Corentin Iltis
email: corentin.iltis@u-bourgogne.fr.

Jérôme Moreau

Corentin Manière

Denis Thiery

Lionel Delbac

Philippe Louapre

Denis Thiéry

Philippe Louâpre

Where you come from

Keywords: Host eggs, oophagous parasitoid, parental effects, temperature, trophic dynamics

come

Introduction

Host-parasitoid interactions modulate the composition of communities and the functioning of ecosystems in both natural and agricultural landscapes [START_REF] Godfray | Parasitoids: behavioral and evolutionary ecology[END_REF]. Parasitoids exert topdown control on the structure of food webs by regulating the abundance of phytophagous arthropods, while hosts in turn drastically constrain the size of parasitoid populations through bottom-up control [START_REF] Walker | Relative roles of top-down and bottom-up forces in terrestrial tritrophic plant-insect herbivore-natural enemy systems[END_REF][START_REF] Stireman | Climatic unpredictability and parasitism of caterpillars: implications of global warming[END_REF][START_REF] Thomson | Predicting the effects of climate change on natural enemies of agricultural pests[END_REF]. The strength of these top-down and bottom-up forces is governed by a set of biotic and abiotic factors, among which temperature is unequivocally recognised as a key determinant of hostparasitoid interactions [START_REF] Hance | Impact of extreme temperatures on parasitoids in a climate change perspective[END_REF][START_REF] Van Baaren | Consequences of climate change for aphidbased multi-trophic systems[END_REF][START_REF] Jeffs | Effects of climate warming on host-parasitoid interactions[END_REF].

Undeniably, the body temperature and performance of the host and the parasitoid depend on thermal variation among both latitudes and microhabitats [START_REF] Hance | Impact of extreme temperatures on parasitoids in a climate change perspective[END_REF][START_REF] Van Baaren | Consequences of climate change for aphidbased multi-trophic systems[END_REF]Furlong and Zalucki 2017). The thermal sensitivity of these two antagonistic partners makes host-parasitoid interactions likely to be disrupted by global warming [START_REF] Jeffs | Effects of climate warming on host-parasitoid interactions[END_REF]Furlong and Zalucki 2017). For instance, Furlong and Zalucki (2017) suggest that increasing global temperatures will produce a greater negative impact on parasitoid distributions, than on their hosts, due to their lower optimal temperature and narrower thermal tolerance range.

At the individual level, host suitabilitydefined as the accordance between a parasitoid's requirements to complete its development and a host's physiological, morphological and behavioural features (see [START_REF] Vinson | Host suitability for insect parasitoids[END_REF] is affected by temperature in several ways. First, temperature determines the amounts of several energetic compounds in the host, among them proteins, lipids, glycogen and free carbohydrates (Geister et al. 2009;[START_REF] Farahani | The effect of host nutritional quality on multiple components of Trichogramma brassicae fitness[END_REF][START_REF] Iltis | Are life-history traits equally affected by global warming? A case study combining a multi-trait approach with fine-grain climate modeling[END_REF]. Since a host is the sole source of nutrients for an immature parasitoid, this thermal variation in host nutritional quality in turn crucially impacts the development of parasitoids and several aspects of their fitness (e.g. longevity, fecundity) [START_REF] Farahani | The effect of host nutritional quality on multiple components of Trichogramma brassicae fitness[END_REF]). In addition, most parasitoids lack adult lipogenesis and are thus unable to synthesise fat reserves for survival and egg production, which strengthens their dependence on the nutritional resources obtained from their host during development [START_REF] Visser | Lack of lipogenesis in parasitoids: a review of physiological mechanisms and evolutionary implications[END_REF]. Second, temperature alters host immune functions (relying, mostly, on encapsulation and melanisation processes) that are aimed at killing parasitoids during their immature stages [START_REF] Seehausen | High temperature induces downregulation of polydnavirus gene transcription in lepidopteran host and enhances accumulation of host immunity gene transcripts[END_REF][START_REF] Iltis | When warmer means weaker: high temperatures reduce behavioural and immune defences of the larvae of a major grapevine pest[END_REF][START_REF] Iltis | Are life-history traits equally affected by global warming? A case study combining a multi-trait approach with fine-grain climate modeling[END_REF].

