generalists is not an accurate proxy of actual parasitoid realized host range, i.e. performance. The occurrence (or lack thereof) of such relationship, as well as the host specificity index, may provide a reliable indicator of actual generalism -specialism in parasitoids.

All aphid species belong to the family Aphididae and subfamily Aphidinae and their morphological characteristics were described by Blackman and Eastop (2006). All aphids were collected in the field in France during 2013-2014 on their respective host species and maintained in their host plant in ventilated cage (60 x 60 x 60 cm) covered by mesh under controlled conditions (23  2 °C, RH 65  5% and photoperiod 16:8 L:D). n/a means that data are non-available due to the unsuccessful development of the parasitoids in these aphid species. n/a n/a n/a * P < 0.05, ** P < 0.01, *** P < 0.001 (deviation from a 0.5 sex ratio). n/a means that data are non-available due to the unsuccessful development of the parasitoids in these aphid species.

Aphidini Macrosiphini

FIGURE LEGENDS

Figure 33. Synthesis of bottom-up effects of plants on parasitoid community (from Hunter 2003)

We focused on the bottom-up effect of abiotic stresses on the host specificity of parasitoids.

Firstly, we performed an analytic review on the bottom-up effects of all abiotic stresses on the tri-trophic plant-aphid-parasitoid to define the most relevant factor for our experimental set-up. Secondly, we chose one parasitoid among our three parasitoids based on previous results (chapter 4). Thirdly, we designed experiments to question the ability of such abiotic factor to modulate the host range of our parasitoid (fig. 32).

Choice of a relevant abiotic factor to analyze impacts of bottom-up effect on the host specificity of parasitoids

Gathering data

To gather all articles on the subject 'bottom-up effects of abiotic stress on aphid parasitoids', we based on the process of meta-analysis review [START_REF] Koricheva | Handbook of Meta-analysis in Ecology and Evolution[END_REF]. The first step of the process consisted of the construction of a database of all relevant articles based on Web of Science ®.

We To eliminate irrelevant studies, we considered only studies that question the bottom-up effect of abiotic factors on the tritrophic system 'plant-aphid -parasitoid'. These studies contain data sets from both optimal and stress conditions (average +/-variance). Finally, the following set of criteria were applied: Based on these keywords, 746 studies were found. By reading titles, abstracts or if necessary, articles, 230 articles that followed our criteria were chosen (annex 1, figure 36). However, only 18 studies provide the required information, i.e. the parameters of three trophic under optimal conditions and abiotic stress; the number of replications for each trophic.

Data extraction and statistical analysis

We extracted all data related to the modifications on different parameters of life-history traits of the three trophic levels: plant-aphid-parasitoids. The parameters for plants were morphology, primary metabolism, and secondary metabolism. The parameters for both aphids and parasitoids were the preference, performance, and population dynamics. The data were extracted from tables or figures using ImageJ. Three experimental scales have been taking on: laboratory, greenhouse or on the field. We quoted the stress type (drought, nutrients, temperature) and the ways those stresses were applied (continuous or pulsed). The data were analyzed by Pearson's Chi-squared test with Yate continuity correction to compare the performance of plants, aphids, and parasitoids between optimal and stress conditions.

The purpose was to find if abiotic factors have a significant impact on the third trophic level, i.e. parasitoids. We counted the number of parameters of performance that reduced (optimal>stress), increased (optimal<stress) or did not change (optimal = stress) under stress conditions.

Results

Abiotic factors have significant impacts on the whole system (Error! Reference source not found., p value < 0.001). Among all types of abiotic stress, continuous water limitation adversely affected parasitoid life-history traits (p value < 0.001) and plants (p value = 0.013).

However, aphids were only marginally impacted (p value = 0.056). There are few data on how pulsed water stress affected the tri-trophic system. Huberty and Denno (2004) suggested that pulsed water stress could indirectly benefit aphids as senescence plants release nutrients to the phloem.

The other stressors such as light and temperature imply both bottom-up effects and direct effects on the other trophic levels (Error! Reference source not found.). Light conditions did not cause significant impacts on plants or aphids (p value > 0.05) but significant impacts on parasitoids (p value = 0.02). Temperatures have negative impacts on all organisms (plants: p value = 0.001; aphids: p value = 0.0098; parasitoids: p value = 0.032). However, it is not clear whether impacts of temperatures on insects are direct or indirect because aphids and parasitoids are temperature sensible (Godfray 1994;van Emden and Harrington 2007). There was no evidence of bottom-up effects of nutrient stress on the whole system or at each trophic level. parasitoids: however, the incomes are both negative and positive, varying with stress nature and herbivore species [START_REF] Price | The Plant Vigor Hypothesis and Herbivore Attack[END_REF]Huberty and Denno 2004;[START_REF] Ramegowda | The interactive effects of simultaneous biotic and abiotic stresses on plants: Mechanistic understanding from drought and pathogen combination[END_REF].

There are so far six articles relevant to our subject of "bottom-up effects of water limitation on aphid parasitoids" (table 5). In general, all studies suggest a decrease of parasitoid efficiency in host suppression (Johnson et al. 2011;[START_REF] Shipp | Greenhouse Climate: an Important Consideration when Developing Pest Management Programs for Greenhouse Crops[END_REF][START_REF] Amini | Impact of Irrigation Systems on Seasonal Occurrence of Brevicoryne brassicae and Its Parasitism by Diaeretiella rapae on Canola[END_REF]Tariq et al. 2013;Aslam et al. 2013;Romo and Tylianakis 2013).

Table 3. Articles on the subject: "Impacts of water stress on the tritrophic plant-aphidparasitoid system."

Explanations of possible bottom-up impacts

Effects on parasitoids may be modulated by the herbivorous interactions between aphids and their host plant (Error! Reference source not found.). Water deficiency in plants may decrease the emission of plant volatiles which serves as cues for parasitoids (Weldegergis et al. 2015) resulting in parasitoids less prefer infested plants (Aslam et al. 2013, Tariq et al. 2013). Herbivore density and size could be modulated by the stress tolerance of plants, which result in affected plant nutritional quality and/or immune system. One scenario of plant stress tolerance is their secondary pathways activated producing insecticidal toxins like phenolic compounds [START_REF] Caretto | Carbon Fluxes between Primary Metabolism and Phenolic Pathway in Plant Tissues under Stress[END_REF]. Those toxins to protect infested plants could delay insect growth and make them more susceptible to natural enemies by diminishing the herbivorous immune response or performance (Ibanez et al. 2012). On the contrary, the plant insecticidal compounds may act like "arms race" of aphids by deterring the performance of parasitoids (Züst and Agrawal 2015) if aphids could sequester them. More specifically, aphids can sequester polar toxic compounds or tolerate apolar induced compounds at low concentration [START_REF] Züst | Mechanisms and evolution of plant resistance to aphids[END_REF]. Morphological modification in plants can influence the overall parasitic efficacy. The structural morphology of plants may be enhanced [START_REF] Couture | Elevated temperature and periodic water stress alter growth and quality of common milkweed (Asclepias syriaca) and monarch (Danaus plexippus) larval performance[END_REF] that cause difficulty for herbivores in foraging. The altered plant quality is accompanied by the reduction in aphid population and the loss in a number of survival parasitoids. In another case, the increase in flower-head size provides shelter for herbivores and reduce the parasitism [START_REF] Dias | Bottom-up effects on a plantendophage-parasitoid system: The role of flower-head size and chemistry[END_REF]. Another critical factor is the presence of symbionts on aphids.

Plant host's stresses can impact the bacterial population on aphids following by the alter the resistance of aphid to parasitism (Cayetano and Vorburger 2013). Overall, the effects of plant hosts quality under stresses on parasitoids are mutually determined by several factors (Error! Reference source not found.). It thus hard to predict the trend of the host range of parasitoids under bottom-up effects.

Choice of a relevant 'plant-aphid-parasitoid' tritrophic system to analyze the host range modulation

Among our three tested parasitoids, we interest in A. ervi. Firstly, A. ervi are intermediate (host) specialist. This intermediate position may allow a shift toward a more generalist or specialist pattern in a variable environment. There is a hypothesis on intermediate specialists/generalists which extinct due to their low efficient adaptation strategy (Colles et al. 2009, Buchi and[START_REF] Buchi | Coexistence of Specialist and Generalist Species Is Shaped by Dispersal and Environmental Factors[END_REF]. We would like to test the adaptability of A. ervi to modulate its host range under environmental stresses. Moreover, A. ervi is commonly used as a biological model to study ecological concepts and evolution mechanisms (annex chap5 table 8). These studies may provide hints for mechanisms underlying the results of bottomup effects we observed.

Based on previously established host range part for A. ervi (chap 4, fig. 30), we chose six aphid species assemblage which is different on taxa and biological traits. Three relatively good aphid hosts (more than 40% emerging adults) were selected: Sitobion avenae on wheat and Acyrthosiphon pisum on faba beans and Macrosiphum euphorbiae on potato. Myzus persicae on cabbage were also selected as medium host (10% emerging adults). All of them belong to the Macrosiphini tribe as the host aphid phylogeny was described previously as a significant factor to explain the host range (chap 4). For the other aphid hosts, A. ervi accepted at low ratio and were not capable of forming mummies inside the rest hosts. We excluded them except for Aphis nerii on Asclepias and Rhopalosiphum padi on wheat to also test our hypotheses on bad hosts from the Aphidini tribe.

Experimental set-up: Does water limitation bottom-up effect modulate A. ervi host specificity?

To disentangle the effect of environmental conditions on the host range modulation, we wanted to test the effect of abiotic factors on our host range indexes previously described (chap 4): the host specificity index and the correlation preference-performance. Our question is whether these indexes would change under water limitation conditions. Firstly, we tested the eventuality of bottom-up effects on two equally good hosts for A. ervi (article 2), i.e.

whether the impact of water limitation could reach and influence the preference and performance of A. ervi. Secondly, we increased the diversity of aphid hosts in quality and quantity to test the impact of bottom-up effect on the correlation preference-performance and host specificity. Moreover, if there is an impact, what happens at the lower trophic level that could explain such result (articles 3)? Our hypothesis was that plant water limitation could affect the preference and performance of A. ervi due to modifications at the plant levels such as defense, morphology or nutritional quality as suggested by [START_REF] Becker | Effects of Abiotic Factors on HIPV-Mediated Interactions between Plants and Parasitoids[END_REF]. As a result, A. ervi host specificity would be impacted by water limitation.

In this study, we chose to apply a long-term and continuous water stress treatment (30% of soil saturation level) compare to optimal conditions (100% of soil saturation in all plants except 70% in cabbage). To define the relevant level of water, we monitored a pre-experiment to test the effect of different water conditions on plant and aphid biological traits. The threshold of 30% was a compromise between an apparent effect of water on plant traits compare to optimal conditions and an acceptable rate of aphid survival when reared on plants submitted to water limitation.

We applied the same host range testing method as previous chapter 4. The biological traits of both plants, aphids, and parasitoids were measured to evaluate the impacts of water limitation. We also calculated two host specificity indexes: the Taxonomic index of specificity (Poulin & Mouillot 2005) which put weigh of specificity on the taxonomic distance among hosts; and the Rohde index of specificity [START_REF] Rohde | How to measure ecological host specificity[END_REF], which measures host specificity based on the parasitism rates on hosts (Chapter 1.4.1).

Water limitation impact preference and performance of good host (article 2)

We were able to show that the impact of water limitation can reach the higher trophic level of natural enemies even when plants and aphids tolerate the applied stress but this effect is not similar in different plant-aphid complexes, yet the relative host qualities are identical.

Plant and aphid traits were negatively affected by water limitation, which might be related to the reduction of host use efficiency of A. ervi. The next question is: whether water limitation impacts on A. ervi performance on sub-optimal hosts or host feeding on toxic plants? Would the results similar across all plant-aphid combinations?

Water conditions modulate A. ervi host specificity (article 3)

We observed that water limitation have negative impacts on parasitoid development in medium and good host quality (M. persicae, M. euphorbiae, and S. avenae). The mortality of parasitoids on low-quality hosts like R. padi or A. nerii remains high which is not different under both water conditions. Our explanation comes from different defense strategies of plants and aphids under combined stresses, and the nutritional quality of both plant and insect. Under severe and/or continuous drought conditions, plants nutrient resources reduce as a trade-off for stress tolerance which reduces herbivore fitness (Price 1991, Huberty andDenno 2004). At the same time, the hardened structure of plants, the stomatal closure or the increase of plant trichome under stress may cause difficulty for herbivores in foraging [START_REF] Couture | Elevated temperature and periodic water stress alter growth and quality of common milkweed (Asclepias syriaca) and monarch (Danaus plexippus) larval performance[END_REF]. The two mechanisms probably cause the decrease of A. ervi performance on M. persicae, M. euphorbiae and S. avenae.

However, on native host species (A. pisum), both preference and performance of A. ervi were unchanged. The resistance of A. ervi developed on A. pisum under cascade impacts of drought could be explained by the effectiveness of the placenta-like structure of larval parasitoid which drives adequate nutrients for larvae, the efficiency of plant symbioses (rhizobacteria) in protecting beans from combined stress.

Besides, we observed that the optimal strategy for A. ervi is not efficient under water limitation i.e. the correlation between preference and performance is lost under stressed conditions compare to optimal conditions. Our study provides evidence for the model of the trade-off between host range breadth and host use efficiency as suggested by Straub et al. (2011).

Figure 35 Impacts of soil water limitation on the relation preference -performance of Aphidius ervi

Interestingly, the impacts of water limitation on the preference and performance of A. ervi were reflected on the shift of host specificity indexes. Among two indexes, the STD* similar, but the LW SS decreased in compare to OW (0.61 and 0.77, respectively). The result means that A. ervi became more specialist under water limitation as they could develop well on only one aphid host, A. pisum. The decrease of host specificity is relevant to the model of Klinken (1999) (see chapter 1.4). The Rhode index, in that case, is more relevant than the STD* as it could detect the subtle change in host specificity through parasitoid performance and A. ervi, under both LW and OW, had the same host range.

In this study, we highlight the environmental context-dependent of outcomes of abiotic stress effects. The information of abiotic factors then should be considered before choosing and releasing on BCA on the field. This study also helps to predict the efficiency of one BCA on the field, which also depends on the host range of both herbivores and parasitoids.

Table 4. Biotic and abiotic factors affecting the host specificity of aphid parasitoids (adapted from Hunter 2003[START_REF] Prado | Ecological Interactions Affecting the Efficacy of Aphidius colemani in Greenhouse Crops[END_REF])

Impacts

Introduction

Arthropod communities are influenced by both bottom-up and top-down forces in wild and agricultural ecosystems, with bottom-up forces being characterized by effects occurring from lower trophic levels to higher ones while the top-down forces show the reverse (Hunter andPrice 1992, Johnson 2008). Natural enemies inhabiting agro-ecosystems such as parasitoids may be largely affected by bottom-up forces because herbivore hosts represent the entire nutritional and physiological environment during immature parasitoid development, and such herbivores are often strongly impacted by bottom-up effects (Han et al. 2014[START_REF] Han | Does plant cultivar difference modify the bottom-up effects of resource limitation on plant-insect herbivore interactions[END_REF]. Parasitoid performance depends mainly on host quality, which in turns is modulated by the host plant and abiotic factors (Vinson, 1990;Godfray, 1994). Also, adult female parasitoid preference, i.e. selection of hosts for laying eggs, is intervened by both their host recognition and acceptance (Godfray 1994). Female choice primarily bases on host-related, contact, and volatile cues (Vet & Dicke 1992). Therefore, stresses inducing bottom-up effects on hosts may, in turn, modulates parasitoid preference (host acceptance)

and/or their performance (host suitability) as these are critical determinants of the parasitoid host range (Desneux et al. 2009a;[START_REF] Desneux | Cryptic species of parasitoids attacking the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in Asia: Binodoxys communis Gahan and Binodoxyx koreanus Stary sp. n. (Hymenoptera: Braconidae: Aphidiinae)[END_REF]2012). For example, plant vigor could modulate dispersal of parasitoids presumably through changes in parasitoid preference when selecting hosts [START_REF] Kher | Plant Vigor Metrics Determine Spatio-Temporal Distribution Dynamics of Oulema melanopus (Coleoptera: Chrysomelidae) and Its Larval Parasitoid, Tetrastichus julis (Hymenoptera: Eulophidae)[END_REF] and plant characteristics mediated by growing conditions can impact parasitoid ability to attack host aphids (Desneux and Ramirez-Romero 2009). Availability of critical nutrients to plants, e.g. nitrogen, could affect as well the development of aphid parasitoids [START_REF] Chesnais | Cascading effects of N input on tritrophic (plant-aphid-parasitoid) interactions[END_REF], Aqueel et al. 2015) but effects vary in function of host species considered. All in all, variations in host plant quality may affect directly herbivorous and parasitoid arthropods as well as their relationships.

Among abiotic stresses, availability of water is one of primary constraint impacting plant quality; it may trigger changes in multi-trophic interactions, population dynamics as well as community structure (Hunter andPrice 1992, Schoonhoven et al. 2005;Han et al. 2015a;[START_REF] Novgorodova | Organization of honeydew collection by foragers of different species of ants (Hymenoptera: Formicidae): Effect of colony size and species specificity[END_REF]. Plant water content affects its nutritional value which, in turn, has an impact on insect behavior. For example, herbivorous insect choosiness when encountering host plants is influenced by plant quality [START_REF] Schoonhoven | Insect-plant biology[END_REF], Metcalfe et al. 2010, Weldegergis et al. 2015), e.g. Mamestra brassicae (moth) preferred to lay their eggs on drought-stressed plants than on control ones. Furthermore, severe drought decreases the emission of herbivore-induced plant volatiles that plays a crucial role in host detection by parasitoids and modifies their host selection [START_REF] Becker | Effects of Abiotic Factors on HIPV-Mediated Interactions between Plants and Parasitoids[END_REF]. Plant quality has an impact also on the higher trophic level performance through three potential mechanisms:

(1) drought stress could promote toxin production by the plant which interferes with the development of parasitoid larvae inside the host, e.g. through sequestration of toxins by the hosts (Malcolm 1989;[START_REF] Ode | Plant chemistry and natural enemy fitness: Effects on herbivore and natural enemy interactions[END_REF]Desneux et al. 2009a, (2) hosts could be qualitatively suboptimal in terms of nutritional requirements for parasitoid larvae (Desneux et al. 2009a), and (3) plant toxins may modulate host immunity enabling higher parasitoid performance [START_REF] Kaplan | Indirect plant-parasitoid interactions mediated by changes in herbivore physiology[END_REF].

Potential bottom-up effect of drought stress in both preference and performance of parasitoids has scarcely been documented. Such knowledge on the impact of bottom-up forces on tritrophic interactions plant-herbivore -parasitoid in agroecosystems may help to improve biological control programs (Hunter 2003). To evaluate the effect of water stress on the third trophic level, we studied the preference and performance of Aphidius ervi, an aphid parasitoid, when parasitizing its two aphid hosts Acyrthosiphum pisum and Sitobion avenae when host plants were subjected to drought.

Material and Methods

Biological materials

Two aphid species were tested: Acyrthosiphon pisum on the fava bean (Vicia faba L.) and Sitobion avenae on the common wheat (Triticum aestivum L.). Both colonies were initiated from individuals collected in Brittany, France. They tested negative for secondary bacterial symbionts (Monticelli, Nguyen & Desneux, unpublished data) when screened for main ones known to provide stress adaptability in aphids [START_REF] Oliver | Parasitic wasp responses to symbiont-based defense in aphids[END_REF]. The endoparasitoid Aphidius ervi (Haliday) was reared on Acyrthosiphon pisum, and both aphid and parasitoid species were reared in a growth chamber at 22 ±2 °C, 65 ± 5 % relative humidity (RH) and 16:8-h light:dark (L:D). Mummies of Aphidius ervi were collected and kept in the dark at 22°C until adult emergence. New emergent parasitoids were captured and transferred into a 3-cm diameter cylindrical tube in a 1:1 ratio and were fed with a water solution containing 50% honey. After 24 hours, the mated females were isolated in gelatin capsules before the no-choice test (see below).

Plant water treatment and infestation by aphids

Plants were grown from seeds in a climatic chamber (24 ± 1°C, 65 ± 5% RH, 12:12-h L:D) in plastic pots (9 × 9 × 10 cm) containing organic soil and limestone grains using a 1:1 ratio. A nutrient solution was used to water plants. For a 100-L stock solution, we added 12.5kg Ca(NO3)2, 0.5kg NH4NO3, 7.5kg KNO3, 3.5kg K2HPO4, 1kg K2SO4, 1.5kg MgSO4, 3L HNO3, 1.5L H3PO4. Micronutrients were provided in the form of 3L Kanieltra 6 Fe (Hydro Azote, Nanterre, France), and iron was supplied by 2.8L of EDTA-Fe. The stock solution was then diluted with tap water using a ratio of 5L per 100L final volume to obtain the final irrigation solution. One week after sowing, bean and wheat seedlings reaching four to eight centimeters in height, were transferred under laboratory conditions (23 ± 2 °C, 65 ± 5% RH and 16:8-h L:D). One-week-old bean and wheat plants were randomly assigned two water levels: 30% and 100% water volumes (referred to as water stress and control conditions).

Both stressed and control plants received the same amount of the necessary nutrient solution for the highest level stressed plants; Control plants then received tap water to reach their irrigation levels. The purpose was to maintain the same amount of nutrients and only to vary the volume of water each plant received during the experiments.

Three weeks after the beginning of the water treatment, wheat and bean plants were offered to aphid colonies in well aerated 60x60x60cm mesh cages. New experimental colonies were initiated by introducing fourth-instar aphids into the control and water stress plant cages until new aphid generations appeared. Aphid parents were then removed. Aphid colonies were maintained from five to ten generations until the experiments ended. New 3week treated wheat or beans were added each week and stayed from one to two weeks in the cages before being replaced. The aphids were used for no-choice host specificity testing as described by Desneux et al. (2009a).

Plant traits: height and leaf mass area

Plant height and leaf mass area (LMA) were recorded before infestation. The LMA (g.m -2 ) is calculated as the dry leaf mass divided by the leaf area. To calculate the leaf area, we cut off leaves, flattened them between transparent plastic sheets, scanned (Sharp MX-3140 scanner) and measured with the ImageJ freeware. The leaves were then put in an oven for 24 h at 70°C and were weighted.

Experiment 1: Host acceptability and preference

We used a no-choice bioassay (adapted from Desneux et al. 2009Desneux et al. , 2012) ) to study parasitoid female host selection behavior, i.e. preference). Female preference was divided into three action steps, from the first contact with the host to the actual stinging of the host. These actions were defined to categorize female parasitoid behaviors when encountering tested hosts : (1) detection -when the parasitoid touched the aphid with its antenna; [START_REF] Calvo | The performance of an aphid parasitoid is negatively affected by the presence of a circulative plant virus[END_REF] acceptance -when the female bent its abdomen and attacked aphid hosts (3) successful stinging -when the female inserted its ovipositor inside the aphid and withdrew it (often resulting in aphid movement). To observe parasitoid behavior, we placed one aphid, and one female parasitoid in a 3-cm diameter and 1-cm high dome. They were both naive and had never been in contact with their counterparts to avoid learning-by-experience impacts.

All insect behaviors were noted for 5 minutes or until successful stinging had taken place.

The standard aphid size was chosen based on the size of the 2 nd Acyrthosiphon pisum instar, known as the preferred instar host of Aphidius ervi [START_REF] Sequeira | Variation in Selected Life-History Parameters of the Parasitoid Wasp, Aphidius-Ervi -Influence of Host Developmental Stage[END_REF]. 30-36 replicates were performed for each aphid species and each watering conditions in experiment 1.

Experiment 2: Host suitability and performance Innate parasitoid performance is determined by the survival of the immature parasitoid stages (egg, larvae, and pupae) inside aphid hosts. To follow up stung aphid development, the aphids previously stung during Experiment 1 (see above) were reared individually in clip cage system on leaflets of water stress or control plants (according to the sources of host aphids tested) for 15 days or until mummification. The clip cages made from 100-μm-poresize Corning® cell strainer (Corning, Inc) were adapted from standard clip-cages (e.g. [START_REF] Mouttet | Phytophagous arthropods and a pathogen sharing a host plant: evidence for indirect plant-mediated interactions[END_REF]. Additional replicates were carried out without behavioral observations to obtain sufficient replicates for the follow-up survival test. The number of mummies, adults and the sex ratio of parasitoids was recorded. 51-89 replicates were performed for each aphid species and each watering conditions in experiment 2.

Statistical analyses

All statistical analyses were performed using R.3.3.3 software (R Core Team, Vienna, Austria 2009). Effect of water treatment on plant height and plant leaf mass area was tested using ANOVA. The proportion of aphids detected, accepted and successfully stung were compared per aphid species using pairwise Fisher tests, with Bonferroni adjustment for multiple comparisons. The proportion of each parasitoid developmental stage and the sex ratio was also analyzed per aphid species using pairwise Fisher tests, with Bonferroni adjustment for multiple comparisons.

Results

Impact of water stress on plant traits: height and leaf mass area (LMA).

Bean and wheat heights were significantly impacted by water stress treatment. Bean height was severely reduced by 27.5% (37.47cm ± 1.53 vs. 27.16cm ±0.88) (F1,18 = 35.61, P < 0.01) and wheat height was decreased by 9% (35cm ± 1.48 vs. 32cm ± 0.78) (F1,26 = 5.8, P = 0.02) (Figure 1,A). Moreover, the wheat LMA was reduced by 15% in comparison to control samples (F1,23 = 7.2, P = 0.013) (Figure 1, B). However, there was no evidence of impact of water stress on the bean LMA (F1,54 = 0.5, P = 0.825).

Impact of water stress on A. ervi preference and performance

Experiment 1: Preference -Detection, acceptance and successful sting rates of A. ervi on aphids A. pisum and S. avenae were not impacted by the water stress treatment (Fisher exact test: P > 0.05) (Table 1). The proportions of A. pisum detected, accepted or stung by A.

ervi were always higher than 0.9 regardless of water treatment. The proportions of S.

avenae detected, accepted or stung by A. ervi were consistently higher than 0.80 regardless of water treatment.

Experiment 2: Performance -When A. ervi parasitized A. pisum, the number of eggs and larvae found during dissections, as well as mummies produced and adults emerging did not change significantly in function of water stress (Fisher exact test: all P > 0.05) (Figure 2A).

When Aphidius ervi encountered S. avenae on well-watered plants, there was no parasitoid mortality (Fisher exact test: all P > 0.05) (Figure 2B). By contrast, there was parasitoid mortality at the mummy stage as adult emergence significantly reduced under water stress, from 0.63 aphids containing a parasitoid egg to 0.29 adults emerging (Fisher exact test: P < 0.01). The sex ratio of parasitoid adults emerging from A. pisum (control: 0.88, water stress: 0.74) or S. avenae (control: 0.72, water stress: 0.79) did not differ as function of water treatments (P = 0.22 and 0.35, respectively).

Discussion

The bottom-up effect of water stress on the aphid parasitoid Aphidius ervi was assessed when encountering two different aphid species on two host plant species. The experimental design efficiently enabled the water stress to affect the plants; plant height was decreased for both plants, as well as leaf mass area in the case of wheat. The cascade impact of this abiotic stress, through host plant of aphid hosts, varied depending on the aphid-plant system considered. Successful parasitoid offspring development reduced when A. ervi was tested on S. avenae reared on water-stressed wheat vs. well water wheat plant. By contrast, no impact of such abiotic stress was detected when comparing offspring development of A.

ervi on A. pisum on stressed vs. well-watered bean plants. Also, there was no bottom-up effect on parasitoid preference (behaviors) when parasitoid encountered the two aphids on water-stressed plants vs. well-watered ones; parasitoid females did not adjust their behavior according to potential bottom-up effect occurring in the host-plant systems they were subjected.

Typical parasitic behaviors of pro-ovigenic parasitoids A. ervi, i.e. short lifespan and initial large egg load at adult emergence such as A. ervi (Dieckhoff et al. 2014) may explain, to some extent, the low choosiness of parasitoid female when encountering aphids on water-stressed plants. Pro-ovigenic parasitoids tend to accept stinging in most encountered host species belonging to the tribe of their preferred host (Desneux et al. 2009a;2009c;[START_REF] Monticelli | Preference-performance relationship in host use by generalist parasitoids[END_REF]. Water stress applied to bean plant did not impact parasitoid offspring performance on Acyrthosiphum pisum. Therefore the parasitoid females did not need to lower their oviposition rate when encountering hosts despite that these hosts were feeding on plants under suboptimal growth conditions (e.g. see Figure 1). By contrast, offspring development was affected when Aphidius ervi parasitized S. avenae on water-stressed wheat plants (decreased survival at pupae stage), but parasitoid females did not lower their oviposition on these potentially suboptimal hosts. It remains unclear whether parasitoid females were not able to identify S. avenae on water-stressed wheat as suboptimal hosts or if female parasitoids recognized them as suboptimal ones but decided to sting these hosts anyway. A. ervi is an intermediate specialist [START_REF] Monticelli | Preference-performance relationship in host use by generalist parasitoids[END_REF] and is partially able to avoid suboptimal hosts. The lower rate of eggs recovered during dissections in stung S. avenae on water-stressed wheat vs. on those on regular wheat plants may hint that A. ervi females did identify the suboptimal hosts and adjusted their selectiveness partially.

Few studies have evaluated the impact of aphid nutrition status on immature parasitoid development and field observations suggested lower parasitoid performance, notably reduced offspring production, of aphids and parasitoid populations under drought stress (Aslam et al. 2013, Romo andTylianakis 2013). Three potential mechanisms may explain bottom-up effects of water stress on parasitoid performance [START_REF] Kaplan | Indirect plant-parasitoid interactions mediated by changes in herbivore physiology[END_REF]): (i) increased sequestration of plant toxins in hosts, owing to a shift in resource allocation from primary to secondary metabolism in water-stressed plants (Mewis et al. 2012); (ii) reduced resource availability for parasitoid offspring development; such effect may cascade from the first mechanism as primary plant metabolism reduced in stressed plants, and it may cascade to lower resources for aphids, and (iii) modulation of host immunity owing to presence of plant toxins.

The two first mechanisms may explain, in part, the lower performance of A. ervi on S.

avenae when developing on water-stressed wheat plants. Both Acyrthosiphum pisum and S.

avenae use general and specific proteins that interfere with plant defensive pathways during feeding [START_REF] Urbanska | Phenol oxidising enzymes in the grain aphid's saliva[END_REF], Rao et al. 2013). However, A. pisum produces metalloproteases in saliva, and this does not occur in the case of S. avenae [START_REF] Carolan | The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry[END_REF], Will et al. 2013). These proteases break down plant phloem proteins into smaller nitrogen compounds used for both modulation-suppression of plant defensive hormones and plant feeding [START_REF] Furch | Direct and individual analysis of stress-related phytohormone dispersion in the vascular system of Cucurbita maxima after flagellin 22 treatment[END_REF][START_REF] Furch | Aphid salivary proteases are capable of degrading sieve-tube proteins[END_REF]; they may lower potential adverse bottom effects toward parasitoid developing in A. pisum on water-stressed plants. It might contribute to A. pisum resistance to plant nitrogen depletion under drought conditions and may have enabled Aphidius ervi to develop well in this host whereas parasitoid offspring development in S. avenae may have been impaired owing to accumulated secondary metabolites and/or reduced proteins availability in this aphid. Such observation still may have to be confirmed by measures of toxins and/proteins content in S. avenae developing on water-stressed plants vs. wheat cropped in well-watered conditions.

Reduced aphid size, as well as general resource availability in host aphids, could also be a factor underneath suboptimal development of parasitoid offspring in S. avenae. There is a positive relationship between plant vigor and herbivore weight in phytophagous arthropods as well as between their weight and potential parasitoid size (Teder and Tummaru 2002). Parasitoids could fail to develop in small hosts owing to low-poor resource availability (Godfray 1994). Sitobion avenae size may be caused by poor plant quality and could be responsible for the reduction of A. ervi parasitism rate under drought stress.

However, aphid length data are lacking to validate this hypothesis in our study. Also, host size may impact parasitoid fitness by modulating sex ratio, i.e. inducing a male-biased sex ratio; parasitoid females lay preferentially more female eggs in large hosts and males in small ones (Godfray 1994). Sex ratio did not vary when A. ervi parasitized the two aphid species on well-watered plants and water-stressed ones, suggesting that A. ervi did not discern or consider the variability in host quality. All in all, a shortage of resources needed to complete parasitoid development in aphid is thought to affect parasitoid offspring mostly at the pupae stage, notably at the time the larvae produce silk for mummy cocoon (Desneux et al. 2009a) whereas sequestration of toxins by aphids proved to be lethal mostly for younger offspring (from egg to larvae or from larvae to pupae). Therefore, reduced development of A. ervi in S. avenae may be more likely linked to diminished host food quality and/or quantity rather than sequestration of toxins by this aphid on the water-stressed wheat plant.

LMA is an important trait in predicting plant adaptability strategies and/or mortality pattern under changing environments (Poorter et al. 2009, Anderegg et al. 2016). Wheat plants under stress had a lower height, and higher LMA than well-watered plants (e.g. Blum and Sullivan 1997) and changes in leaf chemical composition mediated by LMA might reflect the change(s) occurring in the vascular system on which aphids fed (Auclair 1963, Will et al. 2013). LMA in herbaceous plant correlates positively to leaf carbon concentration but negatively to leaf nitrogen concentration, organic acids and protein concentration (Poorter et al. 2009, De La Riva et al. 2016). Plants with higher LMA are associated with lower N content, and it may lower aphid feeding efficiency and subsequently its quality as host for parasitoid. By contrast, bean height was lower, and its LMA did not alter under the water stress. Beans tend to avoid drought by reducing evaporation surface and leaf stomatal conductance which is the most significant morphological adaptation in this species [START_REF] Lizana | Differential adaptation of two varieties of common bean to abiotic stress: I. Effects of drought on yield and photosynthesis[END_REF], Lonbani and Arzani 2011[START_REF] Beebe | Phenotyping common beans for adaptation to drought[END_REF]. Beans did not show increased LMA, suggesting a lower impact of water stress on plant physiology in bean; it may explain the lack of bottom-up effect on A. ervi parasitism when encountering Acyrthosiphum pisum on water-stressed host plants. However, the use of the LMA trait for drought adaptability is insufficient and controversial because of plant diversity and the nature of the stress (Marechaux et al. 2015, He and[START_REF] He | Drought effect on plant nitrogen and phosphorus: a metaanalysis[END_REF]. Further research will require more plant physiological traits to be measured, e.g. photosynthesis and C/N ratio, to deepen our understanding of mechanisms underlying plant stress survival and potential cascading effects toward second and third trophic levels.

The present study stressed the importance of abiotic conditions in plant-herbivoreparasitoid interactions and notably host use by parasitoids. Bottom-up effects may cascade to third trophic level and modulate performance of parasitoids when parasitizing their hosts. Such effects may have a broad impact on insect communities, e.g. it may affect diet breath of parasitoids through narrowing their host range making suitable hosts to turn into poorly suitable or unsuitable ones. (Wiens 2016); the community shift direction and quantitative impacts of community shift on the wild and agricultural ecosystems (Devictor et al. 2010;[START_REF] Moe | Combined and interactive effects of global climate change and toxicants on populations and communities[END_REF]. The tri-trophic plant-aphid-parasitoid system is a good biological model in both ecology and application because of the biodiversity of insects in the terrestrial ecosystem, the tight co-evolution of organisms within the complex and the importance of parasitoid in biological OW as natural enemies against aphids (Loxdale et al. 2011). The host specificity of a parasitoid is its ability to exploit aphid hosts. It is shaped by parasitoid preference (host acceptance) and parasitoid performance (host suitability) which are influenced by aphid quality, aphid food source, plant quality and interactions within this system (Desneux et al. 2009;Desneux et al. 2012;Godfray 1994;Klinken 1999;Poulin and Mouillot 2005). The diet of aphid hosts can affect host suitability for immature aphid parasitoid, however, evidences are scarce. Soil nitrogen fertilizer could improve parasitoid fitness at moderate quantity (Aqueel et al. 2015).

Water stress is among most severe abiotic stresses in current decades. It affects 45% of global farming lands, is predicted to increase at both intensity and frequency [START_REF] Long | More than taking the heat: crops and global change[END_REF], causes nearly 20% agriculture damage (FAO 2015) and biodiversity loss (Archaux and Wolters 2006). Field observations of aphid and their parasitoid populations under water stress suggest a depletion in parasitoid performance (Aslam et al. 2013;Romo and Tylianakis 2013). The water availability mediated by plants triggers a change in population and community structure at the top level (Han et al. 2015a;Han et al. 2015b;Hunter and Price 1992). The outcomes of stress-based modifications at natural enemy level may be predicted by variations in plants which directly affect natural enemies or mediate the variations in aphid quality as hosts, e.g. through reduction of plant volatiles such as synomones under water deficiency (Aslam et al. 2013;[START_REF] Dias | Bottom-up effects on a plantendophage-parasitoid system: The role of flower-head size and chemistry[END_REF]Tariq et al. 2013;Weldegergis et al. 2015). Impacts of abiotic stress on parasitoid may also be mediated by aphids such as modifications in aphid availability (density), nutritional quality (size and content), defenses (by morphology, immune system or symbionts), and growth rate, i.e. lower host density) because of plant morphological, physiological and chemical modifications (Hunter 2003). The overall effects may be either negative or positive on aphid performance but often remain unclear for parasitoids. Several studies reported no impact of fruit fly [START_REF] Martinez-Ramirez | Nutrient uptake and allocation capacity during immature development determine reproductive capacity in Diachasmimorpha longicaudata (Hymenoptera: Braconidae: Opiinae), a parasitoid of tephritid flies[END_REF]) and leaf miner (Dong et al. 2018) parasitoids. On the negative side, plant biomass loss and plant poor nutrient contents relate to the reduction of aphid population and performance (Johnson et al. 2011;McVean and Dixon 2001;Mewis et al. 2012;[START_REF] Simpson | The response of aphids to plant water stress -the case of Myzus persicae and Brassica oleracea var. capitata[END_REF]. Plant trichome increase contributes to plant resistance against herbivores [START_REF] Glas | Plant Glandular Trichomes as Targets for Breeding or Engineering of Resistance to Herbivores[END_REF][START_REF] Handley | Variation in trichome density and resistance against a specialist insect herbivore in natural populations of Arabidopsis thaliana[END_REF]). In the positive side, stomatal plant closure improves aphid feeding under elevated CO2 [START_REF] Sun | Plant stomatal closure improves aphid feeding under elevated CO2[END_REF]. The plant traits variations are determined by plant defense strategies under a combination of stresses and their nature such as intensity and frequency. Under abiotic stress and aphid infestations, plants can produce both more or less defensive allelochemicals. For example, glucosinate concentration in cabbage and cardenolide in milkweed are reduced under water stress, respectively [START_REF] Khan | Influence of water stress on the glucosinolate profile of Brassica oleracea var. italica and the performance of Brevicoryne brassicae and Myzus persicae[END_REF]Mewis et al. 2012). By contrast, the secondary pathways in plants could also be activated under stress to produce more insecticidal toxins, e.g. phenolic compounds [START_REF] Caretto | Carbon Fluxes between Primary Metabolism and Phenolic Pathway in Plant Tissues under Stress[END_REF]. Those toxins could delay the growth of phytophagous insects as well as making them more susceptible to natural enemies (Ibanez et al. 2012).

Bottom-up effects may also impair endosymbionts harbored by aphids, thus possibly making them more vulnerable to parasitism (Cayetano and Vorburger 2013). However, these allelochemicals can even be sequestered by specialist herbivores and be used as protection against parasitism and/or predation (Züst and Agrawal 2015). So far, previous studies hinted that bottom-up effects on host-parasitoid relationships could not be readily generalized and inferred from plant responses to a specific individual stress (Suzuki et al. 2014); the studies assessing potential bottom-up effects should be carried out using a range of tri-trophic complexes under well-defined stress conditions to enable providing broad significance.

In the present study, we studied the impact of a bottom-up force, the water stress, on critical determinants of host specificity (Desneux et al. 2009) of the specialist-generalist aphid parasitoid Aphidius ervi. Based on a previous study on A. ervi diet breath [START_REF] Monticelli | Preference-performance relationship in host use by generalist parasitoids[END_REF], we selected six aphid -host plant complexes to assess the impact of water stress on the parasitoid host specificity: Acyrthosiphon pisum -bean, Sitobion avenaewheat, Rhopalosipum padi -wheat, Myzus persicae -cabbage, Aphis nerii -milkweed, and Macrosiphum euphorbiae -potato. They were chosen as meeting one the following criteria in the absence of water stress [START_REF] Monticelli | Preference-performance relationship in host use by generalist parasitoids[END_REF]): (i) high quality host, i.e. high parasitoid offspring survival until adulthood, or (ii) suboptimal host, i.e. average mortality occurring before adult emergence. These two conditions should enable detecting possible adverse effects (case i) and positive effects (case ii) on parasitoid offspring development, notably owing potential modifications in plant biochemistry and/or host aphid physiology (which is known to impair parasitoid development at larva stage, Desneux et al. 2009). Also, life-history traits of aphids and plants were recorded to further depict results on parasitoid host specificity under bottom-up force conditions. The central hypothesis was tested: (i) parasitoid females may show lower preference toward hosts under bottom-up force owing to decreased quantity and/or quality of chemical cues from host aphids and/or plants, (ii) parasitoid performance would increase on generalist aphids fed on toxic plants and decrease on aphids fed on non-toxic plants, (iii) the relationship preference-performance could change under water stress impacts.

MATERIELS AND METHODS

Biological system

The parasitoid Aphidius ervi (Haliday) was reared on Acyrthosiphon pisum for 20 generations in a growth chamber (23 ±2 °C, 65 ± 5 % RH, 16:8-h L: D). The host specificity of A. ervi was tested in six aphid-plant complexes under two water regimes: optimal water supply (OW) and limited water supply (LW), the irrigation volumes were 100% and 30% of saturated soil volume for five species except for Myzus persicae 70% and 30% of saturated soil volume was applies. The six complexes were: Acyrthosiphon pisum (Harris) on fava bean, Vicia faba L. (referred as Ap100 and Ap30 for OW and LW); Sitobion avenae (Fabricius) and Rhopalosiphum padi (Linnaeus) on common wheat, Triticum aestivum L. (Sa100 and Sa30, R. padi100 and R. padi30, respectively); Myzus persicae (Sulzer) on cabbage, Brassica oleracea var. capitate (M. persicae70 and M. persicae30); Aphis nerii (Boyer de Fonscolombe) on milkweed, Asclepias incarnata (An100 and An30) and Macrosiphum euphorbiae (Thomas ) on potato, Solanum tuberosum (Me100 and Me30).