In this regard, high temperatures may in some cases stimulate the expression of host immunerelated genes with negative consequences for parasitoid survival until emergence. This is especially true if warming concomitantly decreases the ability of the parasitoid to suppress the host immune system, for instance by inducing downregulation of polydnavirus transcription [START_REF] Seehausen | High temperature induces downregulation of polydnavirus gene transcription in lepidopteran host and enhances accumulation of host immunity gene transcripts[END_REF]. In other cases, warmer conditions can elicit extensive weakening of the host's immunity, thereby enhancing host susceptibility to a parasitic attack [START_REF] Iltis | When warmer means weaker: high temperatures reduce behavioural and immune defences of the larvae of a major grapevine pest[END_REF].

Thermal modulation of host suitability can arise from direct effects, whereby ambient temperatures temporarily or permanently experienced by a single host individual during its lifetime might affect the host's immunity [START_REF] Iltis | When warmer means weaker: high temperatures reduce behavioural and immune defences of the larvae of a major grapevine pest[END_REF]) and the resulting interaction with parasitoid eggs or larvae [START_REF] Seehausen | High temperature induces downregulation of polydnavirus gene transcription in lepidopteran host and enhances accumulation of host immunity gene transcripts[END_REF]). These direct thermal effects are known to influence the outcomes of host-parasitoid interactions (e.g. host infestation rates, parasitoid development time and body mass on emergence, parasitoid emergence rates) [START_REF] Bahar | Constant versus fluctuating temperatures in the interactions between Plutella xylostella (Lepidoptera: Plutellidae) and its larval parasitoid Diadegma insulare (Hymenoptera: Ichneumonidae)[END_REF]Delava et al. 2016;[START_REF] Schreven | Contrasting effects of heat pulses on different trophic levels, an experiment with a herbivore-parasitoid model system[END_REF]. Besides direct effects, temperature can also indirectly shape host suitability through parental effects [START_REF] Sgrò | What can plasticity contribute to insect responses to climate change?[END_REF][START_REF] Woestmann | The importance of trans-generational effects in[END_REF]Donelson et al. 2018). Parental effects occur when conditions encountered by members of the parental generation influence the expression of a phenotype in the subsequent generation [START_REF] Sgrò | What can plasticity contribute to insect responses to climate change?[END_REF]Donelson et al. 2018). Indeed, environmental conditions experienced by a host parental generationsuch as temperature, host plant nutritional quality or immune challengehave demonstrated influence on a large variety of offspring traits related with their suitability for parasitoids (e.g. size, mass, amounts of energetic metabolites, immunity) (Geister et al. 2009;[START_REF] Janowitz | Opposing effects of heat stress on male versus female reproductive success in Bicyclus anynana butterflies[END_REF]Eggert et al. 2015;[START_REF] Trauer-Kizilelma | Impact of transgenerational immune priming on the defence of insect eggs against parasitism[END_REF][START_REF] Moreau | Larval food influences temporal oviposition and egg quality traits in females of Lobesia botrana[END_REF]. Beyond these effects at the individual level, to what extent such parental thermal effects might drive the dynamics of the host-parasitoid interaction remains unexplored, as does the relative importance of direct and parental effects for the outcomes of the interaction. From a global warming perspective, such a knowledge gap might limit our ability to forecast the impacts of rising temperatures for the future of host-parasitoid interactions. Indeed, this climatic disturbance will persist across generations and is therefore expected to affect species and interspecific relationships through direct and parental effects in a cumulative way [START_REF] Sgrò | What can plasticity contribute to insect responses to climate change?[END_REF]Donelson et al. 2018).