Impacts of water stress on plants

Plant water stress treatment -The water stress treatment was applied from the previous study of Nguyen, LTH, et al., (2018, in prep). The experimental plants were grown from seeds in a climatic chamber (23 ±2 °C, 65 ± 5 % RH, 12:12-h L:D) in plastic pots (9 × 9 × 10 cm) containing organic soil (Terreau Horticole Bio Tonusol, Agriver, France) and limestone grains (Perlite Italiana Srl, Corsico, Italy) in ratio 1:1. The quantity per pot was five seeds/pot for bean, ten seed/pot for wheat, one seed/pot for other plants. The term 'stres is used here when, for any reason, plant performance in module growth is reduced below that achieved under optimal conditions. The water supply volume for OW plants was determined during preliminary experiments where we LW plants with four water levels: 30%-, 50%-, 70%-and 100% of soil-saturated volume and then we measured plant parameters to find the optimal conditions showing highest plant biomass and metabolism. One week after sowing, plant germinations of 4-8 cm height were transferred under laboratory conditions (23 ±2 °C, 65 ± 5 % RH, 16:8-h L:D). One-week-old bean, wheat, milkweed, and potato were randomly assigned to two water levels: 30% and 100% of soil-saturated volumes (referred as water stress and OW or 30% and 100%). The exceptional case is cabbages of which the OW was 70% of soil-saturated volume because cabbage metabolism decreased at 100% volume irrigation similar to the water stress symptom. The treatments were started three weeks before aphid infestation and was maintained continuously. LW and OW were kept on tested plants during all experiments as well.

Plant morphology measurements -Plant morphological parameters including height and leaf mass area were measured each week. Plant height and number of nodes or stem leaves were measured from the soil surface. Leaf mass per area (LMA) was calculated by dry mass divided by leaf area. The leaves were cut off and flattened between transparent plastic leaflets and then scanned by a Sharp MX-3140 scanner. Leaf area (cm²) was calculated using the freeware ImageJ.

Leaf gas exchange measurement -Non-destructive measurements of leaf photosynthesis rate based on net CO2 assimilation (AN), transpiration rate (E) and stomatal conductance (gs) were performed. We chose the 4 th or 5 th young leaves from the stem which provides optimal aphid feeding and proved suffering water limitation long enough during preliminary experiments.

One leaflet per plant was analyzed using a photosynthesis system (Li-6400, Li-Cor, Lincoln, NE, USA) equipped with a light source (6200-02B LED, LiCor). Leaflets first were acclimatized in the chamber for more than 20 min under controlled conditions: leaf temperature of 27.0 ± (SE) 0.1 C, CO2 air concentration of 500 ± 0.04 μmol , and saturating photosynthetic photon flux density (PPFD) of 700.04 ± 0.05 μmol hν . The light intensity of 700 µmol m 2 s 1 PAR is high enough to stimulate leaf transpiration and is closer to the laboratory light condition. Relative humidity was maintained between 10% and 50% in the cuvette for all measurements.

After detecting a significant difference in at least one of morphological or metabolic parameters, we transferred plants to aphid-feeding cages. Infestation periods were determined for each plant by preliminary tests. Intrinsic water use efficiency (AN/gs) was calculated as the ratio between leaf photosynthesis rate (AN) and leaf stomatal conductance (gs) as the study of [START_REF] Medrano | From leaf to whole-plant water use efficiency (WUE) in complex canopies: Limitations of leaf WUE as a selection target[END_REF].

Bottom-up effect of water stress on aphids

Plant infestation -LW and OW plants were offered to aphid colonies in a cage of the dimension 60x60x60cm covered by mesh placed in a climatic chamber (23 ±2 °C, 65 ± 5 % RH, 16:8-h L:D). We initiated new colonies by introducing 4 th instar aphids into the cage of OW and LW plants until the reproduction of new generations. Aphid parents were then removed. Aphid colonies were maintained for 5 to 10 generations until experiments ended.

New plants were added every week and stayed from 1 to 2 weeks in the cages before being removed. All plant metabolism and morphology were measured (see above) prior aphid infestation to make sure LW plants were effectively under water stress.

Aphid performance: survival rate, generation time (D), and the intrinsic rate of increase (rm).

We evaluated aphid performance on LW and OW plants on three parameters: The survival rate, the generation time (D), and the intrinsic rate of increase (rm) was calculated as described by [START_REF] Wyatt | Simple Estimation of Intrinsic Increase Rates for Aphids and Tetranychid Mites[END_REF]van Emden and Harrington 2007). We placed ten 4 th

Bottom-up effect of water stress on parasitoids

Parasitoid preference: no-choice test -We conducted the parasitoid specificity test as previously described by Desneux et al. (2009) to test behavioral and physiological traits of parasitoids on potential aphid hosts. This test design included observing the behaviour of aphids and parasitoids when they individually encounter in a small area of 3-cm diameter, 1cm height -dome. Parasitoids were one-day-emerged, mated and naive. Aphids were standardized by size equal the second instar of A. pisum, the natal parasitoid host. The standard size was chosen based on relative size of different aphid colonies and the preferable host instar of A. ervi while parasitizing A. pisum.

The host selection process, i.e. female preference) was divided into 3 steps, each with a perceptible representative sign: (1) detect (when the parasitoid touched the aphid either by antenna or leg) -accept (when the female bent its abdomen and attacked aphid hosts, following or not by aphid defense) -successful sting (when the female inserted its ovipositor inside the aphid and withdrew it resulting in aphid movement). After one successful sting, aphids were removed from the dome immediately for not being super parasitized by A. ervi. Aphid defensive behaviors were recorded as antennal push, cornicle secretion, kick or rotation (Desneux et al. 2009). All insect actions were noted as described above until 5 minutes or until successful sting, depending on what happened first. A. ervi females were aggressive toward aphids during our experiments, so 5-minute length is enough to complete their host selection process in a small dome.

Parasitoid performance: sequential dissection -To follow up immature parasitoid development, stung aphids from plants under limited water supply and optimal water supply conditions (from the previous behavioral assay, see above) were individually reared in the clip cage system on leaflets belonging to their respective plant treatment, i.e. LW or OW). Two third of stung aphids were then sequentially dissected to find the egg and larval survival at 1-and 5-day after being stung, respectively. The remaining 1/3 were kept in clipcaged for up to 15 days, or until mummy formed, the emergence rate and the survival aphids from parasitism were then recorded. We repeated the dome experiment without actual behavioral observations to increase the number of replications for this assay. To analyze the correlation between preference and performance for A. ervi, we considered the successful stung ratio per total observed aphids as a proxy of parasitoid preference and the adult emergence rate per stung aphids as a proxy of parasitoid performance.

Statistical analysis

Impact of the water limitation on plant height, plant leaf mass area and leaf gas exchange was analyzed using factorial ANOVA. The impact of water stress on aphid generation time and intrinsic rate of development was examined using factorial ANOVA. The impact of water stress on aphid survival rate and other life history traits was analyzed using Fisher exact test.

Each trait was compared in pairs between LW and OW plants. The relationship between parasitoid preference for and performance on aphids feeding on LW or OW plants was analyzed using logistic regression with a binomial distribution. Detection, acceptance and sting rates were compared, per species for each water treatment, using pairwise compared using permuted Fisher Exact test with Bonferonni adjustment method. Similar analyze method was used to compare the proportion of aphids containing an egg, larvae, producing a mummy and adult. All tests were performed using R software (R Core team). All graphics were processed using Prism 5 software (GraphPad Software Inc 2007). Impact of water limitation on the parasitoid A. ervi (Figure 4A,B)

Parasitoid survival rate -The survival of parasitoid at mummy stage and adulthood was significantly reduced when developing on S. avenae, and M. persicae reared on water stress plants (LW) when compared to those reared on optimal water conditions (OW) (Table 3: survival until mummy stage: S. avenae, p value = 0.006, M. persicae, p value = 0.038; survival at adulthood: S. avenae, p value = 0.029, M. persicae, p value = 0.030). The survival until adulthood was notably reduced by 85% and 40% when developing in M. persicae and S.

avenae subjected to water stress-related bottom-up effect, respectively. The similar pattern was observed in M. euphorbiae though it was only marginally significant (survival until mummy stage: p value = 0.075, survival at adulthood: p value = 0.088). The water stress did not show a significant effect on parasitoid development in other aphid species tested (all p value > 0.05).

Correlation preference -performance (table 5) -There was a significant preferenceperformance correlation when A. ervi was parasitizing aphids reared in optimal watering conditions (OW, p value = 0.002, R²= 0.71). By contrast, this relationship was weaker when aphids were reared on plants suffering water stress (R²= 0.45), and there was no significant correlation anymore (p value = 0.071).

DISCUSSION

In the present study, testing six aphid species as potential hosts and generating bottom-up effects on host aphids through varying water stress in host plants, we demonstrated that bottom-up effects effectively occurred on parasitoid host specificity and that it can modulate its actual host range. The parasitoid choosiness was not drastically affected by bottom-up effect while host suitability for parasitoid offspring development was decreased in three out of the six aphid species tested. Water stress did negatively affect plant primary metabolism-related mechanisms, e.g. leaf transpiration rate and stomatal conductance, and it proved to cascade to the second trophic level, i.e. the aphids; their development speed and growth were decreased for half of aphid species considered. Adverse bottom-up effects observed on aphid hosts were linked to subsequent parasitoid performance on these hosts, except for sone aphid species, those showing reduced survival, generation time and/or intrinsic rate of population increase (rm) proved to be suboptimal hosts for the parasitoid when plants were suffering water stress. This research highlights that actual parasitoid diet breath observed in wild conditions largely depend on abiotic factors impacting parasitoids themselves but also through less intuitive effects occurring through both host plants and hosts owing to bottom-up forces.

Parasitoid preference under bottom-up force

We demonstrated that preference traits of the aphid parasitoid [START_REF] Harvey | Flexible Larval Growth Allows Use of a Range of Host Sizes by a Parasitoid Wasp[END_REF]Sequeira and Mackauer 1992). In other insect families, poor host food quality increases parasitoid larval mortality [START_REF] Brodeur | Functional ecology of immature parasitoids[END_REF][START_REF] Jonasson | Parasitoids of Delia root flies in brassica vegetable crops: coexistence and niche separation in two Aleochara species (Coleoptera: Staphylinidae)[END_REF]). Besides, low quality of egg and pupae as parasitoid hosts affected immature parasitoid survival [START_REF] Panizzi | Insect Bioecology and Nutrition for Integrated Pest Management (IPM)[END_REF] or supplement proteins enhance reproduction in an ectoparasitoid [START_REF] Harvey | Honey and honey-based sugars partially affect reproductive trade-offs in parasitoids exhibiting different life-history and reproductive strategies[END_REF] thus suggesting the role of host protein composition in successful parasitoid development.

Another possible mechanism underneath may be a decrease in density of the endosymbiont Buchnera in aphids feeding on low-quality plants. The venom the female parasitoid injects into its host while oviposition plays the role of aphid castration completed by tetratocyte production, to redirect host nutrients to its larva; notably enhancing benefits from the metabolism of the obligate aphid symbiont Buchnera toward parasitoid needs (Pennacchio and Mancini 2012;Strand 2014). Moreover, there is evidence that parasitoid could manipulate the abundance of the primary symbiont Buchnera, from the egg and larval stage (Martinez et al. 2014).

Parasitoid larval mortality may occur through sequestration of plant toxins via aphids [START_REF] Mooney | The Tri-Trophic Interactions Hypothesis: Interactive Effects of Host Plant Quality, Diet Breadth and Natural Enemies on Herbivores[END_REF]. However, plants could both induce or decrease their toxin production as a strategy to tolerate water stress. Plants then reallocate resources and increase their defense via secondary metabolism, resulting in aphid host less palatable for parasitoids (Mewis et al. 2012). Aphids may sequester specific toxins against their natural enemies [START_REF] Goodey | Aphids Pick Their Poison: Selective Sequestration of Plant Chemicals Affects Host Plant Use in a Specialist Herbivore[END_REF] also not always occurring, e.g. increase of plant toxins may negatively affect aphids without reaching parasitoids (Le [START_REF] Guigo | Plant-mediated effects on a toxin-sequestering aphid and its endoparasitoid[END_REF]). Among the plants used in the study, cabbage, milkweed, and potato belong to the families of Brassicaceae, Asclepias, and Solanaceae, respectively; all are well-known for their constitutive toxic compounds. The tissues of cabbage contain glucosinolates (sulfur derived compounds), Solanaceae contains glycosidic alkaloids (tomatine, solanine) and milkweeds contain cardenolides. However, the impact of water limitation on aphid performance on those plants is not similar. Different mechanisms might explain the results. For the M. euphorbiae-potato complex, the trichome increases and prohibit aphids from plant feeding, therefore the mortality of aphids on LW plants are relatively high (>60% under LW conditions vs. <20% under OW conditions).

Decreased M. persicae performance on cabbage occurred owing to known reduced plant nutritional quality and increased glucosinate concentration which M. persicae tolerates only at low concentration (Ali and Agrawal 2012). By contrast, the performance of A. nerii on milkweed was not affected by water limitation, suggesting a tolerance to plant responses in this aphid. Besides, the status of the low-quality host of this species for A. ervi did not change to a better owing to bottom-up effect. There was a similar case for another low-quality host for A. ervi: the aphid R. padi developing on wheat did not show increased suitability for A. ervi when developing on water stress plants. These occurred despite the apparent negative impact of bottom-up effect on the aphid itself; higher mortality occurred likely owing to increased wheat leaf rigidity (see LMA results).

Finally, impairment in host metabolism regulation by the parasitoid may explain also partially reduced the performance of A. ervi offspring when developing in hosts suffering water-stress bottom-up effect. Parasitoid female could manipulate host metabolism and adjust host nutritional balance to meet their larval dietary needs. The development, survival, and fitness of the parasitoid offspring depend on regulatory factors they inject into the host during oviposition including teratocytes, venoms, polydnaviruses and virus-like particles [START_REF] Harvey | Intrinsic Inter-and Intraspecific Competition in Parasitoid Wasps[END_REF][START_REF] Poirie | Virulence strategies in parasitoid Hymenoptera as an example of adaptive diversity[END_REF]. Such disturbance may have occurred in the case of A. ervi developing in M. persicae feeding on water stress plants as we observed mortality at larval and mummy stages.

It remains unclear why A. ervi was not affected when developing in A. pisum suffering water stress bottom-up effect. Various mechanisms may explain this result. First, bean plants are well tolerant to water stress thank their nitrogen fixation symbionts [START_REF] Laranjo | Legume growth-promoting rhizobia: An overview on the Mesorhizobium genus[END_REF], which induce plant nitrogen fixation and trehalose under stress. These both compounds increase plant stress tolerance [START_REF] Lunn | Trehalose metabolism in plants[END_REF]. Second, photosynthesis rate of beans was maintained under water limitation conditions, the same as wheat and potato in our experiments. Differently, bean morphological palatability did not impact (like in wheat which increased leaf rigidity, or potato which produced more trichomes). Third, A.

pisum was the natal host for A. ervi, and it may be more adapted to potential variations occurring in this particular host.

Pattern of correlation preference -performance

The correlation between parasitoid preference and performance at optimal water condition proved that female A. ervi could detect low-quality hosts and avoid parasitizing those in some extent (in concordance with our previous results, [START_REF] Monticelli | Preference-performance relationship in host use by generalist parasitoids[END_REF]. However, when the aphid-plant systems were subjected to a bottom-up effect, water stress in our study, the preference-performance was weakened. The capacity of host evaluation of A. ervi may be disturbed when encountering hosts suffering suboptimal development conditions. It hinted that the assessment made by parasitoid females when facing hosts might be mostly based on fixed aphid species-related traits rather than characteristics potentially varying as a function of the aphid feeding status. We observed that there was no drastic change in A.

ervi behavioral pattern when tested on aphids reared on LW plants; it hints that changes in A. ervi behaviors were minor, but the trend was strong enough to affect the overall female capacity of optimizing diet breath as done under the optimal water supply.

Bottom-up effects on aphids

All aphids expressed in some extent tolerance to bottom-up impacts of water stress on plants, illustrated by their population stably maintained during several weeks in the laboratory on both treatments. However, their life history-traits were impacted at different levels. Among six aphid species, the performance of A. nerii and A. pisum were scarcely affected (it not) by water stress on plant hosts. Their ability to, well perform despite bottom-up effect may stem from two different mechanisms. A. nerii is a specialist of milkweed plants and Oleander trees. The host fidelity of A. nerii is likely linked to an optimized fitness on a given plant when compared to other host aphids that are for most of them quite polyphagous [START_REF] Harrison | Evidence for an Invasive Aphid "Superclone": Extremely Low Genetic Diversity in Oleander Aphid (Aphis nerii) Populations in the Southern United States[END_REF][START_REF] Smith | Coexistence of three specialist aphids on common milkweed, Asclepias syriaca[END_REF]. The performance of A. pisum on water stress bean plants may result from the sound nutritional quality of their plant hosts under the suboptimal watering conditions. Among the five plants tested, only beans showed both LMA and photosynthesis not impacted by water stress. Such tolerance in beans results from the mutualist protection of plant symbionts, i.e.

rhizobacteria and/or mycorrhizal fungi [START_REF] Eldin | Enhancement of Nitrogen-Fixation in Lentil, Faba Bean, and Soybean by Dual Inoculation with Rhizobia and Mycorrhizae[END_REF][START_REF] Nanjareddy | Nitrate regulates rhizobial and mycorrhizal symbiosis in common bean ( Phaseolus vulgaris L.)[END_REF]. By contrast, the survival rate of S. avenae, R. padi on wheat and M. euphorbiae on potato was reduced under water stress. Both LW wheat and potato morphologically reduced aphid feeding, as wheat LMA significantly increased as well as the density of potato trichomes which entangled aphids (observed from our experiments).

The reduced performance of aphids on wheat, cabbage, and potato was highlighted by their increased generation time and decreased the intrinsic rate of development. We supposed the inadequate nutrients of plant hosts lengthened the aphid feeding time and reduced their fecundity as previously shown by other studies (Han et al. 2014;[START_REF] Price | The Plant Vigor Hypothesis and Herbivore Attack[END_REF][START_REF] White | The Abundance of Invertebrate Herbivores in Relation to the Availability of Nitrogen in Stressed Food Plants[END_REF]2009).

Impact of water limitation on plants

The assays used were successful in efficiently impacting key plant traits through water stress. Wheat under stress had higher LMA than OW plants. Leaf mass per area value (LMA, g.m -2 ) is structural plant trait reflecting leaf thickness and/or leaf density. LMA relates to the plant metabolism (photosynthesis, respiratory rate), and plant vascular hydraulic transport system, as well as plant growth and decomposition (de la Riva et al. 2016). LMA is considered the trade-off between plant defenses, e.g. from herbivores, by the leaf rigidity and the light prevention from photosynthesis and/or the plant resource allocation. Lower LMA enhances conductivity within the leaf, which may facilitate photosynthesis (Poorter et al. 2009). Impacted by water stress, folio cell walls are thicker. Therefore, LMA is a crucial trait to predict plant adaptation strategies and/or mortality pattern under unstable environments (Anderegg et al. 2016;Poorter et al. 2009). The change in leaf chemical composition mediated by LMA might reflect the difference in the vascular system. LMA in herbaceous plant correlates positively to leaf carbon concentration but negatively to leaf nitrogen concentration, organic acids and protein concentration (de la Riva et al. 2016;Poorter et al. 2009). As phloem-and xylem-feeders, insects rely on phloem available nutrients (free amino acids, sugars). Plant higher LMA associated with lower N content could decline aphid feeding efficiency and its quality as parasitoid host (Auclair 1963;Will et al. 2013).

The plant water transport system is a vital function in plant life. In a simplified cycle, plants draw water from soil via root system, water then lost during plant transpiration in exchange for CO2 uptake (Sack and Scoffoni 2012). Plant mortality paradigms state that plants die from either carbon starvation (carbon starvation hypothesis) or hydraulic failure (hydraulic hypothesis) (Barigah et al. 2013;McDowell 2011;McDowell et al. 2008;Sevanto et al. 2014).

Parallelly, plants might shift their regulation between strategies of reduction of respiration and/or carbon use efficiency to survive under water stress (Metcalfe et al. 2010). Those accommodative behaviors in plants are classified into a spectrum of isohydric (remain leaf water potentials and reduce CO2 uptake via the stomatal closure) and anisohydric categories (decline leaf water potential in optimizing CO2 uptake) (Landsberg et al. 2017;Martinez-Vilalta et al. 2014). The stomatal closure as stress tolerance strategy consisted of results described by [START_REF] Flexas | Leaf mesophyll conductance and leaf hydraulic conductance: an introduction to their measurement and coordination[END_REF][START_REF] Westoby | Understanding ecological variation across species: area-based vs mass-based expression of leaf traits[END_REF], the strategy might benefit over leaf lifetimes. The trade-off reduction of respiration results in the decrease in photosynthesis and the deplete of carbon hydrate resources, which makes the plants more susceptible to herbivores (Landsberg et al. 2017).

Change in plant primary metabolism and its impacts on aphid feeding.

During plant stress adaptation process, the plant quality as food resources for phloem suckers has been shown to be impacted. Physically, water scarcity results in phloem water shortage, or phloem viscosity increase and challenge aphid feeding (Landsberg et al. 2017).

Chemically, plant nitrogen and phosphorus content reduce [START_REF] He | Drought effect on plant nitrogen and phosphorus: a metaanalysis[END_REF] well on aphid foraging strategies, flush or senescence feeders [START_REF] White | Plant vigour versus plant stress: a false dichotomy[END_REF], White 2015). As there was no evidence of A. pisum and S. avenae belonging to senescence group (White 2015), we assumed they belong to flush feeders group preferring young and soft leaves as the majority of insects [START_REF] Price | The Plant Vigor Hypothesis and Herbivore Attack[END_REF]. Under moderate constant water limitation, A. pisum performance at the population level was reduced but not at the early stage of plants (Mcvean 2001). However, no impact of water limitation is reported in S. avenae both at individual and population levels on wheat (Pons and Tatchell 1995). Therefore, the effects of abiotic stress on aphids are complex and simple measurements of aphid life history traits could not provide high predictive results regarding adaptive trend.

We demonstrated that the abiotic stress on plants could cascade to both second and third trophic levels, even though plants and herbivores may be tolerant of long-term water stress.

In overall, water stress mediated by plant hosts had an indirect adverse effect on parasitoid survival and development on aphid hosts, but the impact magnitude depended on the aphid-plant complex. The interaction of plant tolerance strategies and aphid salivary protein Symbiontdependent [START_REF] Donald | Protection of Pea Aphids Associated with Coinfecting Bacterial Symbionts Persists During Superparasitism by a Braconid Wasp[END_REF][START_REF] Ferrari | Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance[END_REF]Lukasik et al. 2015;[START_REF] Nyabuga | Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study[END_REF][START_REF] Sanders | Defensive insect symbiont leads to cascading extinctions and community collapse[END_REF][START_REF] Smith | Patterns, causes and consequences of defensive microbiome dynamics across multiple scales[END_REF][START_REF] Vorburger | Symbiont-conferred resistance to parasitoids in aphids -Challenges for biological control[END_REF][START_REF] Zepeda-Paulo | Host genotype-endosymbiont associations and their relationship with aphid parasitism at the field level[END_REF]Bilodeau et al. 2013;[START_REF] Cloutier | Impact of a parasitoid on the bacterial symbiosis of its aphid host[END_REF][START_REF] Heyworth | A facultative endosymbiont in aphids can provide diverse ecological benefits[END_REF][START_REF] Lukasik | The diversity and fitness effects of infection with facultative endosymbionts in the grain aphid, Sitobion avenae[END_REF][START_REF] Mclean | An Experimental Test of whether the Defensive Phenotype of an Aphid Facultative Symbiont Can Respond to Selection within a Host Lineage[END_REF]2015;[START_REF] Nyabuga | Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study[END_REF][START_REF] Oliver | Population dynamics of defensive symbionts in aphids[END_REF]Oliver et al. 2009;[START_REF] Oliver | Variation in resistance to parasitism in aphids is due to symbionts not host genotype[END_REF]2006;[START_REF] Oliver | Parasitic wasp responses to symbiont-based defense in aphids[END_REF]Oliver et al. 2003;Behaviors Gillespie and Acheampong 2012;[START_REF] Sloggett | Parasitoids induce production of the dispersal morph of the pea aphid, Acyrthosiphon pisum[END_REF][START_REF] Godfray | More than kin and less than kind: The evolution of family conflict[END_REF]Multi-modal Gerardo et al. 2010;[START_REF] Lagos | Behavioural thermoregulation in Acyrthosiphon pisum (Homoptera : Aphididae): the effect of parasitism by Aphidius ervi (Hymenoptera : Braconidae)[END_REF][START_REF] Martinez | Specificity of Multi-Modal Aphid Defenses against Two Rival Parasitoids[END_REF][START_REF] Martinez | Multi-modal defenses in aphids offer redundant protection and increased costs likely impeding a protective mutualism[END_REF]; Impacts of environmental stress [START_REF] Guay | Impact of environmental stress on aphid clonal resistance to parasitoids: Role of Hamiltonella defensa bacterial symbiosis in association with a new facultative symbiont of the pea aphid[END_REF] Aphid resistance genome/proteome Hansen et al. 2012;[START_REF] Nguyen | Proteomes of the aphid Macrosiphum euphorbiae in its resistance and susceptibility responses to differently compatible parasitoids[END_REF];

FIGURES AND TABLES 801

Parasitoid offense /counterdefenses

Host manipulation by venom injection [START_REF] Colinet | Identification of the main venom protein components of Aphidius ervi, a parasitoid wasp of the aphid model Acyrthosiphon pisum[END_REF][START_REF] Le Ralec | Host range limitation caused by incomplete host regulation in an aphid parasitoid[END_REF][START_REF] Digilio | Host castration by Aphidius ervi venom proteins[END_REF][START_REF] Digilio | Host regulation effects of ovary fluid and venom of Aphidius ervi (Hymenoptera : Braconidae)[END_REF][START_REF] Falabella | A novel fatty acid binding protein produced by teratocytes of the aphid parasitoid Aphidius ervi[END_REF][START_REF] Falabella | A gamma-glutamyl transpeptidase of Aphidius ervi venom induces apoptosis in the ovaries of host aphids[END_REF][START_REF] Falabella | Aphidius ervi teratocytes release an extracellular enolase[END_REF][START_REF] Falabella | Host regulation by the aphid parasitoid Aphidius ervi: the role of teratocytes[END_REF][START_REF] Thi | Early presence of an enolase in the oviposition injecta of the aphid parasitoid Aphidius ervi analyzed with chitosan beads as artificial hosts[END_REF]; Host regulation: aphid phenotype and behavior Christiansen-Weniger and Hardie 2000; [START_REF] Demmon | Aphidius ervi (Hymenoptera : Braconidae) increases its adult size by disrupting host wing development[END_REF][START_REF] Guerra | Differences in behavioral responses of Sitobion avenae (Hemiptera : Aphididae) to volatile compounds, following parasitism by Aphidius ervi (Hymenoptera : Braconidae)[END_REF][START_REF] Chow | Altered dispersal behaviour in parasitised aphids: parasitoid-mediated or pathology?[END_REF][START_REF] Khudr | Parasitoid wasps influence where aphids die via an interspecific indirect genetic effect[END_REF]Martinez et al. 2014b;Pennacchio et al. 1995;[START_REF] Rahbe | Physiological interactions in the pea aphid bacteriocyte symbiosis under parasitism by the Braconid Aphidius ervi[END_REF][START_REF] Rahbe | Metabolic and symbiotic interactions in amino acid pools of the pea aphid, Acyrthosiphon pisum, parasitized by the braconid Aphidius ervi[END_REF][START_REF] Villagra | Antipredator responses of aphids to parasitoids change as a function of aphid physiological state[END_REF][START_REF] Walton | Flying with a 'death sentence' on board: electrophoretic detection of braconid parasitoid larvae in migrating winged grain aphids, Sitobion avenae (F.)[END_REF]Adaptation Hufbauer 2001;[START_REF] Dion | Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts[END_REF][START_REF] Le Ralec | Evolutionary ecology of the interactions between aphids and their parasitoids[END_REF][START_REF] Henry | Covariance of phenotypically plastic traits induces an adaptive shift in host selection behaviour[END_REF]; Parasitoid behavioral and physiological traits

Host location and recognition

Volatile cues : [START_REF] Battaglia | Cornicle Secretion of Acyrthosiphon-Pisum (Homoptera, Aphididae) as a Contact Kairomone for the Parasitoid Aphidius-Ervi (Hymenoptera, Braconidae)[END_REF][START_REF] Battaglia | The Role of Physical Cues in the Regulation of Host Recognition and Acceptance Behavior of Aphidius-Ervi Haliday (Hymenoptera, Braconidae)[END_REF]Dewhirst et al. 2008;[START_REF] Du | Relative importance of semiochemicals from first and second trophic levels in host foraging behavior of Aphidius ervi[END_REF][START_REF] Du | Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi[END_REF][START_REF] Guerrieri | Flight Behavior of the Aphid Parasitoid Aphidius-Ervi (Hymenoptera, Braconidae) in Response to Plant and Host Volatiles[END_REF][START_REF] Mayhew | Adaptive patterns of host-plant selection by phytophagous insects[END_REF][START_REF] Heuskin | Optimisation of a semiochemical slow-release alginate formulation attractive towards Aphidius ervi Haliday parasitoids[END_REF][START_REF] Pareja | Multivariate statistics coupled to generalized linear models reveal complex use of chemical cues by a parasitoid[END_REF][START_REF] Poppy | Aphid parasitoid responses to semiochemicals -Genetic, conditioned or learnt?[END_REF][START_REF] Powell | Strategies involved in the location of hosts by the parasitoid Aphidius ervi Haliday (Hymenoptera : Braconidae : Aphidiinae)[END_REF][START_REF] Stilmant | Attractiveness and Acceptability of Sitobion-Avenae (Aphididae, Homoptera) for Aphidius-Rhopalosiphi and a-Ervi (Aphidiidae, Hymenoptera)[END_REF][START_REF] Wickremasinghe | Reactions of Adult Female Parasitoids, Particularly Aphidius-Rhopalosiphi, to Volatile Chemical Cues from the Host Plants of Their Aphid Prey[END_REF]Bruce, T.J. et al. 2002;Bruce, T.J.A. et al. 2008;Glinwood et al. 1999a;Glinwood et al. 1999b;[START_REF] Weinbrenner | Oviposition behaviour of the aphid parasitoid, Aphidius ervi: Are wet aphids recognized as host?[END_REF]; Visual cues: [START_REF] Michaud | The Use of Visual Cues in Host Evaluation by Aphidiid Wasps .1. Comparison between 3 Aphidius Parasitoids of the Pea Aphid[END_REF]Powell et al. 1998 Physical cues : [START_REF] Battaglia | The Role of Physical Cues in the Regulation of Host Recognition and Acceptance Behavior of Aphidius-Ervi Haliday (Hymenoptera, Braconidae)[END_REF]Battaglia, Donatella et al. 2000;Nakashima and Akashi 2005 Host acceptance [START_REF] Michaud | The Use of Visual Cues in Host Evaluation by Aphidiid Wasps .1. Comparison between 3 Aphidius Parasitoids of the Pea Aphid[END_REF][START_REF] Poppy | Aphid parasitoid responses to semiochemicals -Genetic, conditioned or learnt?[END_REF][START_REF] Guerrieri | Effect of adult experience on in-flight orientation to plant and plant-host complex volatiles in Aphidius ervi Haliday (Hymenoptera, Braconidae)[END_REF][START_REF] Henry | Size-mediated adaptive foraging: a hostselection strategy for insect parasitoids[END_REF][START_REF] Langley | Learning by the parasitoid wasp, Aphidius ervi (Hymenoptera : Braconidae), alters individual fixed preferences for pea aphid color morphs[END_REF][START_REF] Schworer | Foraging behavior of Aphidius ervi (Haliday) (Hymenoptera : Braconidae : Aphidiinae) at different spatial scales: Resource utilization and suboptimal weather conditions[END_REF][START_REF] Larocca | Functional bases of host-acceptance behaviour in the aphid parasitoid Aphidius ervi[END_REF][START_REF] Pennacchio | Host Recognition and Acceptance Behavior in 2 Aphid Parasitoid Species -Aphidius-Ervi and Aphidius-Microlophii (Hymenoptera, Braconidae)[END_REF] Reproductive strategy [START_REF] Bueno | Parasitism by Aphidius-Ervi (Hym, Aphidiidae) -Preference for Pea Aphid and Blue Alfalfa Aphid (Hom, Aphididae) and Competition with a-Smithi[END_REF][START_REF] He | Emergence, sexual maturation and oviposition of Aphidius ervi (Hymenoptera : Aphidiidae)[END_REF][START_REF] Schworer | Foraging behavior of Aphidius ervi (Haliday) (Hymenoptera : Braconidae : Aphidiinae) at different spatial scales: Resource utilization and suboptimal weather conditions[END_REF]Henry et al. 2005;[START_REF] Olson | Spatially aggregated parasitism on pea aphids, Acyrthosiphon pisum, caused by random foraging behavior of the parasitoid Aphidius ervi[END_REF]; Learning: innate i.e. Premature or acquired [START_REF] Chow | The Influence of Prior Ovipositional Experience on Host Selection in 4 Species of Aphidiid Wasps (Hymenoptera, Aphidiidae)[END_REF][START_REF] Du | Chemically mediated associative learning in the host foraging behavior of the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae)[END_REF][START_REF] Guerrieri | Effect of adult experience on in-flight orientation to plant and plant-host complex volatiles in Aphidius ervi Haliday (Hymenoptera, Braconidae)[END_REF][START_REF] Gutierrez-Ibanez | Pre-pupation behaviour of the aphid parasitoid Aphidius ervi (Haliday) and its consequences for pre-imaginal learning[END_REF][START_REF] Langley | Learning by the parasitoid wasp, Aphidius ervi (Hymenoptera : Braconidae), alters individual fixed preferences for pea aphid color morphs[END_REF][START_REF] Takemoto | Learning is involved in the response of parasitic wasps Aphidius ervi (Haliday) (Hymenoptera: Braconidae) to volatiles from a broad bean plant, Vicia faba (Fabaceae), infested by aphids Acyrthosiphon pisum (Harris) (Homoptera: Aphididae)[END_REF]2012;[START_REF] Lanteigne | Patch Experience Changes Host Acceptance of the Aphid Parasitoid Aphidius ervi[END_REF][START_REF] Villagra | The effect of larval and early adult experience on behavioural plasticity of the aphid parasitoid Aphidius ervi (Hymenoptera, Braconidae, Aphidiinae)[END_REF]Mating Battaglia et al. 2002;[START_REF] He | Reproductive strategies of Aphidius ervi Haliday (Hymenoptera : Aphidiidae)[END_REF]McClure and McNeil 2009;[START_REF] Mcclure | Courtship behavior in relation to the female sex pheromone in the parasitoid, Aphidius ervi (Hymenoptera : Braconidae)[END_REF][START_REF] Villagra | Associative odour learning affects mating behaviour in Aphidius ervi males (Hymenoptera : Braconidae)[END_REF]2008;[START_REF] Nyabuga | Mating Strategies in Solitary Aphid Parasitoids: Effect of Patch Residence Time and Ant Attendance[END_REF][START_REF] Villagra | Male wing fanning by the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae) produces a courtship song[END_REF][START_REF] Villagra | Olfactory conditioning in mate searching by the parasitold Aphidius ervi (Hymenoptera : Braconidae)[END_REF]; Sex ratio Mackauer and Lardner 1995; Oviposition behavior: multi and super parasitism [START_REF] Bai | Conspecific Superparasitism in 2 Parasitoid Wasps, Aphidius-Ervi Haliday and Aphelinus-Asychis Walker -Reproductive Strategies Influence Host Discrimination[END_REF][START_REF] Bai | Recognition of Heterospecific Parasitism -Competition between Aphidiid (Aphidius-Ervi) and Aphelinid (Aphelinus-Asychis) Parasitoids of Aphids (Hymenoptera, Aphidiidae, Aphelinidae)[END_REF]1992;[START_REF] Chua | Searching Efficiency and Multiparasitism in Aphidius-Smithi and Aphidius-Ervi (Hym, Aphidiidae), Parasites of Pea Aphid, Acyrthosiphon-Pisum (Hom, Aphididae)[END_REF][START_REF] Donald | Protection of Pea Aphids Associated with Coinfecting Bacterial Symbionts Persists During Superparasitism by a Braconid Wasp[END_REF][START_REF] Mcbrien | Heterospecific Larval Competition and Host Discrimination in 2 Species of Aphid Parasitoids -Aphidius-Ervi and Aphidius-Smithi[END_REF]1991;[START_REF] Micha | Time-Related Rejection of Parasitized Hosts in the Aphid Parasitoid, Aphidius-Ervi[END_REF]Sidney et al. 2010a;[START_REF] Bai | Conspecific Superparasitism in 2 Parasitoid Wasps, Aphidius-Ervi Haliday and Aphelinus-Asychis Walker -Reproductive Strategies Influence Host Discrimination[END_REF][START_REF] Bai | Recognition of Heterospecific Parasitism -Competition between Aphidiid (Aphidius-Ervi) and Aphelinid (Aphelinus-Asychis) Parasitoids of Aphids (Hymenoptera, Aphidiidae, Aphelinidae)[END_REF]1992;[START_REF] Mcbrien | Decision to Superparasitize Based on Larval Survival -Competition between Aphid Parasitoids Aphidius-Ervi and Aphidius-Smithi[END_REF][START_REF] Micha | Time-Related Rejection of Parasitized Hosts in the Aphid Parasitoid, Aphidius-Ervi[END_REF]; Adult parasitoid physiological traits Christiansen-Weniger and Hardie 1997; [START_REF] He | Asymmetric size effect of sexes on reproductive fitness in an aphid parasitoid Aphidius ervi (Hymenoptera : Aphidiidae)[END_REF][START_REF] He | Emergence, sexual maturation and oviposition of Aphidius ervi (Hymenoptera : Aphidiidae)[END_REF][START_REF] Grbic | Shifts in the life history of parasitic wasps correlate with pronounced alterations in early development[END_REF][START_REF] Malina | Developmental rates of the aphid Aphis pomi (Aphidoidea: Aphididae) and its parasitoid Aphidius ervi (Hymenoptera: Aphidiidae)[END_REF]; Immature parasitoid traits [START_REF] He | Host Age Preference Behavior in Aphidius ervi Haliday (Hymenoptera: Aphidiidae)[END_REF][START_REF] Henry | Size-mediated adaptive foraging: a hostselection strategy for insect parasitoids[END_REF][START_REF] Poppy | Aphid parasitoid responses to semiochemicals -Genetic, conditioned or learnt?[END_REF]Sequeira and Mackauer 1992a Impacts of hosts Host developmental stages: age, body size [START_REF] Clarke | Susceptibility of Macrosiphum euphorbiae to the parasitoid Aphidius ervi: larval development depends on host aphid genotype[END_REF][START_REF] Colinet | Host age and fitness-related traits in a koinobiont aphid parasitoid[END_REF]Sequeira and Mackauer 1992b;1994;Sidney et al. 2010b;[START_REF] He | Host Age Preference Behavior in Aphidius ervi Haliday (Hymenoptera: Aphidiidae)[END_REF][START_REF] Mackauer | Sexual size dimorphism in solitary parasitoid wasps: Influence of host quality[END_REF][START_REF] Trotta | Plastic responses of some life history traits and cellular components of body size in Aphidius ervi as related to the age of its host Acyrthosiphon pisum[END_REF] Host genotypes intra and interspecific variation Gagic, Vesna et al. 2016;[START_REF] Ferrari | Clonal variation and covariation in aphid resistance to parasitoids and a pathogen[END_REF][START_REF] Li | Pea aphid clonal resistance to the endophagous parasitoid Aphidius ervi[END_REF]Martinez et al. 2014a;[START_REF] Michaud | The oviposition behavior of Aphidius ervi and Monoctonus paulensis (Hymenoptera: Aphididae) encountering different host species (Homoptera: Aphididae) in sequential patches[END_REF] [START_REF] Bennett | Plant and insect microbial symbionts alter the outcome of plant-herbivore-parasitoid interactions: implications for invaded, agricultural and natural systems[END_REF][START_REF] Calvo | The performance of an aphid parasitoid is negatively affected by the presence of a circulative plant virus[END_REF][START_REF] Harri | Extended larval development time for aphid parasitoids in the presence of plant endosymbionts[END_REF][START_REF] Battaglia | Tomato Below Ground-Above Ground Interactions: Trichoderma longibrachiatum Affects the Performance of Macrosiphum euphorbiae and Its Natural Antagonists[END_REF]Plant pathogens Calvo and Fereres 2011;[START_REF] Christiansen-Weniger | Plant virus and parasitoid interactions in a shared insect vector/host[END_REF]Hodge et al. 2011a;[START_REF] Hodge | Complex interactions between a plant pathogen and insect parasitoid via the shared vector-host: consequences for host plant infection[END_REF] Parasitoid natural enemies: predators [START_REF] Meisner | Intraguild predation on the parasitoid Aphidius ervi by the generalist predator Harmonia axyridis: the threat and its avoidance[END_REF][START_REF] Nakashima | The role of semiochemicals in the avoidance of the seven-spot ladybird, Coccinella septempunctata, by the aphid parasitoid, Aphidius ervi[END_REF][START_REF] Nakashima | Chemically mediated intraguild predator avoidance by aphid parasitoids: Interspecific variability in sensitivity to semiochemical trails of ladybird predators[END_REF];