Here we investigated the consequences of direct and parental thermal effects for an interaction between host eggs and oophagous parasitoids. We developed an experimental design that allowed us to separate the relative impacts of: (i) parental thermal effects, through differences in temperatures experienced by a host parental generation from larval development to egg laying (i.e. parental temperature), and (ii) direct thermal effects, through differences in ambient temperatures at which host eggs were incubated following parasitism (i.e. offspring temperature). As an experimental imitation of global warming, we built two realistic, fluctuating regimes reflecting current and future thermal conditions in our focal area (Eastern France). We focused on the host-parasitoid complex constituted by eggs of one of the most harmful vineyard pests in the Palearctic region: the European grapevine moth Lobesia botrana (Lepidoptera: Tortricidae), as host for the oophagous parasitoid Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae) ̶ a candidate for the biological control of L. botrana populations [START_REF] Pizzol | Parasitoid and host egg ages have independent impact on various biological traits in a Trichogramma species[END_REF]Thiéry et al. 2018). Considering that parental effects are known to be a major source of variation in offspring quality traits, particularly in the early life stages like eggs (reviewed by Woestmann and Saastamoinen 2016), we hypothesised that host egg suitability for parasitoids should be influenced by parental temperature to a greater extent than offspring temperature. Specifically, we expected lower parasitoid emergence rates from host eggs originating from warm conditions, as a consequence of a low suitability of these eggs. Indeed, higher temperatures experienced by L. botrana parents during development should shorten the duration of their larval stage and reduce their food intake ̶ congruently with previous works conducted on this species (Iltis et al. 2018[START_REF] Iltis | Are life-history traits equally affected by global warming? A case study combining a multi-trait approach with fine-grain climate modeling[END_REF]. Lower larval food intake should, in turn, negatively affect parental investment in egg quality, because L. botrana adults are non-feeding and their reproductive output, along with egg quality traits, tightly hinges on resources accumulated as caterpillars [START_REF] Moreau | Grape variety affects larval performance and also female reproductive performance of the European grapevine moth Lobesia botrana (Lepidoptera: Tortricidae)[END_REF][START_REF] Moreau | Larval food influences temporal oviposition and egg quality traits in females of Lobesia botrana[END_REF].

Materials and methods

Thermal regimes

Thermal regimes used in this study reflected realistic current and future climatic conditions in Burgundy, Eastern France (Longvic-Dijon weather station, 47,27°N; 5,09°E; altitude = 219 m) (www.meteofrance.com). These regimes focused on the summer period, extending from 15-July to 15-Aug, because this date range is associated with high levels of activity for the host and the parasitoid in Eastern France, as shown by concomitant peaks of adult moth emergence and number of L. botrana eggs parasitised by T. cacoeciae [START_REF] Barnay | Survey of natural populations of Trichogramma (Hym., Trichogrammatidae) in the vineyards of Alsace (France)[END_REF].

The thermal regime designed to reflect conditions currently found in Burgundy, called the 'current regime', was generated according to 20-year recordings of in situ hourly temperatures (1995-2014 period). The current regime was compared with the 'future regime', describing the summer thermal conditions (15-July to 15-Aug) likely to occur in Burgundy by the end of this century (2081-2100 period). To design the future regime, we combined six General Circulation Models and six Regional Climate Models, selecting the most pessimistic greenhouse gas emissions scenario: RCP 8.5 (see Beaumont et al. 2008;[START_REF] Harris | Climate projections for ecologists[END_REF] for an in-depth description of the use of climate models in ecology). Data are available on the Drias portal (www.drias-climat.fr). Daily cycles constituting the current regime and the future regime were composed of six temperature segments, each lasting 4h and calculated (i) as the mean segment over the 30 days (15-July to 15-Aug) and the 20 years of in situ data for the current regime, or (ii) as the mean segment over the six simulations run for the future regime (Fig. 1). Compared with the current regime, the future regime shows an increase in mean temperature of 5.3°C (25.8°C for the future regime versus 20.5°C for the current regime) and an increase in thermal range (the difference between maximum and minimum daily temperatures) of 0.6°C (5.6°C for the future regime versus 5.0°C for the current regime) (Fig. 1).