Population dynamic

Bottom-up regulation Desneux and Ramirez-Romero 2009;Petermann et al. 2010a;[START_REF] Powell | The Influence of Host Food Plants on Host Recognition by 4 Aphidiine Parasitoids (Hymenoptera, Braconidae)[END_REF][START_REF] Schadler | Host plant genotype determines bottomup effects in an aphid-parasitoid-predator system[END_REF]Top-down regulation Feng et al. 1991;[START_REF] Nakashima | Field evaluation of synthetic aphid sex pheromone in enhancing suppression of aphid abundance by their natural enemies[END_REF][START_REF] Sanders | Defensive insect symbiont leads to cascading extinctions and community collapse[END_REF]Hufbauer 2002;[START_REF] Ingerslew | Mechanisms Underlying the Nonconsumptive Effects of Parasitoid Wasps on Aphids[END_REF]Kavallieratos et al. 2004;[START_REF] Mitchell | Combining plant resistance and a natural enemy to control Amphorophora idaei[END_REF][START_REF] Northfield | A simple plant mutation abets a predator-diversity cascade[END_REF]Field observation Bosque-Perez et al. 2002;[START_REF] Gruber | Hymenopterous Parasites and Hyperparasites of Schizaphis-Graminum (Rondani) (Hom, Aphididae) on Sorghum, in the Drome, France[END_REF][START_REF] Senoo | Seasonal abundance of primary parasitoids and hyperparasitoids associated with Acyrthosiphon pisum (Harris) and Acyrthosiphon kondoi Shinji (Homoptera : Aphididae) on alfalfa[END_REF][START_REF] Zuparko | Survey of the Parasitoids of the Tuliptree Aphid, Illinoia-Liriodendri (Hom, Aphididae), in Northern California[END_REF][START_REF] Al Dobai | Parasitoids and hyperparasitoids of cereal aphids (Homoptera, Aphididae) on winter wheat in Slovakia[END_REF][START_REF] Baudino | Pest and natural enemies report in the lettuce crop. La Pampa province (Argentina)[END_REF]Desneux et al. 2006b;Feng, M.C. et al. 1993;Feng, M.G. et al. 1991;1992;[START_REF] Tomanovic | Regional Tritrophic Relationship Patterns of Five Aphid Parasitoid Species (Hymenoptera: Braconidae: Aphidiinae) in Agroecosystem-Dominated Landscapes of Southeastern Europe[END_REF][START_REF] Gruber | Hymenopterous Parasites and Hyperparasites of Schizaphis-Graminum (Rondani) (Hom, Aphididae) on Sorghum, in the Drome, France[END_REF][START_REF] Havelka | Review and Key to the World Parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Aphis ruborum (Hemiptera: Aphididae) and Its Role as a Host Reservoir[END_REF]Kos et al. 2012;[START_REF] Lumbierres | Seasonal parasitism of cereal aphids in a Mediterranean arable crop system[END_REF][START_REF] Nebreda | Seasonal abundance of aphid species on lettuce crops in Central Spain and identification of their main parasitoids[END_REF][START_REF] Pons | Parasitoid complex of alfalfa aphids in an IPM intensive crop system in northern Catalonia[END_REF][START_REF] Pons | Spring aphid-parasitoid (Hom., Aphididae, Hym., Braconidae) associations and interactions in a Mediterranean arable crop ecosystem, including Bt maize[END_REF][START_REF] Rakhshani | Distribution and diversity of wheat aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) in Iran[END_REF][START_REF] Stary | Macrosiphum-Albifrons Essig, an Invasive Lupin Aphid and Its Natural-Enemy Complex in Czechoslovakia (Homoptera, Aphididae)[END_REF][START_REF] Tomanovic | Cereal aphids (Hemiptera : Aphidoidea) in Serbia: Seasonal dynamics and natural enemies[END_REF][START_REF] Wickremasinghe | Reactions of Adult Female Parasitoids, Particularly Aphidius-Rhopalosiphi, to Volatile Chemical Cues from the Host Plants of Their Aphid Prey[END_REF];

Molecular and biochemical mechanisms

Host-dependent transcriptome [START_REF] Ballesteros | Expression differences in Aphidius ervi (Hymenoptera: Braconidae) females reared on different aphid host species[END_REF][START_REF] Clarke | Susceptibility of Macrosiphum euphorbiae to the parasitoid Aphidius ervi: larval development depends on host aphid genotype[END_REF] Parasitoid genome [START_REF] Gilchrist | A quantitative genetic analysis of thermal sensitivity in the locomotor performance curve of Aphidius ervi[END_REF]Sequeira and Mackauer 1992c;[START_REF] Varricchio | Characterization of Aphidius-Ervi (Hymenoptera, Braconidae) Ribosomal Genes and Identification of Site-Specific Insertion Elements Belonging to the Non-Ltr Retrotransposon Family[END_REF]Molecular identification Trybush et al. 2006;[START_REF] Derocles | Identification of molecular markers for DNA barcoding in the Aphidiinae (Hym. Braconidae)[END_REF][START_REF] Gadallah | Identification key, diversity and host associations of parasitoids (Hymenoptera: Braconidae: Aphidiinae) of aphids attacking cereal crops in Egypt[END_REF]; Nutrient absorption of larvae / metabolism [START_REF] Fiandra | Leucine transport by the larval midgut of the parasitoid Aphidius ervi (Hymenoptera)[END_REF][START_REF] Caccia | Unexpected similarity of intestinal sugar absorption by SGLT1 and apical GLUT2 in an insect (Aphidius ervi, Hymenoptera) and mammals[END_REF][START_REF] Caccia | Functional analysis of a fatty acid binding protein produced by Aphidius ervi teratocytes[END_REF][START_REF] Caccia | Nutrient absorption by Aphidius ervi larvae[END_REF][START_REF] De Eguileor | Larval anatomy and structure of absorbing epithelia in the aphid parasitoid Aphidius ervi Haliday (Hymenoptera, Braconidae)[END_REF][START_REF] Giordana | Absorption of sugars and amino acids by the epidermis of Aphidius ervi larvae[END_REF][START_REF] Grossi | Extracellular matrix degradation via enolase/plasminogen interaction: Evidence for a mechanism conserved in Metazoa[END_REF][START_REF] Sabri | Placenta-Like Structure of the Aphid Endoparasitic Wasp Aphidius ervi: A Strategy of Optimal Resources Acquisition[END_REF][START_REF] De Eguileor | Larval anatomy and structure of absorbing epithelia in the aphid parasitoid Aphidius ervi Haliday (Hymenoptera, Braconidae)[END_REF]

Intra-specific variation

Physiological traits Takada and Tada 2000 by geography Morphological traits Nemec and Stary 1983a;b;[START_REF] Stary | Color Patterns of Adults as Evidence on Aphidius-Ervi Biotypes in Field Environments (Hymenoptera, Aphidiidae)[END_REF]Villegas et al. 2017; by geographical variation; by host species Genetic diversity/gene flow [START_REF] Emelianov | Fusion-fission experiments in Aphidius: evolutionary split without isolation in response to environmental bimodality[END_REF][START_REF] Henry | Assortative mating and the role of phenotypic plasticity in male competition: implications for gene flow among host-associated parasitoid populations[END_REF][START_REF] Henry | Hostadapted parasitoids in biological control: Does source matter?[END_REF][START_REF] Henter | The Potential for Coevolution in a Host-Parasitoid System .2. Genetic-Variation within a Population of Wasps in the Ability to Parasitize an Aphid Host[END_REF][START_REF] Henter | The Potential for Coevolution in a Host-Parasitoid System .1. Genetic-Variation within an Aphid Population in Susceptibility to a Parasitic Wasp[END_REF][START_REF] Nemec | Genetic Diversity of the Parasitoid Aphidius-Ervi on the Pea Aphid, Acyrthosiphon-Pisum in Czechoslovakia (Hymenoptera, Aphidiidae -Homoptera, Aphididae)[END_REF]Sequeira and Mackauer 1992c;[START_REF] Zepeda-Paulo | Does sex-biased dispersal account for the lack of geographic and hostassociated differentiation in introduced populations of an aphid parasitoid?[END_REF][START_REF] Daza-Bustamante | Attraction toward alfalfa and wheat aphid-host plant complexes explains the absence of genetic population structure of the parasitoid Aphidius ervi (Hymenoptera : Braconidae) in Chile[END_REF][START_REF] Ferrari | The maintenance of intraspecific biodiversity: the interplay of selection on resource use and on natural enemy resistance in the pea aphid[END_REF][START_REF] Hufbauer | The population genetics of a biological control introduction: mitochondrial DNA and microsatellie variation in native and introduced populations ofAphidus ervi, a parisitoid wasp[END_REF][START_REF] Hufbauer | Isolation and characterization of microsatellites in Aphidius ervi (Hymenoptera : Braconidae) and their applicability to related species[END_REF]Behavioral traits Daza-Bustamante et al. 2002;[START_REF] Ives | Variability and parasitoid foraging efficiency: A case study of pea aphids and Aphidius ervi[END_REF]; Biological control Cold storage Colinet and Hance 2010;[START_REF] Ismail | Fitness consequences of low temperature storage of Aphidius ervi[END_REF][START_REF] Ismail | What are the possible benefits of small size for energy-constrained ectotherms in cold stress conditions?[END_REF][START_REF] Ismail | Physiological costs of cold exposure on the parasitoid Aphidius ervi, without selection pressure and under constant or fluctuating temperatures[END_REF]Frère et al. 2011;Introduction Gavkare et al. 2014;Hufbauer 2002;[START_REF] Milne | The Release and Establishment of Aphidius-Ervi Haliday (Hymenoptera, Ichneumonoidea) in Lucerne Aphids in Eastern Australia[END_REF][START_REF] Stary | The Fate of Released Parasitoids (Hymenoptera, Braconidae, Aphidiinae) for Biological-Control of Aphids in Chile[END_REF][START_REF] Brewer | Hymenopteran parasitoids and dipteran predators of the invasive aphid Diuraphis noxia after enemy introductions: Temporal variation and implication for future aphid invasions[END_REF][START_REF] Cameron | A retrospective evaluation of the host range of four Aphidius species introduced to New Zealand for the biological control of pest aphids[END_REF][START_REF] Milne | Evaluation of the establishment of Aphidius ervi Haliday (Hymenoptera : Braconidae) in lucerne aphid populations in New South Wales[END_REF][START_REF] Sterk | IPM on strawberries in glasshouses and plastic tunnels in Belgium, new possibilities[END_REF]Genetic management Hopper et al. 1993;[START_REF] Zepeda-Paulo | Signatures of genetic bottleneck and differentiation after the introduction of an exotic parasitoid for classical biological control[END_REF] Mix assemblage [START_REF] Enkegaard | Shallot aphids, Myzus ascalonicus, in strawberry: Biocontrol potential of three predators and three parasitoids[END_REF][START_REF] Rocca | Combining lacewings and parasitoids for biological control of foxglove aphids in sweet pepper[END_REF][START_REF] Snyder | Generalist predators disrupt biological control by a specialist parasitoid[END_REF][START_REF] Cardinale | Biodiversity and biocontrol: emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem[END_REF]; Side-effect of insecticides [START_REF] Araya | Effects of Some Insecticides Applied in Sublethal Concentrations on the Survival and Longevity of Aphidius ervi (Haliday) (Hymenoptera : Aphidiidae) Adults[END_REF][START_REF] Hogervorst | Snowdrop lectin (Galanthus nivalis agglutinin) in aphid honeydew negatively affects survival of a honeydew-consuming parasitoid[END_REF][START_REF] Kramarz | Population level effects of cadmium and the insecticide imidacloprid to the parasitoid, Aphidius ervi after exposure through its host, the pea aphid, Acyrthosiphon pisum (Harris)[END_REF][START_REF] Azzouz | Potential effects of plant protease inhibitors, oryzacystatin I and soybean Bowman-Birk inhibitor, on the aphid parasitoid Aphidius ervi Haliday (Hymenoptera, Braconidae)[END_REF][START_REF] De Zutter | Effect of the mycotoxin deoxynivalenol on grain aphid Sitobion avenae and its parasitic wasp Aphidius ervi through food chain contamination[END_REF]Desneux et al. 2006a;Desneux et al. 2004a;Desneux et al. 2004b;[START_REF] Joseph | Effects on the aphid parasitoid Aphidius ervi of an insecticide (Plenum (R), pymetrozine) specific to plant-sucking insects[END_REF][START_REF] Stark | Limitations to Use of Topical Toxicity Data for Predictions of Pesticide Side-Effects in the Field[END_REF] Side-effect of Btbased compound [START_REF] Cowgill | Multitrophic interactions involving genetically modified potatoes, nontarget aphids, natural enemies and hyperparasitoids[END_REF][START_REF] Digilio | Interactions between tomato volatile organic compounds and aphid behaviour[END_REF]

Nutritional ecology

Sugar sources [START_REF] Araj | Floral diversity, parasitoids and hyperparasitoids -A laboratory approach[END_REF][START_REF] Araj | Searching behavior of an aphid parasitoid and its hyperparasitoid with and without floral nectar[END_REF][START_REF] Azzouz | Effects of feeding frequency and sugar concentration on behavior and longevity of the adult aphid parasitoid: Aphidius ervi (Haliday) (Hymenoptera: Braconidae)[END_REF][START_REF] Lenaerts | Adult Parasitoids of Honeydew-Producing Insects Prefer Honeydew Sugars to Cover Their Energetic Needs[END_REF][START_REF] Vollhardt | Nectar vs. honeydew feeding by aphid parasitoids: does it pay to have a discriminating palate?[END_REF][START_REF] Wade | Excised or intact inflorescences? Methodological effects on parasitoid wasp longevity[END_REF][START_REF] Hayashi | Effects of Sugar Supply on Longevity and Progeny Production of an Aphid Parasitoid, Aphidius ervi (Hymenoptera: Aphidiidae)[END_REF][START_REF] Hogervorst | Effects of honeydew sugar composition on the longevity of Aphidius ervi[END_REF]; Artificial diet [START_REF] Couty | Effects of artificial diet containing GNA and GNA-expressing potatoes on the development of the aphid parasitoid Aphidius ervi Haliday (Hymenoptera : Aphidiidae)[END_REF][START_REF] Larocca | An 'artificial aphid' for Aphidius ervi (Hym., Braconidae)[END_REF]; Diet for immature parasitoid Pennacchio et al. 1999;

1

GENERAL DISCUSSION

The use of biological control agents: BCA that are natural enemies of agricultural pests requires a deep understanding of their ecological specialization. BCA preference and performance on specific hosts/preys determine their pest suppression efficacy. Their host fidelity predicts their ability to switch from one targeted host to another non-targeted species.

Their diet breadth predicts the ability to implement and maintain their presence in a new environment. These parameters depend on the BCA host specificity, which is furthermore influenced by ecological forces. Aphid parasitoids, one common BCA were the model in this study. Their larvae develop inside the aphid host of which the adults emerge. The host bodies, then, represent both food resource and environment for larva parasitoid development. The host choice of female adults is the dead-or-living matter for the larvae. On encountering a host, the female adult should decide to lay eggs or not, and the sex ratio of their offspring. It seems that parasitoid mothers know what is best for their descendants and their species as a whole. Understanding factors leading to such preference is therefore essential. The parasitoid strategies of specialization could focus on plant or aphid resources because both aphid and plant host quality could impact parasitoid performance. Some parasitoids, for instance, specialize in phylogenetically closed aphids. Others could specialize on plant species regardless of aphid phylogeny.

This study focused on the factors modulating the host specificity of aphid parasitoids within the plant-aphid-parasitoid tri-trophic system in the laboratory. These factors are both biotic and abiotic, i.e. plant-, aphid-and parasitoid traits as well as environmental stress, more especially soil water limitation. The first goal was to assess the fundamental host specificity of three parasitoids by the host range testing method on 14 aphid species. Also, their degree of host specificity was evaluated with the host specificity index and the relationship preference-performance. The discrimination between parasitoid specialists and generalists vaguely mentioned in literature has been clarified on a subtle scale in this study. The second goal was to assess the impact of water limitation on the fundamental host specificity of one parasitoid, i.e. on their preference and performance and their optimal foraging pattern.

First of all, we showed that our three parasitoids have different fundamental host specificity.

One parasitoid (A. ervi) is an intermediate specialist and mainly parasitizes aphids from the Macrosiphini tribe. The others, D. rapae, and A. abdominalis are generalists and parasitize a phylogenetically broad range of aphid hosts. Their behaviors differed: A. ervi showed a preference for hosts on which they performed well, but D. rapae and A. abdominalis did not.

The preference-performance correlation relates to a lower host range for A. ervi and a smaller host specificity index. In other words, specialist parasitoids are more selective in host choice if they specialize in a few hosts and is called the optimal foraging pattern. As the three parasitoids are often considered host generalists in literature, the host specificity index and the optimal foraging strategy are efficient ways to classify specialist/generalist species on a fine scale.

This study on host specificity confirms the general statement that A. ervi is an intermediate specialist, not sufficiently proved in previous literature, of the Macrosiphini tribe. However, among Macrosiphini, A. ervi was unable to parasitize M. dirhordum, either because it is protected by its bacterial symbiont Hamiltonella defensa or because the A. ervi strain in this study did not genetically adapt to M. dirhordum. Biotic or biogeographical factors might be able to modulate the host range. The difference between the parasitoid field host range and the fundamental host range implies the impact of environmental and geographical factors to parasitoid specialization. Future research should focus on the calculation of field host specificity index for a wide range of BCA, as in the Skoracka and Kuczyński study (2012).

Moreover, the host specificity index would provide a broader and deeper view on the potential phylogenetic signal of parasitoid species on their host specificity [START_REF] Derocles | Are generalist Aphidiinae (Hym. Braconidae) mostly cryptic species complexes?[END_REF] as the phylogenetic relationship may correlate to similar traits in host species (Guénard et al. 2013). Furthermore, we could study the characteristics of intermediate specialist/generalists, for example, whether the correlation preference-performance only exists for intermediate specialist/generalist but not for extreme specialists or generalists? Secondly, water limitation was proved to affect parasitoid efficiency, specifically A. ervi. Both their preference and performance on aphid hosts were adversely impacted, however asymmetrically. In most cases, A. ervi preference on aphid hosts was not significantly reduced except the detection rate when they encountered the aphid M. persicae. However, their performance on good or suboptimal quality hosts decreased considerably. These asymmetrical modifications in life-history traits of A. ervi led to the loss of the correlation preference-performance. Differently speaking, their host selection efficiency was impacted; parasitoids mother no longer knew which best hosts for their offspring were. For further study, we should test A. ervi behavior in choice-conditions to see if learning could improve their capacity of evaluating low-quality hosts.

This study also showed a diversity of responses to water stress at both trophic levels, plant, and aphid, resulting in different impacts on the third trophic level, parasitoid. Plants react differently to water regimes. For example, optimal water supply for cabbages was 70% field capacity while it was 100% for all the other plants. The 100% soils saturated volume cause stress symptom on cabbages similar to water limitation (consistent with [START_REF] Khan | Influence of water stress on the glucosinolate profile of Brassica oleracea var. italica and the performance of Brevicoryne brassicae and Myzus persicae[END_REF].

Interestingly, parasitoid performance was more efficient on 70% cabbages (chapter 5, article 3) compare to 100% (chapter 4, article 1), strengthening the preference-performance correlation under optimal environmental conditions. Water limitation might also influence plant physical and/or chemical defenses. In this study, aphid survival rate significantly decreased in water-stressed wheat with harden structure (increased LMA) and [START_REF] Glas | Plant Glandular Trichomes as Targets for Breeding or Engineering of Resistance to Herbivores[END_REF] shown a negative impact on aphid of the increased of trichome density in potato.

The resistance of aphid A. pisum to the bottom-up effect of water stress and A. ervi performance on such aphids are interesting. Why could not the bottom-up impact reach the top-level like in the other plant-aphid combinations? One hypothesis suggests a positive effect of the symbiosis between Rhizobium and fava beans that buffer the bottom-up effect at higher trophic levels. Also, whether the advantage of natal hosts on A. ervi could buffer impacts of plant water stress? What happens if A. ervi are reared on a different host species but not A. pisum? For further study, one could test A. ervi on natal host S. avenae and compare their performance on S. avenae and A. pisum under similar water limitation.

In parasitoids, the mortality at egg stage is caused by host immune defenses or symbionts, at larva stage by plant toxins sequestrated by aphids and at the nymphal stage by low nutritional quality (Desneux et al. 2009a). Regardless of insecticidal compounds of plant hosts or host quality, A. ervi mortality happened mostly from the nymphal stage but not earlier. A. ervi late mortality inside aphid hosts probably because they have a placenta-like structure of eggs with a thick cellular wall, which helps the egg to second instar larva to drive the nutrients efficiently [START_REF] Sabri | Placenta-Like Structure of the Aphid Endoparasitic Wasp Aphidius ervi: A Strategy of Optimal Resources Acquisition[END_REF]. This structure is unique to A. ervi until now [START_REF] Martinez | Specificity of Multi-Modal Aphid Defenses against Two Rival Parasitoids[END_REF] and probably confer resistance to A. ervi larva even when they develop on aphid hosts feeding on toxic plant hosts like A. nerii. It could be interesting to test the hypothesis on other parasitoids to see their pattern of mortality inside aphid hosts. Nitrogen-deprived compounds in aphids might have high impacts on the parasitoid larval development Diet breadth of both aphids and parasitoids seems to affect their efficiency of host exploiting, as predicted by the "trade-off host range breadth -host use efficiency" model (Straub et al. 2011). Myzus persicae, an extreme generalist aphid, was severely suffered from water stress as well as parasitoid parasitizing them. The trade-off model could be investigated further at aphids, that is to say, whether more specialist aphids could resist better under bottom-up impacts of water stress. One could equally examine other parasitoids share the same hosts with A. ervi but have different diet breadth like Aphidius rhopalosiphi, a so-called specialist on wheat aphids, or Aphelinus abdominalis, a generalist, to compare the magnitude of bottom-up impacts.

Implication in biological control and ecology

Overall, this evidence of the bottom-up effect of soil water limitation on parasitoid host specificity raises a concern for parasitoids as BCA. Both plants and aphids can tolerate a moderate, long-term water limitation, even though their performance were negatively impacted. Aphid populations could be maintained on water stress plants for several weeks without extinction in this study. However, the parasitoid mortality on aphid hosts significantly increased, such as from 60% under optimal water supply to 94.5% under water limitation on M. persicae hosts. Therefore, the top trophic level with high degree of food specialization like parasitoids might suffer more than the lower trophic levels. Further studies should be done to confirm this statement, for example investigating parasitoid population dynamic on aphid hosts feeding on water-stressed plants.

In case of confirmed negative bottom-up impacts of abiotic factors on parasitoids, should one release these BCA under abiotic constraints? That could be an economic loss. In the field application, practitioners could increase parasitoid host selection effectiveness by methods like (1) previous learning, such as exposing them to low-quality hosts before or by inducing volatile plant compounds to locate hosts; (2) application of a mix of natural enemies, e.g. specialist BCA on shared host aphids; (3) use of banker plant-aphid combination that are resistant to abiotic stress to support BCA. The responses of organisms from their morphology to metabolism and proteome profiles are very different for each kind of water stress or stress combination, e.g. the intensity, duration, and timing (Huberty and Denno 2004;[START_REF] White | Plant vigour versus plant stress: a false dichotomy[END_REF][START_REF] Price | The Plant Vigor Hypothesis and Herbivore Attack[END_REF]. It could be interesting to test all kinds of water limitation regimes or combined abiotic stress, e.g. water limitation and fertilizer supply on similar tri-trophic systems to optimize water regimes.

Prospects for risk and efficiency assessments of BCA

From this study, we highlighted the importance of parasitoid capacity of adaptation under field conditions, especially on current climate change era. This capacity is called parasitoid plasticity. We also emphasized the necessity of both efficiency and risk assessments of BCA, where parasitoid specificity could predict parasitoid plasticity. We shared the same view with Heimpel (2017) of raising acceptable risk levels of non-targeted species for BCA. Zero-risk parasitoids could fail in the field in considering the trade-off between specialist and generalist, specificity and plasticity. Firstly, the more specialist parasitoids could result in the less productive BCA on the disturbed environment. Secondly, risk assessment in laboratory conditions could result in overestimating the ecological risks of the BCA and pretermit good BCA. Thirdly, invasive species are continuously introduced into new areas following human activities; the ecological risks are nonetheless unavoidable. The requirement of non-risk BCA could delay the process of new BCA approval and BC practices in general. However, this shifting paradigm requires cautious improvement of risk and efficiency the assessment.

Notably, we suggested several ideas of specificity and plasticity evaluations as following.

Methods of host specificity evaluation could be broadened to find correlation among parasitoid traits in combining with different indexes. For example, we could study the set of criteria of host specificity index and correlation performance-host phylogeny, or the set of host specificity index and ovigeny index. Concerning parasitoid plasticity, it should be considered multidimensional concept similar to specificity. The degree of plasticity could be different to each dimension. Parasitoid behavioral plasticity could be understood as the low choosiness towards aphid hosts. Determinants of generalist behaviors in parasitoids could be innate, such as parasitoid time, energy and egg constraints; or through interactions like host deprivation/availability, competition. Determinants of parasitoid physiological plasticity could underly in their venom compositions. Therefore a comparison of venom compositions of parasitoids reared on different hosts over several generations could be interesting. The study of parasitoid plasticity to disturbed conditions should play vital roles in BCA efficiency assessments. Determinants of stress tolerance at both aphid and parasitoid levels should be highlighted. In aphids, this information serves to understand aphid prevalence, in parasitoids to choose relevant BCA. These determinants could be surprisingly similar in both parasitoids and aphids, e.g. multi-dimensional specificity could impact plasticity: generalist vs. extreme specialist parasitoid, time-limited vs. egg-limited, habitat vs. host. The types of stressors such as nutrients or soil salinity could determine the defensive and adaptive strategies of all trophic levels. The frequency, intensity, and duration of stressors: pulsed vs. continuous, high vs. medium, long-term vs. short-term could drive the outcomes of plasticity.

This study of factors modulating the host specificity of aphid parasitoids not only suggest the significant roles of abiotic constraints on BCA but also contributing to more extensive ecological understanding and theory on parasitoid host specialization.

FiguresFigure 1 .

 1 Figures

Figure 2 .

 2 Figure 2. Types of biological control agents.

Figure 3 .

 3 Figure 3. Spatial and temporal scales of the four main approaches of the BC process.

Figure 4 .

 4 Figure 4. Aphid adult morphology.

Figure 5 .

 5 Figure 5. Aphid internal morphology.

Figure 6 .

 6 Figure 6. Egg development from oviposition to first hatching.

Figure 7 .

 7 Figure 7. A conceptual model for the evolution of ecological specialization.

Figure 8 .

 8 Figure 8. Multi-dimensions of the host specificity.

Figure 9 .

 9 Figure 9. A gradation model of host specificity from specialist to generalist based on the number of host species and host phylogeny.

Figure 10 .

 10 Figure10. A hypothetical gradation of host specificity from specialist to generalist.

Figure 11 .

 11 Figure 11. Visualization of aphid host diversity parameters in grey scale.

Figure 12 .

 12 Figure 12. Host selection process.

Figure 13 .

 13 Figure 13. Immature Aphidius ervi pass through different stages inside aphid hosts.

Figure 14 .

 14 Figure 14. Testing schemas to approve one biological control agent.

Figure 15 .

 15 Figure 15. The comparison between fundamental host range tested in the laboratory and the realized host range in the field.

Figure 16 .

 16 Figure 16. The implication of host specificity testing in biological control.

Figure 17 .

 17 Figure 17. An ecosystem consists of six types of interactions among three biotic and three abiotic compartments.

Figure 20 .

 20 Figure 20. Bottom-up impact of plant insecticidal on the community.

Figure 22 .

 22 Figure 22. Aphid immunity interactions.

Figure 21 .

 21 Figure 21. The potential phenotypic response of plants exposed to a combination of water stress and pathogen infection.

Figure 23 .

 23 Figure 23. Impacts of plant, aphid and parasitoid traits on parasitoid host specificity.

Figure 18 .

 18 Figure 18. Multitrophic level interactions might affect herbivorous insects.

Figure 19 .

 19 Figure 19. Ecological interactions impact the efficacy of aphid parasitoids in greenhouse conditions.

Figure 24 .

 24 Figure 24. Could abiotic environmental stresses imply bottom-up effects on parasitoid host specificity?

Figure 26 .

 26 Figure 26. Lists of aphids and the phylogenetical relationship among them.

Figure 27 .

 27 Figure 27. Host specificity testing in the laboratory.

Figure 28 .

 28 Figure 28. Serial dissections of parasitized pea aphids.

Figure 29 .

 29 Figure 29. The host specificity indexes and the correlation preference-performance of six parasitoids, Aphidius ervi, Diaeretiella rapae, Aphelinus abdominalis, Binodoxys communis, B. koreanus and Lysiphlebus testaceipes.

Figure 30 .

 30 Figure 30. Host specificity of Aphelinus abdominalis (A), Diaeretiella rapae (B) and Aphidius ervi (C).

Figure 31 .

 31 Figure 31. Phylogenetical relationships among Aphidiinae parasitoids Figure 32. Parasitoid responses at each step of parasitism process and possible mechanisms of their mortality.

Figure 33 .

 33 Figure 33. Synthesis of bottom-up effects of plants on parasitoid community.

Figure 34 .

 34 Figure 34. Host range testing of Aphidius ervi under water limitation condition.

Figure 35

 35 Figure 35 Impacts of soil water limitation on the relation preference -performance of Aphidius ervi.

Figure 36 .

 36 Figure 36. Distribution of studies on bottom-up effects of abiotic stress.

  prédire l'efficacité et les impacts non ciblés des ALB avant leur libération. Mon travail de thèse s'est concentré sur la spécificité d'hôtes des parasitoïdes dans un système tritrophique 'plante -puceron -parasitoïde'. L'espèce et la qualité des plantes, l'espèce et la qualité des pucerons ainsi que le comportement et la physiologie des parasitoïdes sont des facteurs susceptibles de modifier cette spécificité d'hôte. L'environnement abiotique est également susceptible de moduler cette spécificité. Cette étude propose donc tout d'abord d'évaluer cette spécificité d'hôte avec des tests comportementaux et physiologiques, puis de tester l'impact de différents facteurs biotiques et abiotiques susceptibles de la moduler. Le chapitre I rappelle le concept de spécialisation écologique et les méthodes d'évaluation de la spécificité d'hôte. Dans notre cas, la spécialisation écologique représente la gamme d'hôte appropriée d'un parasitoïde i.e. le nombre d'hôtes dans lequel il peut effectuer un développement complet. Deux tendances opposées existent : les espèces spécialistes (peu d'hôtes) et les espèces généralistes (large choix d'hôte). Mais à partir de quel seuil peut-on considérer qu'une espèce est généraliste ou spécialiste ? Existe-t-il un continuum entre ces deux tendances ? Quelle serait la stratégie dominante et valorisée sur le plan évolutif ? Cette stratégie dominante dépend-elle du contexte environnemental ? La présence d'idées opposées pendant des décennies révèle la complexité de la question de la spécialisation écologique et des supports empiriques existent pour chaque hypothèse. Les principes et les applications des méthodes de test de la gamme d'hôtes sont également rappelées dans ce chapitre. Il existe en l'occurrence de nombreuses options pour améliorer ces méthodes en précisant le degré de spécialisation au sein du continuum généraliste-spécialiste. Nous avons choisi d'utiliser deux méthodes d'évaluation pour la suite de notre étude : l'indice de spécificité d'hôte et la corrélation entre la préférence des parasitoïdes (traits comportementaux) et leur performance (traits physiologiques). Le chapitre II rappelle le contexte écologique des effets possibles des facteurs environnementaux sur les réseaux écologiques et notamment trophiques. Un niveau trophique peut réguler d'autres niveaux trophiques par leur interaction par le biais de forces ascendantes ou descendantes. Les forces ascendantes (bottom-up forces) signifient que les ressources (niveau trophique inférieur ou bottom) influencent les consommateurs des niveaux trophiques supérieurs (ou up). Les forces descendantes (top-down forces) signifient que les consommateurs (niveaux trophiques supérieurs ou top) influencent les niveaux trophiques inférieurs (ou down). La question de la force dominante dans un écosystème (bottom-up ou top-down) fait toujours débat et des supports empiriques existent pour chaque hypothèse. La première partie du chapitre II rappelle ces différentes hypothèses, dont la démonstration dépend du contexte environnemental (comme pour le débat sur la spécialisation). Dans les deux cas, le rôle des plantes est majeur car les forces bottom-up et top-down sont le plus souvent médiées par ce niveau trophique

Figure 2 .

 2 Figure 2. Types of biological control agents.

Figure 4 .

 4 Figure 4. Aphid adult morphology A: Wingless aphid with body parts as head, thorax, abdomen, siphunculus, attena, and cauda. B: Winged aphids (from van Emden and Harrington 2007)

Figure 5 .

 5 Figure 5. Aphid internal morphology (picture of The American Phytopathological Society 2017). Salivary gland excretes saliva to plant phloem and help aphids to avoid the plant immune system. During the phloem sucking process, aphids could also transmit viruses.

Figure 6 )

 6 Figure6). During their development, immature parasitoid produces an embryo structure with a thick wall to protect eggs. The structure is thought to adapt to the deficient nutrient reserves of A. ervi eggs which are fluid-filled, yolkless, and contain only few lipid globules. Under nutrient constraint, early egg development depends on how fast the embryo uptake resources from its host and defend against the immune systems. The embryo complexity of A. ervi different from other taxa-closed parasitoids and shared-host parasitoids, i.e. Praon pequodorum[START_REF] Martinez | Specificity of Multi-Modal Aphid Defenses against Two Rival Parasitoids[END_REF], Sabri et al. 2011).

Figure 6 .

 6 Figure 6. Egg development from oviposition to first hatching A: Stage 1 -egg oviposition and hatch B: Stage 2 -from egg hatching to larval development (from Sabri et al. 2011).

Pandit

  et al. (2009) suggest different mechanisms governing each group of habitat specialization that habitat specialists respond to species abundance and diversity or environmental factors and habitat generalists respond to dispersal processes. In other arguments, the authors considered the transition of narrowing (specialization) or broadening (generalization) one species resources is bi-directional and balance in nature (Nosil and Mooers 2005; Angosta et al. 2010).

Figure 7 .

 7 Figure 7. A conceptual model for the evolution of ecological specialization.

Figure 9 .

 9 Figure 9. A gradation model of host specificity from specialist to generalist based on the number of host species and host phylogeny (Adapted from[START_REF] Gagic | The Effects of Aphid Traits on Parasitoid Host Use and Specialist Advantage[END_REF], Poulin 2003; Helmus 2007; Desneux 2012).

Figure 10 .

 10 Figure 10. A hypothetical gradation of host specificity from specialist to generalist based on relative host suitability/preference (Adapted from Klinken 2000, Poulin et Mouillot 2005, Godfray 1994). (A): specialists accept or develop well on only one host species, (B): intermediate specialist/generalist accept/develop on several host species but prefer/perform well on only few host species, (C): generalists which accept and develop relatively well on several host species.

Figure 12 .

 12 Figure 12. Host selection process

Figure 13 .

 13 Figure13. Immature Aphidius ervi pass through different stages inside aphid hosts from eggs -1 st instar -2 nd instar (aphid death) -3 rd instar (pupation, mummy forming) -4 th instar (eclosion) (from Gutierrez-[START_REF] Gutierrez-Ibanez | Pre-pupation behaviour of the aphid parasitoid Aphidius ervi (Haliday) and its consequences for pre-imaginal learning[END_REF]

Figure 14 .

 14 Figure 14. Testing schemas to approve one biological control agent -BCA as ecologically safe and get permitted to use this BCA in the field (van Lenteren 2010).

  ) interactions between organisms and abiotic (non-resource) conditions, -(3) spatial interactions (inputs and outputs of energy, nutrients, organisms), -(4) non-trophic direct interactions among organisms, -(5) physical and chemical interactions among factors/compartments, -(6) external forcing of abiotic conditions.These six types of interactions potentially operate among three biotic and three primary abiotic compartments (Figure17). The abiotic compartments are (1) abiotic resources, such as light, nitrate, ammonium, phosphate, consumed by autotrophs, (2) non-consumed abiotic conditions, such as salinity, soil texture, sediment aeration, soil and water pH, temperature and (3) detritus, i.e. non-living organic material. The main three biotic compartments are (1) autotrophs that can harvest their energy, either from light or chemical sources, (2) microbial detrivores that break down detritus into mineral components, thus producing resources for autotrophs and (3) higher trophic levels that consume autotrophs, microbial detrivores and/or each other, and mineralize nutrients for autotrophs.

Figure 17 .

 17 Figure 17. An ecosystem consists of six types of interactions among three biotic and three abiotic compartments. Three abiotic compartments are (1) abiotic resources, (2) abiotic conditions, and (3) detritus. Three biotic compartments are (1) autotrophs (2) microbial

2. 3 .

 3 Bottom-up forces of abiotic factors on a tritrophic plant-aphid-parasitoid system 2.3.1. How could plant traits mediate bottom-up and top-down forces? Plant traits that determine the tri-trophic interaction include species, nutritional quality, defenses against herbivores, mutualism with soil bacteria and fungi (van Veen 2015). The adaptation of each trophic level to the system are multilateral: plants tolerate or defense against herbivory. Aphids develop top-down offense or counter-defenses against plants, and they defend against parasitism from bottom-up. Parasitoids evolve offense or counterdefenses against aphids and by that indirectly protect plants from their herbivores. In reverse, plants reward their mutualist parasitoid by emitting semiochemicals locating plant hosts or producing nectar as food. However, plants might indirectly harm parasitoids through aphid "arm-race" strategy, as plant toxins sequestering in the aphid host body is lethal to larval parasitoids. The whole system is impacted by surrounding abiotic factors like temperatures, soil conditions, water. Through those interactions, plant quality influenced by abiotic factors might ladder up to the top levels of natural enemies and notably reduce their performance. Parasitoid adapt to the plant hosts of their aphid hosts, e.g. parasitoids on the same plants have the same enzyme families (Ryalls et al. 2017). Parasitoid performance, or more specifically parasitism rate change when aphid hosts feed on different plants (Jervis 2005).

Figure 18 .

 18 Figure 18. Bottom-up impact of plant insecticidal on the community.

  vital defense mechanisms are aphid immune system (innate defenses) (Poirie and Coustau 2011, Error! Reference source not found.2), symbionts-dependent defenses (acquired defenses) (Vorburger 2014) and 'arms-race' defenses (by sequestering plant toxins against natural enemies) (Züst and Agrawal 2016).

  responses of plants to combined stresses depend on what came first and the severity of each stress.[START_REF] Ramegowda | The interactive effects of simultaneous biotic and abiotic stresses on plants: Mechanistic understanding from drought and pathogen combination[END_REF] proposed four scenarios of combined stresses on plants (Error! Reference source not found.1). In the scenario 1, plants undergo combined stresses; water stress happens before pathogen infection. In the second scenario, plants sequentially expose to water stress then pathogen infection. In the third one, water stress and pathogens simultaneously happen. In the fourth one, plants undergo combines stress but being pathogen infested first. All scenarios could lead to two possible outcomes: plants increase stress resistance or stress susceptibility due to the same mechanisms.

Figure 20 .

 20 Figure 20. The potential phenotypic response of plants exposed to a combination of water stress and pathogen infection.

Figure 21 .

 21 Figure 21. Impacts of plant, aphid and parasitoid traits on parasitoid host specificity. The green arrow and texts mean plant traits. The blue arrow and texts mean aphid traits. The orange texts mean parasitoid traits. The continued line means direct effects. The dashed line means indirect effects.

Figure 22 .

 22 Figure 22. Multitrophic level interactions might affect herbivorous insects 1. direct bottomup effects, 2. direct top-down effects, 3. direct competition, 4. apparent competition, 5.induced defenses, 6. host-plant quality affecting natural enemies (fromGripenberg et al. 2007).

Figure 23 .

 23 Figure 23. Ecological interactions impact the efficacy of aphid parasitoids in greenhouse

Figure 24 .

 24 Figure 24. Could abiotic environmental stresses imply bottom-up effects on parasitoid host specificity? The green arrow and texts mean plant traits. The blue arrow and texts mean aphid traits. The orange texts mean parasitoid traits. The continued line means direct effects. The dashed line means indirect effects. The plus (+) symbols mean positive effects; the minus (-) symbols mean negative effects.

  strategy of being physiologically adapt to a wide range of hosts relate to the less choosiness behavior (as known as the generalist behavior)? Do the change in preference/performance could result in the change of host specificity. In other terms, do parasitoids become more specialist or generalist under field conditions?The primary goal of this chapter was finding an intermediate specialist/generalist parasitoid to detect their adaptation, as they could be flexible toward both directions of specificity spectrum. Our objectives are (1) to assess the fundamental host range in laboratory conditions for three parasitoids(2) calculating the host specificity index and analyze the preference-performance of six parasitoids based on the set of data generated in our laboratory (article 1), and (3) to compare the fundamental host range, the field host range reported from the literature and the correlation preference-performance pattern to propose specific and quantifiable criteria to classify host specialist/generalist parasitoids. The three parasitoids A. ervi, D. rapae and A. abdominalis are good models to test our question because they are BCA, are considered host generalists and represent two different families of parasitoids with different life-history traits. Our study could provide information on the host switching ability and ecological risks on non-target species of specific biotype parasitoids that are legally mandatory.

Figure 25 .

 25 Figure 25. Morphology of the three parasitoids: Diaeretiella rapae, Aphidius ervi and Aphelinus abdominalis(From Bernard Chaubet, INRA)

Figure 26 .

 26 Figure 26. Lists of aphids and the phylogenetical relationship among them

Figure 27 .

 27 Figure 27. Host specificity testing in the laboratory. Parasitoid behavioral traits (preference) are subsequent actions leading to host acceptance or rejection. Physiological host range (performance) is the number of species in which the parasitoid could fully complete its development.

Figure 28 .

 28 Figure 28. Serial dissections of parasitized pea aphids

to 2 .

 2 55 in order of decreasing specificity: D. rapae,A. abdominalis, A. ervi, L. testaceipes, B. koreanus and B. communis. Their Rhode indexes of specificity (SS) range from 0.37 to 0.70 in order of decreasing specificity: L. testaceipes, A. abdominalis, D. rapae, A. ervi, B. communis and B. koreanus. The correlation preference-performance exist for A. ervi, L. testaceipes and B. communis, which are more specialists, but not for D. rapae and A. abdominalis which are more generalists based on STD*. The existence of correlation pattern in these parasitoids are therefore relevant to the degree of specificity measured by STD*.