Moth maintenance and host egg production

All L. botrana individuals used in this experiment belonged to a laboratory, diapause-free population maintained at the French National Institute for Agricultural Research (INRA, Villenave d'Ornon, France). This large stock was comprised of several thousand adults per week, and was regularly supplemented with wild individuals collected from nearby vineyards (cultivar Sémillon) to preserve genetic diversity [START_REF] Vogelweith | Defense strategies used by two sympatric vineyard moth pests[END_REF]. Moths were reared in a large cage at 20 ± 0.5°C, 60 ± 5% relative humidity, under a light cycle of L17: D6 with one hour of dusk. Luminosity reached 650 lx during photophase and fell to 100 lx at dusk. Two bands of waxed paper (5 x 10 cm) were hung inside the cage for egg laying. Every 3 days, these oviposition supports were renewed and transferred into plastic boxes covered by a moist piece of paper towel to protect eggs from desiccation until hatching.

Over two months, a total of 5520 freshly hatched larvae (age < 24h) were collected with a fine brush and isolated in Eppendorf tubes filled with 1.5 ml of artificial medium that is typically used for the laboratory rearing of this species (composition for 1000 ml: 1000 ml water, 15 g agar, 86.6 g maize flour, 41.3 g wheat germ, 45.5 g beer yeast, 6 g ascorbic acid, 3.4 g mineral salt, 0.32 g Scala, 2.7 g benzoic acid, 2.8 g Nipagin and 5 ml 95% ethanol) [START_REF] Thiéry | Relative performance of European grapevine moth (Lobesia botrana) on grapes and other hosts[END_REF][START_REF] Muller | Direct benefits from choosing a virgin male in the European grapevine moth, Lobesia botrana[END_REF][START_REF] Iltis | When warmer means weaker: high temperatures reduce behavioural and immune defences of the larvae of a major grapevine pest[END_REF]. Individual rearing in Eppendorf tubes avoided larval competition and subsequent food deprivation [START_REF] Thiéry | Larval intraspecific competition for food in the European grapevine moth Lobesia botrana[END_REF]). Tube caps were drilled for air circulation and covered with a piece of fine mesh fabric to prevent larvae from escaping. Individuals were randomly assigned to four incubators (ST 2/2 BASIC, Pol-Eko Aparatura, Wodzisław Śląski, Poland), two of which being programmed to run the current regime and the other two to run the future regime (temperature ± 0.1°C, 50 ± 10% relative humidity, L18: D6, 650 lx). Twice a week, larvae from a given thermal regime were switched between the two climate chambers running this regime, as well as the relative locations of individuals inside these chambers. Temperatures inside the devices were recorded by independent data loggers (Hobo, Onset Computer Corporation, Bourne, USA) and conformed to the thermal regimes programmed during the whole course of the experiments.

To limit disturbance, larval viability and pupation were monitored only when swapping rearing tubes between incubators (i.e. twice a week).

Within 3 or 4 days following pupation, chrysalises were carefully extracted from their silk cocoons with fine forceps and weighed to the nearest 0.1 mg with a balance (Pioneer PA214C, OHAUS, Greifensee, Switzerland). Chrysalises were subsequently isolated in clean glass tubes (70 x 9 mm diameter) closed by cotton plugs before being returned to their rearing thermal regime. They were checked daily for imaginal emergence. Moths were sexed upon emergence and were supplied daily with water ad libitum through soaked cotton plugs. At dusk, one 24-48h virgin female was randomly placed for one night in a clean glass mating tube (100 x 15 mm diameter) with one 24-72h virgin male originating from the same thermal regime. We restricted the age ranges of sexual partners, and only used virgin individuals because age and mating history are known to affect several traits in this species that influence egg quality (e.g. spermatophore volume, number of eggs laid, egg size) [START_REF] Moreau | Grape variety affects larval performance and also female reproductive performance of the European grapevine moth Lobesia botrana (Lepidoptera: Tortricidae)[END_REF][START_REF] Muller | Direct benefits from choosing a virgin male in the European grapevine moth, Lobesia botrana[END_REF]. Males were removed the following morning to avoid multiple mating, and were no longer used for the experiments. Females were allowed to oviposit freely in their mating tube closed by a daily soaked cotton plug as a water supply. Mating and egg laying occurred within the thermal regime from which the pair originated.