Figure 29 .

 29 Figure 29. The host specificity indexes and the correlation preference-performance of six parasitoids, Aphidius ervi, Diaeretiella rapae, Aphelinus abdominalis (Monticelli, Nguyen, et al. 2018), Binodoxys communis, B. koreanus and Lysiphlebus testaceipes (data generated in the laboratory). The blue arrow means Rohde index of specificity (SS), the bigger the index, the more specialist parasitoid. The green arrow means the taxonomic index of specificity (STD*), the smaller the index, the more specialist parasitoid. The red check means the correlation preference-performance exists for that parasitoid. The green X means there is no correlation preference-performance.

  Figure 30. Host specificity of Aphelinus abdominalis (A), Diaeretiella rapae (B) and Aphidius ervi (C). Results from the non-choice host specificity assay in the laboratory.

Figure 31 .

 31 Figure 31. Phylogenetical relationships among Aphidiinae parasitoids

  Experiment 2: performance.The physiological host range was established observing the parasitoids development in the different aphid species. Aphids previously stung in experiment 1 were isolated in plastic Petri dishes on one leaf of their respective host plant in a climatic room at 23  1 °C, RH 65  5% and photoperiod 16:8 L:D. Because a higher number of replicates was needed in experiment 2, additional replicates were performed in the same conditions of experiment 1 (without recording the parasitoid behavior).Parasitoid development within the hosts was monitored at four different times. The aphids were dissected (1) after being stung (monitoring egg survival) under a binocular microscope at 100x magnification, (2) after 4 days (tracking larvae survival) under a binocular microscope at 40x magnification, (3) after 7 days to monitor aphid mummification, and (4) the emergence rate and the sex ratio was finally recorded.Experiment 3: Presence of secondary endosymbionts in aphids.To tested the impact of aphid secondary endosymbionts on the development of juvenile parasitoids, all of the aphid species were screened to detect the presence of 9 facultative symbionts genera that are known to interact with aphids(Ferrari and Vavre 2011):Arsenophonus, Hamiltonella defensa (T-type), PAXS (Pea-aphid X-type symbiont), Regiella insecticola (U-type), Rickettsia, Rickettsiella, Serratia symbiotica (R-type), Spiroplasma, Wolbacchia.Insect sampling and DNA extraction. 0.01 g of aphids were collected from each aphid colony.Each sampling was washed in 70 % ethanol for 2 to 5 minutes (aphid size dependent) rinsed in PBS (phosphate buffer solution) for 1 minute and finally washed in pure water. Samples were homogenized with a piston (1 piston/sample) in Lysis buffer for DNA extraction. Then, samples were placed in 10 L of RNase A, 50 L of lysozyme and 20 L of protease K and incubated at 55 °C for 1 hour. For DNA purification, samples were centrifuged at 3000 rpm for 5 minutes, and the supernatants were collected. 1mL of absolute ethanol and 50 L of sodium acetate were added and the mixture was placed in -20°C overnight. Samples were then centrifuged at 14000 rpm for 20 minutes, and the supernatants were removed. After adding 1mL of 70 % ethanol, the mixture was homogenized and centrifuged at 14000 rpm for 5 minutes. After 5 minutes at room temperature to let the pellet dry, 50 L of pure water was added to the pellet and then stored at -20 °C until used. The quantity and quality of the DNA were measured with the NanoDrop and diluted to obtain 50 g of DNA /µL for each sample.

  the host specificity and was computed with the program TaxoBiodiv2(Poulin and Mouillot 2005) with a taxonomic tree of hosts build on family, tribes, genus, and species (Blackman and Eastop 2006). The index was computed for each parasitoid species tested and for three other specialist parasitoid species: Binodoxys communis(Desneux et al. 2009a), Binodoxys koreanus[START_REF] Desneux | Cryptic species of parasitoids attacking the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in Asia: Binodoxys communis Gahan and Binodoxyx koreanus Stary sp. n. (Hymenoptera: Braconidae: Aphidiinae)[END_REF] and Lysiphlebus testaceipes (from France and USA; Desneux & Heimpel, unpublished data).

  X 2 1 = 23.53, P > 0.05, dispersion parameter = 11.71, Figure3 and S1, A).The highest adult survival rate for A. ervi was in A. pisum, M. euphorbiae (tomato plant) and S. avenae. The proportions of adults emerged ranged from 0.43 to 0.69 (Figure2, B). The other aphid species could be separated by the stages at which the parasitoid development failed. Firstly, fewer eggs were deposited in B. brassicae, and S. graminum compare to the proportion of egg deposited in the rearing host (P < 0.01; P = 0.043, respectively). Then, a significant parasitoid egg mortality was observed in M. euphorbiae (potato plant) (P < 0.01) but the proportion of parasitoid larvae in this aphid species was not different compared to the proportion of larvae in the rearing host (P > 0.05). The parasitoid mortality between the larval and the mummy stage were observed in A. craccivora, A. fabae, A. gossypii, A. nerii, M. dirhodum and R. padi, (all P < 0.045); and the proportion of mummies was significantly different than the proportion of mummies in the rearing host (P < 0.01). Finally, for M.

  linked to actual suitability for offspring development in the parasitized host species. The two secondary endosymbionts H. defensa and R. insecticola were detected in only two host species (M. dirhodum and A. fabae) and the host specificity index indicated that D. rapae and A. abdominalis are true generalist parasitoids whereas A. ervi and L. testaceipes are likely intermediate specialist-generalist, and B. communis and B. koreanus are specialist

  koreanus are specialized on the Aphis genus(Desneux et al. 2009 a, b) whereas L.testaceipes is specialized on the Aphidini tribe(Desneux & Heimpel, unpublished data, figure 4). By contrast, A. abdominalis and D. rapae had a successful development in both tested tribes and in different genus tested. However, A. ervi showed a lower host specificity index than the two other generalist species because its performance was more efficient on host from Macrosiphini tribe(Zepeda-paulo et al. 2013, Raymond et al. 2015), indicating that A.

  abdominalis and D. rapae, due to their low host selectivity and their high performance among the hosts. A. ervi is considered as an intermediate specialist-generalist because it showed a successful development only in three of the aphid species stung; and its low selectivity can be explained by its strategy to avoid aphid defenses (highly aggressive and quick oviposition when it encountered hosts;Bilodeau et al. 2013). Furthermore, a possible phylogenetical signal could exist among its hosts(Zepeda-Paulo et al. 2013); suggesting a host phylogenetic specialization (as for B. communis,Desneux et al. 2012).

Figure 1 :

 1 Figure 1: Relationship between the stinging rate (preference) and the aphid defensive

Figure 2 .

 2 Figure 2. Proportion of stinging aphids that: contained an egg (dissection after stung),

Figure 3 .

 3 Figure 3. Relationship between the stinging rate (preference) and the emergence rate

Figure 4 .

 4 Figure 4. Host specificity index (STD*) values and ranking of the parasitoids according to their

  Figure 1. 18

  Figure 4.

Figure 32 .

 32 Figure 32. Parasitoid responses at each step of parasitism process and possible mechanisms of their mortality (from Desneux 2009a).

  temperature on parasitoids, e.g. storage temperature without plant or aphid presence are not considered.

  Results were found from the database of Web of Science ®. Codes of experimental scales: laboratory: L, Greenhouse: G, Field: F, Observation in the field: O. NE stands for all parasitoids. Year Scale Parasitoid species Reference 2012 O Diaeretiella rapae Amini et al. (2012) 2013 L Aphidius ervi Aslam et al. (2013) 2011 L Aphidius ervi Johnson et al. (2011) 2013 L Diaeretiella rapae Romo and Tylianakis (2013) 2011 G Aphelinid spp. Shipp et al. (2011)2013L Aphidius colemaniTariq et al. (2013)

Figure 34 .

 34 Figure 34. Host range testing of Aphidius ervi under water limitation condition. The redboxed aphid names were chosen for the previous experiment (chapter 4): Sitobion avenae and Acyrthosiphon pisum (good hosts), Myzus persicae and Macrosiphum euphorbiae (medium hosts), Rhopalosiphum padi (reported as host in the field), and Aphis nerii (attacked at high rate but unsuitable for A. ervi development).

Figure 1 .

 1 Figure legend.

Figure 2 .

 2 Figure 2. The proportion of successfully stung aphids [Acyrthosiphum pisum on Bean (A),

  Figure 1 463

  instar aphids on LW and OW plants on a Petri-dish cage system of 85mm-diameter covered by mesh. When second aphid generations were born, we removed aphid parents and used offspring aphids for evaluating aphid performance. 1-day-old aphids from the same cohort were then individually confined into clip-cages attached to the experimental leaves in all plants from LW and OW conditions, ten clip-cages per plant, three plants per treatment. We measured the survival rate as the number of aphids surviving after seven days in clip-cages per total clip-caged aphids. The generation time ( D) was determined by recording duration from aphid to their first reproduction. The intrinsic rate of the increase relates the fecundity of an individual aphid to its development time: rm = (lnMd x 0.738) / D, where Md is the number of nymphs produced by the adult in the first D days of reproduction after the adult molt (van Emden and Harrington 2007).

  2D). Water use efficiency WUE of milkweed and potato only marginally increased (p value = 0.059 for both plants). Impact of water limitation on aphid performance: survival rate, generation time and intrinsic rate of development The life-history traits of A. pisum and A. nerii including survival rate, generation time (D), and intrinsic rate of development (rm) were not significantly different between LW and OW (p value > 0.05) (Figure 3A, B, C). The generation time of three species S. avenae, M. persicae and M. euphorbiae were significantly reduced in LW plants (factorial ANOVA tests for S. avenae: p value = 0.0036, F1,19 = 11; for M. persicae: p value = 0.026, F1,28 = 5.56; for M. euphorbiae: p value < 0.001, F1,30 = 33.41). The intrinsic rate of development of three species R. padi, M. persicae and M. euphorbiae were significantly reduced in LW plants (R. padi: F1,43 = 7.16, p value = 0.01; M. persicae: F1,30 = 4.29, p value = 0.047; M. euphorbiae: F1,49 = 33.41, p value < 0.001).

  , carbon content (Reddy et al. 2004), increase ratio C: N which is an indicator for plant defensive compound concentration (Royer et al. 2013). Higher sugar concentration in phloem and weaken the immune defense of plants due to water scarcity might lead to aphid preference on stressed plants. But plant poor nutrient quality (plant stress hypothesis) lead to aphids smaller in size, lower in nutrient quality to bear parasitoid larvae. But the impacts depend as

  Figure 1A, B, C. Plant height and plant nodes, respectively (N = 16-99) of 5 plants: bean,

Figure

  Figure 2A, B, C: Leaf photosynthesis rate, transpiration rate, and stomatal conductance (95%

Figure

  Figure 3A, B, C: Survival ratio, generation time (D) and intrinsic rate of development (rm) of

Figure

  Figure 4A, B, C. Preference and performance of Aphidius ervi while encountering six aphid

  Figure 1A802

  Figure 1C806

Figure 36 .

 36 Figure 36. Distribution of studies on bottom-up effects of abiotic stress

  Table of Contents .

Table 1 .

 1 Specialists vs generalists: pros and cons in biological control

	Trade-off hypothesis Specialist Generalist
	Ecological safety	+++	-
	Pest control efficiency	++	+
	Establishment success	++	+
	Adaptability	-	++

Table 2 .

 2 Host specificity of five a priory defined categories displayed over host range.

	A-monophagous, B-narrow oligophagous, C-moderate oligophagous, D-broad
	oligophagous, E-polyphagous (from Zikic et al. 2017).

Host specificity group Species host range Generic host range Subfamily host range Average host range (species- genus-subfamily)

Commensalism One species obtain benefits such as food, shelter, or locomotion from another species without causing adverse effects

		-antagonistic	plants -	Polis et al. 1989
	Herbivory	(against each	herbivores	Olff et al. 2009
	Predation	other)	preys -
	Parasitism	-direct	predators
		-reciprocal	hosts -
			parasitoids
	Direct competition (intraspecies)		intra-guild,
	Competition	-antagonistic	inter-guild	Holt 1977
	-Apparent (two preys/host	-indirect		Elias et al. 2013,
	species share one predator	-reciprocal		Montoya et al.
	/parasitoid)			2006
	-Exploitative (two
	predators/parasitoids share one
	prey/host species)
	Facilitation			Callaway 2007
	Mutualistic	-benefits for	flowers -	Oksanen 1988;
	Facultative	both partners	pollinators	Vandermeer
	Obligate	-indirect or	bacterial	1980; Ulanowicz
		direct	symbiosis -	1997
		-reciprocal	aphids
		-positive	clownfish and	Olff et al. 2009
		-direct	corals	Mougi 2016
		-unilateral

Amensalism One organism harm another organism without receiving any costs or benefits

	-negative	Penicillium kills	Olff et al. 2009
	-direct	certain bacteria
	-unilateral	by producing
		penicillin

  plants, the aphid tribe and the number of replications performed in experiments for each parasitoid species are reported Table1. Twelve aphid species spread over two different tribes (aphidini and macrosiphini) were used in this study and were chosen to encompass a wide phylogenetic range of aphid species (van Emden and Harrington 2007). Among this aphid species, Macrosiphum euphorbiae was maintained on two plant species: Solanum Parasitoids and aphid species were reared in climatic cabinets (23  2 °C, RH 65  5% and photoperiod 16:8 L: D h) and parasitoids were maintained on their main hosts in the field: Acyrthosiphum pisum for A. abdominalis and A. ervi and Brevicoryne brassicae for D.

tuberosum identified by (P) and S. lycopersicum identified by (T) in the text and the other figure and table. Also, there were two phenotypes of Myzus persicae (one green and one red).

  The impact of H. defensa in the D. rapae development cannot be discussed because A. fabae and M. dirhodum are low parasitized. However, a high parasitoid larval mortality of A. ervi was observed when it encountered A. fabae and M. dirhodum, whereas H. defensa was detected in A. fabae and M. dirhodum and R. insecticola was also detected in

M. dirhodum (as reported by

[START_REF] Lukasik | Horizontal transfer of facultative endosymbionts is limited by host relatedness[END_REF]

. However, A. ervi is well known to parasite Macrosiphininae species such as A. pisum, M. euphorbiae, S. avenae and M. dirhodum

[START_REF] Stary | The Fate of Released Parasitoids (Hymenoptera, Braconidae, Aphidiinae) for Biological-Control of Aphids in Chile[END_REF], Kavallieratos et al. 2004)

, suggesting that the presence of H. defensa and/or R. insecticola reduces the A. ervi host range. Several studies have shown that endosymbionts confer protection only against the more specialized natural enemies and not against generalist ones

[START_REF] Parker | Symbiont-Mediated Protection against Fungal Pathogens in Pea Aphids: a Role for Pathogen Specificity?[END_REF], Asplen et al. 2014, Hrcek et al. 2016, Kraft et al. 2017)

, which consolidate the hypothesis whereby A. ervi is an intermediate specialist-generalist.

  sting rate (0.73 and 0.56 respectively). However, D. rapae is well known to have a successful development in B. brassicae; suggesting the success of the acclimation through phenotypic plasticity for this parasitoid. By contrast, M. persicae is not a glucosinolate-sequestering aphid whether it feeds on cabbage too. It excretes the glycosinolates in its honeydew, and the impact on parasitoid offspring development is low(Weber et al. 1986, Merritt 1996, Francis et al. 2001). In our study, A. abdominalis has a successful development in M. persicae (0.73 adults in the next generation) compared to no

. The specialist aphid species A. nerii and B. brassicae are known to sequester cardenolide (Asclepias) and glucosinolate (cabbage) respectively

(Desneux et al. 2009a[START_REF] Jones | Purification and characterisation of a non-plant myrosinase from the cabbage aphid Brevicoryne brassicae (L.)[END_REF]

) and these toxic allelochemical molecules have a drastic impact on immature parasitoid survival

[START_REF] Mooney | Coexisting congeners: demography, competition, and interactions with cardenolides for two milkweed-feeding aphids[END_REF][START_REF] Pratt | Accumulation of Glucosinolates by the Cabbage Aphid Brevicoryne brassicae as a Defense Against Two Coccinellid Species[END_REF], Desneux et al. 2009a, Kos et al. 2011)

. The three generalist parasitoids cannot successfully parasitize A. nerii despite a high sting rate (ranged from 0.55 to 0.84). They all reached the larval stage and then died. Similarly, A. abdominalis and A. ervi cannot successfully parasitize B. brassicae despite a high development at all in B. brassicae, indicating that A. abdominalis is strongly affected by glycosinolates. However, A. ervi cannot parasitize M. persicae whereas it is a suitable host

Table 1 .

 1 Desneux, N., Starý, P., Delebecque, C. J., Gariepy, T. D., Barta, R. J., Hoelmer, K. A., & Aphid species, their color, host plants and the number of replicates for each experiment (1, 2 or 3). Specifically, for the experiment 1 and 2, the number of experiment is followed by the number of replicates in the whole experiment for A. abdominalis, A. ervi and D. rapae respectively.

	Heimpel, G. E. (2009b). Cryptic Species of Parasitoids Attacking the Soybean Aphid
	(Hemiptera: Aphididae) in Asia: Binodoxys communis and Binodoxys koreanus
	(Hymenoptera: Braconidae: Aphidiinae). Annals of the Entomological Society of
	America, 102(6).
	Desneux, N., Barta, R. J., Delebecque, C. J., & Heimpel, G. E. (2009c). Transient host paralysis
	as a means of reducing self-superparasitism in koinobiont endoparasitoids. Journal of
	Insect Physiology, 55(4): 321-327.

Devictor, V., Clavel, J., Julliard, R., Lavergne, S.,

Mouillot, D., Thuiller, W., … Mouquet, N. (2010)

.

Defining and measuring ecological specialization. Journal of Applied Ecology, 47(1): 15-25. Driessen, G., Hemerik, L. & Boonstra, B. (1991). Host selection behaviour of the parasitoid Leptopilina clavipes, in relation to survival in hosts. Neth. J. Zool. 41:99±111 Dunning, C. E., Redak, R. A., & Paine, T. D. (2003). Preference and performance of a generalist insect herbivore on Quercus agrifolia and Quercus engelmannii seedlings from a southern California oak woodland. Forest Ecology and Management, 174(1-3): from First (Brassicaceae) and Second (Myzus persicae and Brevicoryne brassicae) Trophic Levels on Adalia bipunctata. Journal of Chemical Ecology, 27(2): 243-256.

Friberg, M.,

Posledovich, D., & Wiklund, C. (2015)

. Decoupling of female host plant preference and offspring performance in relative specialist and generalist butterflies.

Oecologia, 178(4): 1181-1192.

Futuyma, D. and Moreno (1988)

. The Evolution of Ecological Specialization. Annual Review of

Ecology and Systematics, 19

(1): 207-233. Gagic, V., Petrović-Obradović, O., Fründ, J.,

[START_REF] Gagic | The Effects of Aphid Traits on Parasitoid Host Use and Specialist Advantage[END_REF]

. The Effects of Aphid Traits on Parasitoid Host Use and

Table 2 .

 2 Proportions of aphid detected, accepted, and stung by A. abdominalis (Aa), A. ervi (Ae) and D. rapae (Dr) respectively when they encountered different aphid species (experiment 1).

		Proportion of aphids detected	Proportion of aphids accepted	Proportion of aphids stung
	Aphid species /Parasitoid species Aa	Ae	Dr	Aa	Ae	Dr	Aa	Ae	Dr
	Acyrhtosiphum pisum	1	1	1	0.97	0.95	0.83	0.91	0.95	0.77
	Aphis craccivora	1	1	0.58	0.48	0.5**	0.19***	0.48	0.49**	0.13***
	Aphis fabae	0.94	0.92	0.83	0.34***	0.48**	0.3**	0.31***	0.42**	0.17***
	Aphis gossypii	0.91	0.96	0.93	0.34*** 0.77	0.47*	0.25*** 0.77	0.37***
	Aphis nerii	1	0.98	0.97	0.89	0.68	0.74	0.84	0.68	0.55*
	Brevicoryne brassicae	0.97	0.96	1	0.73	0.57*	0.98	0.73	0.56*	0.96
	Macrosiphum euphorbiae (P)	0.97	1	0.77	0.94	0.96	0.43*	0.94	0.92	0.17***
	Macrosiphum euphorbiae (T)	0.97	1	0.93	1	0.88	0.37**	0.91	0.71	0.17***
	Metopolophium dirhodum	0.97	0.96	0.77	0.81	0.93	0.23***	0.69	0.87	0.2***
	Myzus persicae (Green)	0.97	0.97	1	0.84	0.94	0.79	0.77	0.94	0.67
	Myzus persicae (Red)	0.97	1	0.93	0.69	0.93	0.63	0.69	0.91	0.54*
	Rhopalosiphum padi	1	0.92	0.94	0.82	0.55*	0.47*	0.67	0.52*	0.38***
	Schizaphis graminum	0.97	0.91	0.98	0.81	0.71	0.95	0.81	0.64	0.95
	Sitobion avenae	1	1	1	0.89	0.92	0.84	0.86	0.9	0.76

* P < 0.05, ** P < 0.01, *** P < 0.001 means a significant difference compare to the rearing host (A. pisum for A. abdominalis and A. ervi and B. brassicae for D. rapae (in italic)) by GLM followed by multi-comparison test.

Table 3 .