The number of eggs laid by females was recorded every morning via visual inspection.

Only mating tubes containing at least 30 eggs laid within 12h (i.e. during one single night) were used for parasitism tests. A lower limit of 30 eggs was set to ensure that host egg number was not a limiting factor for the parasitoid during parasitism tests and to reduce variation in host egg density. For the purpose of standardisation, host egg age was restricted to 12h or less because it might affect the outcomes of interactions with T. cacoeciae (e.g. number of eggs parasitised, parasitoid emergence rates) [START_REF] Moreno | Effects of Lobesia botrana (Lepidoptera: Tortricidae) egg age, density, and UV treatment on parasitism and development of Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae)[END_REF][START_REF] Pizzol | Parasitoid and host egg ages have independent impact on various biological traits in a Trichogramma species[END_REF]). In addition, using such freshly laid host eggs is appropriate to investigate parental thermal effects, because these eggs have been exposed to environmental conditions for a very short duration before parasitism tests. Hence, variation in their suitability for parasitoids should be importantly driven by parental effects. This selection procedure retained 512 mating tubes out of a total of 734 tubes, which represents 98% of the 523 tubes with eggs found inside. This high percentage can be explained by the fact that L. botrana females usually lay the largest amounts of eggs at the beginning of their oviposition period, especially during the first night succeeding to mating [START_REF] Moreau | Larval food influences temporal oviposition and egg quality traits in females of Lobesia botrana[END_REF]. Lobesia botrana females were then removed and the tubes of freshly laid eggs were photographed using a stereomicroscope at 8x magnification (Stemi 508, Zeiss, Göttingen, Germany). For each tube, one picture including five eggs on the same horizontal plane was taken to reliably estimate mean egg size (surface area) within the clutch [START_REF] Moreau | Larval food influences temporal oviposition and egg quality traits in females of Lobesia botrana[END_REF]. We then randomly selected 123 pictures (n = 57 for the current regime, n = 66 for the future regime) and assessed the surface area of five eggs for each picture (estimated as an elliptic surface, 𝑆 = 𝜋 × 𝑎 × 𝑏 in mm², where a and b are the ellipse semi-axes) with a precision of ± 0.001 mm². The photographic data were analysed with ImageJ software (version 1.51j8, National Institutes of Health, Bethesda, USA).

Parasitoid maintenance and parasitism procedure

Experimental lines of T. cacoeciae involved in this study were all thelytokous, and therefore only constituted by females. We ran one single experiment using parasitoids belonging to four different strains in order to generalise our conclusions about the thermal modulation of host egg suitability to a generic parasitoid pressure. Hence, parasitoid strain was included as a treatment (involving four levels) in the experiment. These four strains were derived from field populations collected in June 2017 at four French localities: Aime (45,33°N; 6,39°E), Banyuls-sur-Mer (42,45°N; 3,09°E), Le Crouzet (44,38°N; 3,63°E) and Sophia Antipolis (43,61°N; 7,08°E). These sites were chosen because they are distant enough from each other to avoid any confounding genetic effect, given the relatively low dispersal abilities of Trichogramma species (Fournier and Boivin 2000). Wild populations were initially sampled on Rosa sp. and Prunus sp. with baits comprised of cards covered with ultraviolet sterilised eggs of the Mediterranean flour moth Ephestia kuehniella (age < 5 days) as a substitute host.