 3 Female sex ratio (proportions females) for each parasitoid species developing on different hosts.

	Female sex ratio (proportion females)

  chose the following combination of keywords for searching on Web of Science ®: (((aphid*

OR apheli*) AND parasitoid AND (stress* OR abiotic OR drought OR water OR inundation OR logged OR dry OR dessic* OR sal* OR temperature OR winter OR cold OR heat OR cool OR thermal OR nutri* OR fertili* OR nitrog* OR potassium OR phosphat* OR light OR UV OR ozone OR elevated OR climat* OR weather OR plant condition OR plant quality OR bottom-up OR humidity OR wind)) NOT whitefly NOT moth NOT coccine* NOT ladybeetle).

Table 2 .

 2 Bottom-up effects of abiotic factors including water supply, nutrient supply, light, and temperature. The data were analyzed by Pearson's Chi-squared test with Yate continuity correction (test of significance) to compare the performance of plants, aphids, and parasitoids between optimal and stress conditions. Code of the threshold to reject the null hypothesis of no difference between optimal and stress For this study, we focused on water limitation. Firstly, water stress is one of the most common abiotic factors that adversely affected the agriculture, perturbed the agrosystem and cause severe economic and social damage(FAO 2015;[START_REF] Ziolkowska | Socio-Economic Implications of Drought in the Agricultural Sector and the State Economy[END_REF]. Secondly, water limitation could have bottom-up effects (indirect impacts starting from lower trophic level) on

	condition:
	* p value < 0.05, ** p value < 0.01, *** p value < 0.001, N/A: not enough data to conclude
	Factor	Trophic	Impacts of abiotic stress	χ²	p value	Statistical
			(Numbers of variables of organism's performance)			significance
			positive	negative	not significant
			(control < treat)	(control > treat)	(control = treat)
	1. All stress	All	192	409	16	39.72	< 0.001	***
	2. All drought	All	25	86	1	16.89	< 0.001	***
	3. Continous	All	18	71	1	15.95	< 0.001	***
	drought
	4. Pulsed drought	All	7	15	0	0.85	0.358
	5. Light	All	35	80	1	8.32	0.004	**
	6. Nutrients	All	42	46	0	0.02	0.880
	7. Temperature	All	90	197	14	19.87	< 0.001	***
	8. Continous T°	All	20	31	0	0.79	0.373
	9. Pulsed T°	All	70	166	14	19.53	< 0.001	***
	10. All stress	Parasit	113	219	12	16.72	< 0.001	***
		oids
	11. All drought	Parasit	14	41	0	5.99	0.014	*
		oids

  A. ervi toward hosts might be only slightly modulated by bottom-up force occurring through water stress applied to actual plants bearing the host aphids. No drastic difference was observed in detection, acceptance and stinging rates of A. ervi when parasitizing five of the six aphid species tested (R. padi, M. euphorbiae, A. nerii, A. pisum and S. avenae) on LW vs. OW plants. The host selection behavior in Aphidiine aphid parasitoids relies on host-associated cues, both from the host external and internal, e.g. haemolymph quality assessed during insertion of the ovipositor[START_REF] Larocca | Functional bases of host-acceptance behaviour in the aphid parasitoid Aphidius ervi[END_REF]. The present study hinted that such traits were not modified in the tested aphid species, at least not enough for changing the parasitoid host selection pattern. However, it could not be excluded that potential difference may occur in harsher bottom-up force conditions, i.e. that was not tested in the present study, e.g. stresses inducing more variations in aphid physiology. It may also indicate that A. ervi, being an intermediate generalist-specialist, may not be adapted to detect tedious differences in quality of hosts encountered. By contrast, the parasitoid behavior pattern, here detection rate, was modified when parasitizing the aphid M. persicae on LW plant. Host detection step by aphid parasitoid relies mostly on chemical cues on aphid cuticles[START_REF] Hatano | Chemical cues mediating aphid location by natural enemies[END_REF]), e.g. glucosinate[START_REF] Pratt | Accumulation of Glucosinolates by the Cabbage Aphid Brevicoryne brassicae as a Defense Against Two Coccinellid Species[END_REF]. Water stress-associated decrease of glucosinate induction in plants(Khan et al. 2011) may translate to a reduction of this compound in M. persicae cornicle secretion(Blande et al. 2008). Therefore, the decrease in M. persicae detection by A. ervi females may be related to such reduction of glucosinolate in the aphid cornicle secretion.Aphidius ervi showed reduced performance developing in high-quality hosts, i.e. S. avenae, M. persicae, and M. euphorbiae reared on plants suffering water stress (reduced mummy and adult numbers). It did not occur when developing in its natal host, A. pisum, on which the parasitoid performed well independently of the water stress applied to host plant (bean). Inadequate or imbalanced nutrients could play a role in significant mortality during the mummy stage of parasitoids (also evidence are scarce). Juvenile larval performance depends on host size and age at parasitism, which correlates with host nutritional quality in aphid parasitoids

	Parasitoid performance under bottom-up force

Table 1 .

 1 Effect of water stress on plant morphological traits and leaf gas exchange activities analyzed by factorial ANOVA test. The asterisks indicate critical probability threshold

(significance code: 0 '***' 0.001 '**' 0.01 '*' 0.05) that the observed data are inconsistent with the null hypothesis of no difference or no association between variables in case of covariance or correlation test, respectively. N/A means no information.

Table 2 .

 2 Effect of water stress on aphid survival ratio, generation time (D) and intrinsic rate of

	development (rm) of aphids feeding on plants of optimal water (OW) and limited watered (LW)
	supply, analyzed using Fisher's exact test for survival ratio and factorial ANOVA analysis for D
	and rm. The asterisks indicate critical probability threshold (significance code: 0 '***' 0.001
	'**' 0.01 '*' 0.05) that the observed data are inconsistent with the null hypothesis of no
	difference or no association between variables in case of covariance or correlation test,
	respectively.

Table 3 .

 3 Impacts of plant water limitation on the preference and performance of Aphidius Macrosiphum euphorbiae on potato. Behavioral and suitable traits of Aphidius ervi on one species under LW and OW were compared using pairwise Fisher exact test. The asterisks indicate critical probability threshold that the observed data are inconsistent with the null hypothesis of no difference between variables (P value <P value < .05).

ervi while encountering six aphid species: Aphis nerii on milkweed, Myzus persicae on cabbage, Rhopalosiphum padi on wheat, Sitobion avenae on wheat and Acyrthosiphon pisum on beans and

Table 4 .

 4 Comparison of behavioral stages or fitness gain during parasitoid parasitism; using multiple comparisons Fisher's exact tests with Bonferonni adjustment method. The asterisk means the probability of rejecting the null hypothesis below the threshold value (adjustedp value < 0.0167 in preference traits and p value < 0.0083 in performance traits).

Table 5 .

 5 The relationship between parasitoid preference for and performance on (logistic

regression) a range of aphid hosts, Aphis nerii on milkweed, Myzus persicae on cabbage, Rhopalosiphum padi on wheat, Sitobion avenae on wheat and Acyrthosiphon pisum on beans and Macrosiphum euphorbiae on potato under optimal and limited water supply. The parasitoid preference represented by the successful sting rate from total behavioral observations, the parasitoid performance represented by the successful emergent rate from the follow-up of total stung aphids. The asterisks indicate critical probability threshold (significance code: 0 '***' 0.001 '**' 0.01 '*' 0.05) that there is no association between variables in correlation test.

001 *** < 0.001 *** < 0.001 *** < 0.001 *** 0.018 * F F1,30 = 15.47 F1,24 = 21.38 F1,52 = 34.06 F1,29 = 17.88 F1,27 = 6.323

	828	Table 1
		Effect of water stress	Water stress duration	Bean	Wheat	Cabbage	Milkweed	Potato
			(week-old)	3-5	3-5	3-10	3-11	3 -7
		Plant height	p value	< 0.001 ***	0.023 *	0.621	< 0.001 ***	< 0.001 ***
		(H)	F	F1,30 = 34.28	F1,26 = 5.81	F1,16 = 0.254	F1,127 = 42.21	F1,99 = 50.89
		Number of nodes	p value	< 0.001 ***	N/A	0.008 **	< 0.001 ***	N/A
		(N)	F	F1,16 = 26.51		F1,16 = 9.262	F1,127 = 19.06
		Leaf mass area	p value	0.825	0.013 *	0.548	0.638	0.232
		(LMA)	F	F1,54 = 0.05	F1,23 = 7.20	F1,52 = 0.366	F1,29 = 0.226	F1,27 = 1.494
		Photosynthesis	p value	0.125	0.605	< 0.001 ***	0.002 **	0.012 *
			F	F1,30 = 2.487	F1,24 = 0.275	F1,68 = 17.23	F1,29 = 11.7	F1,27 = 7.293
		Conductance < 0.Transpiration p value p value 0.00292 **	< 0.001 ***	< 0.001 ***	< 0.001 ***	0.0103 *
			F	F1,30 = 10.5	F1,24 = 27.52	F1,52 = 24.11	F1,29 = 15.31	F1,27 = 7.617
		Intrinsic water use efficiency	p value	0.005 **	< 0.001 ***	0.0001 ***	0.059	0.060
		(WUE)	F	F1,30 = 9.16	F1,24 = 27.52	F1,68 = 16.19	F1,29 = 3.88	F1,27= 3.868

Table 2 830 Main effect of water stress Acyrthosiph on pisum Sitobion avenae Rhopalosiphu m padi Myzus persicae Aphis nerii Macrosiphum euphobiae

 2

	Generation time (factorial	p value 0.251	0.004 **	0.19	0.026 *	0.575	< 0.001 ***
	ANOVA)	F	F1,18 = 1.41	F1,19 = 11	F1,39 = 1.77	F1,28 = 5.56	F1,29 = 0.32	F1,30 = 17.92
	Intrinsic rate of development	p value 0.4	0.320	0.010 *	0.047 *	0.134	< 0.001 ***
	(rm) (factorial ANOVA)	F	F1,18 = 0.75	F1,26 = 1.02	F1,43 = 7.16	F1,30 = 4.29	F1,29 = 2.381	F1,49 = 33.41
	Survival rate (Fisher's exact	p value 0.45	0.041*	0.013 *	451	1	< 0.001 ***
	test)

Table 6 :

 6 The difference between female ratio and emergence ratio of parasitoids testing on aphid species-treatment combinations in compare to

	host natal on optimal treatment; using multiple comparisons Fisher's exact tests. The asterisk means the probability of rejecting the null
	hypothesis below the threshold value (adjusted p value < .00455)
	χ²	An30	An100	M.p30	Mp70	Rp30	Rp100	Sa30	Sa100	Ap30	Me30	Me100
		vs.	vs.	vs.	vs.	vs.	vs.	vs.	vs.	vs.	vs.	vs.
		Ap100	Ap100	Ap100	Ap100	Ap100	Ap100	Ap100	Ap100	Ap100	Ap100	Ap100
	Emergence	0.00002*	0.00002*	0.00005*	0.0966	0***	0*** 0.00271* 0.18374	0.5282 0.00005*	0.02171
	ratio	**	**	**							**
	Female	0.00055*	0.00055*	0.00017*	0.30636 0.00001*	0.00001*	0.02497 0.28505 0.54669 0.00141* 0.03967
	ratio	*	*	*		**	**

Table 7 :

 7 Impacts of water stress on parasitoid offsprings parasitized six aphid species feeding on plants received under optimal water (OW) versus

	limited water irrigation (LW, 30% of optimal watering volume? N = 7-21). The asterisks indicate significant difference (p value < 0.05) between
	parasitoids on aphids feeding OW and LW plants (factorial ANOVA analysis).

Main effect of water stress on parasitoid offspring Aphidius ervi on Acyrthosiphon pisum A. ervi on Sitobion avenae A. ervi on Myzus persicae

		p value	F1,21	p value	F1,15	p value	F1,7
	Tibia length	0.0599	3.954	0.0557	0.303	0.00017***	52.56
	Glycogen content	0.417	0.687	0.058	4.213	0.0327*	7.054
	Fructose content	0.0131*	7.349	0.169	2.093	0.0688	4.615
	Sucrose content	0.0608	3.927	0.00304**	12.45	0.0319*	7.139
	Total sugar content	0.120	2.628	0.0292*	5.816	0 .0732	0.128

Table 9 .

 9 Aphid diet breadth and sub-guild 847

	Aphid classification	Sub-guild	Plant	Reference
		trophic:	host
		Senescenc	specialit
		e (Se) vs.	y:
		flush	specialist
		feeder (Fl)	(Sp) vs.
			generalis
			t (Ge)
	Myzus persicae	Se	Ge	Simpson 2012,
	Brevicoryne brassicae	Fl	Sp	van Emden and Harrington 2007
	Schizaphis graminum	Se	Sp	Sandstrom et al. 2000
	Rhopalosiphum padi	Se	Sp	White 2015
	Sitobion avenae	Fl	Sp	White 2015
	Acyrthosiphon pisum	Fl	Sp	van Emden and Harrington 2007
	Aphis nerii	Fl	Sp	Agrawal 2011, Hall and Ehler (1980)
	Macrosiphum	Fl	Ge	http://www.cabi.org/isc/datasheet/32
	euphorbiae			154

Table 5 .

 5 Articles on the subject: 'Impacts of abiotic stress on the tritrophic plant-aphidparasitoid system". Results were found from the database of Web of Science (c).

	Codes of

Table 6 .

 6 Lists of study using Aphidius ervi as biological models. The data were found with keyword "Aphidius ervi" in either titles, abstracts or keywords from the database of Web of Science ®.

	Subjects	Characteristics	References
	Aphid defenses	Immunity-based	Gwynn et al. 2005; Poirie and Coustau 2011
	from natural
	enemies

  ; Sidney et al. 2010; Host pathogens Ban et al. 2008; Baverstock et al. 2005 Host density Ives and Settle 1996; van Veen et al. 2005;

	Host phenotype	Losey et al. 1997;
	Host cues	Nakashima et al. 2016;
	Impacts of plants Plant symbionts

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Acknowledgments Acknowledgments

We thank Philippe Bearez and Christiane Metay-Merrien for technical assistance. This work was funded by the FP7-IRSES APHIWEB project.

Acknowledgement

The authors thank P. Bearez and I. Le Goff for technical assistance. This research was supported by a grant from the Marie-Curie F7-IRSES Action (project APHIWEB -611810) to ND, a Ph.D. fellowship from the French Ministry of Foreign Affairs to LTHN, and a Ph.D. fellowship from the Doctoral School Sciences de la Vie et de la Santé ED85 to LM.

director of my Ph.D., for his scientific expertise and his unconditional support during this study. My gratitude is to Dr. Gérard Blanc for his thorough reliability and Dr. Pascal Gantet (U. Montpellier) for giving me this opportunity. I am especially grateful to them. This Ph.D. thesis was supported by a fellowship from the French government and funds from the French National Institute for Agricultural Research and the FP7-IRSES APHIWEB project. I acknowledge this financial support.

Aphid species

Supplementary material 1. Endosymbiont targeted, the target gene, the primer name, the primer sequence (5'-3'), the expected product size (in bases), the temperature of melting (TM) and the references.

Target

Target

ABSTRACT

Shift in the ecological specialization of herbivorous and predatory species may occur through the indirect impact of abiotic stresses arising at lower trophic levels, e.g. in plants (effects so-called bottom-up effects). A tritrophic system "plant-aphid (sap-feeding herbivores) -parasitoid (Aphidius ervi, Hymenoptera: Braconidae: Aphidiinae)" was used as a biological model to study such potential shift in parasitoid host specificity owing to bottom-up impact; we measured possible effects on both behavioral and physiological parasitoid traits. It was investigated using six host plant-aphid complexes, and water limitation were used as abiotic stress inducing the bottom-up effect. Also, the impact of water stress on host plants and aphid life-history traits were assessed. We demonstrated that bottom-up effects effectively occurred on parasitoid host specificity and that it can modulate its actual host range. The parasitoid choosiness was not drastically affected by bottom-up effect while aphid host suitability for parasitoid offspring development was decreased in three out of the six aphid species tested. Besides, water stress negatively affected plant primary metabolism-related mechanisms, e.g. leaf transpiration rate and stomatal conductance, and it cascaded to aphids; their development speed and growth were decreased for half of aphid species considered. Adverse bottom-up effects observed on aphid hosts were linked to subsequent parasitoid performance on these hosts; except for one aphid species, those showing reduced survival, generation time and intrinsic rate of population increase (rm) proved to be suboptimal hosts for the parasitoid when plants were suffering water stress. This research highlights the potential impact of abiotic-related stress on actual host specificity in parasitoids.

Keywords: host specificity, preference-performance hypothesis, tritrophic interactions, water limitation, biological control, biological control agents

RESULTS

Impact of stress on plant morphological and metabolic traits:

Plant height, the number of nodes and leaf mass area (LMA) (Figure 1A,B,C) -Plant height was significantly reduced under water stress for all plants tested; still, the impact was not similar among plant species. Bean, milkweed, and potato showed severe height reduction by up to 34% (Figure 1A, p value < 0.001) whereas the height of wheat was slightly decreased (p value = 0.02). There was no evidence of the difference of cabbage height between OW and LW (p value > 0.05); however the number of cabbage leaves was significantly lower than in optimal water supplied plants which reduced by 23% under LW (p value = 0.007). There was no evidence water limitation impact on LMA of all plants (p value > .05) except wheat with LMA increased by 15% (p value = 0.013). Semiochemical compounds [START_REF] Rodriguez | Effect of innate preferences, conditioning and adult experience on the attraction of Aphidius ervi (Hymenoptera : Braconidae) toward plant volatiles[END_REF][START_REF] Sasso | Hostlocating response by the aphid parasitoid Aphidius ervi to tomato plant volatiles[END_REF][START_REF] Sasso | Electrophysiological and behavioural responses of Aphidius ervi (Hymenoptera: Braconidae) to tomato plant volatiles[END_REF][START_REF] Guerrieri | Induction and systemic release of herbivore-induced plant volatiles mediating in-flight orientation of Aphidius ervi[END_REF][START_REF] Powell | The Influence of Host Food Plants on Host Recognition by 4 Aphidiine Parasitoids (Hymenoptera, Braconidae)[END_REF]Takemoto, H. and

Leaf photosynthesis, conductance, transpiration rate and the intrinsic water use efficiency

Ecological interaction

Inter-guild competition [START_REF] George | Dichotomy of male and female responses to hoverfly-driven cues and floral competition in the parasitoid wasp Aphidius ervi Haliday[END_REF]Le Lann et al. 2011;Intra-guild competition Bribosia et al. 1995;McLean and Godfray 2016;[START_REF] Almohamad | Encounters with aphid predators or their residues impede searching and oviposition by the aphid parasitoid Aphidius ervi (Hymenoptera: Aphidiinae)[END_REF][START_REF] Baverstock | Intraguild interactions between the entomopathogenic fungus Pandora neoaphidis and an aphid predator and parasitoid at the population scale[END_REF][START_REF] Nakashima | Avoidance of ladybird trails by an aphid parasitoid Aphidius ervi: active period and effects of prior oviposition experience[END_REF][START_REF] Schellhorn | Competition between native and introduced parasitoids of aphids: Nontarget effects and biological control[END_REF][START_REF] Taylor | Effect of aphid predators on oviposition behavior of aphid parasitoids[END_REF][START_REF] Frago | Avoidance of intraguild predation leads to a longterm positive trait-mediated indirect effect in an insect community[END_REF][START_REF] Snyder | Interactions between specialist and generalist natural enemies: Parasitoids, predators, and pea aphid biocontrol[END_REF]Kraft et al. 2017;McLean, A. H. C. et al. 2017Apparent Frago 2016;[START_REF] Fan | Mechanisms for Stable Coexistence in an Insect Community[END_REF]McLean, A. H. C. and Godfray 2017;[START_REF] Meisner | Presence of an unsuitable host diminishes the competitive superiority of an insect parasitoid: a distraction effect[END_REF][START_REF] Morris | Field experiments testing for apparent competition between primary parasitoids mediated by secondary parasitoids[END_REF][START_REF] Pope | Apparent competition between two species of aphid via the fungal pathogen Erynia neoaphidis and its interaction with the aphid parasitoid Aphidius ervi[END_REF]Larval stage Sidney et al. 2010a Parasitoid natural enemies: hyperparasitoid Muller andGodfray 1998;[START_REF] Raworth | Primary and secondary parasitoids (Hymenoptera) of aphids (Hemiptera : Aphididae) on blueberry and other Vaccinium in the Pacific Northwest[END_REF][START_REF] Schooler | Hyperparasitoid aggregation in response to variation in Aphidius ervi host density at three spatial scales[END_REF][START_REF] Araj | Adding floral nectar resources to improve biological control: Potential pitfalls of the fourth trophic level[END_REF][START_REF] Mcmenemy | Biology of the European large raspberry aphid (Amphorophora idaei): its role in virus transmission and resistance breakdown in red raspberry[END_REF][START_REF] Noma | Hymenopteran parasitoids and dipteran predators of Diuraphis noxia in the west-central Great Plains of North America: Species records and geographic range[END_REF][START_REF] Schooler | The potential for hyperparasitism to compromise biological control: Why don't hyperparasitoids drive their primary parasitoid hosts extinct?[END_REF][START_REF] Volkl | Foraging behaviour, host plant and host location in the aphid hyperparasitoid Euneura augarus[END_REF]