Parasitoids emerging from these baits were first identified as T. cacoeciae individuals based on molecular analyses involving PCR amplification of a microsatellite marker [START_REF] Pizzol | A single molecular marker to distinguish between strains of Trichogramma cacoeciae[END_REF], and then used to establish laboratory colonies. Until the start of the experiments (i.e. over 9 months), they were reared in plastic culture tubes plugged with cotton (10 x 1 cm diameter) under controlled common conditions (23.1 ± 0.5°C, 60 ± 5% relative humidity, photophase of L18: D6, 650 lx). One piece of cardboard (1 x 6 cm) covered with ultraviolet sterilised eggs of E. kuehniella (age < 5 days) was provided for parasitoid multiplication.

After 4 days of exposure, the cardboard pieces were transferred to clean rearing tubes for parasitoid emergence. A droplet of honey was deposited into each rearing tube to feed emerged adults. Prior to our parasitism tests, individuals originating from the four collected strains were genetically identified to ensure that no contamination had occurred within each strain [START_REF] Pizzol | A single molecular marker to distinguish between strains of Trichogramma cacoeciae[END_REF]).

Only T. cacoeciae females, less than 24h old, were picked for the experiments. These females had not parasitised any host eggs before their contact with L. botrana eggs during the parasitism tests. Parasitoid age was restricted (< 24h) to standardise its effects on the total number of host eggs parasitised [START_REF] Pizzol | Parasitoid and host egg ages have independent impact on various biological traits in a Trichogramma species[END_REF]. Tubes of freshly emerged parasitoids were gently tapped until T. cacoeciae females fell from the tubes. A tube of host eggs was then inversely placed over the parasitoid until it climbed the walls of the tube. We only selected actively moving parasitoids tipped from their rearing tubes to make sure their physical integrity had not been altered during manipulation. To avoid any confusion, T. cacoeciae females used to parasitise L. botrana eggs will be referred to as 'mothers' and those that emerged from these eggs will be called 'daughters'.

Each day, host egg tubes originating from each thermal regime were equally distributed among T. cacoeciae strains to ensure temporal randomisation. Parasitism tests were conducted under a common temperature of 23.1°C (± 0.5°C, 60 ± 5% relative humidity, 650 lx) to standardise the effect of ambient temperature on parasitoid behaviour, and also because 23.1°C is the rearing temperature of parasitoids as well as the intermediate temperature from which host egg tubes originated: between the mean temperatures of the current regime (20.5°C) and the future regime (25.8°C). Parasitoid mothers were introduced inside host egg tubes at 9:00 AM and delicately removed with a fine brush at 3:00 PM.

Exposure duration was set at 6h to ensure parasitism was not limited by the number of host eggs available and to avoid superparasitism. Indeed, more than 6h should be needed for one T. cacoeciae female to parasitise at least 30 eggs of L. botrana under the controlled conditions at which parasitism occurred [START_REF] Moreno | Effects of Lobesia botrana (Lepidoptera: Tortricidae) egg age, density, and UV treatment on parasitism and development of Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae)[END_REF]. No food or water was supplied to parasitoid mothers during the experiments. After their removal from host egg tubes, T. cacoeciae mothers were placed individually in clean Eppendorf tubes until their death. Using a stereomicroscope at 100x magnification (Stemi 508, Zeiss, Göttingen, Germany), we then measured the length of their left hind tibia as an estimation of body size (precision ± 0.1 µm) ̶ following the standard procedure described by [START_REF] Olson | Larval crowding and adult nutrition effects on longevity and fecundity of female Trichogramma nubilale Ertle & Davis (Hymenoptera: Trichogrammatidae)[END_REF]. These measurements were taken to control for an effect of the body size of parasitoid mothers on the number of host eggs parasitised, the percentage of parasitoid emergence, and the hind tibia length of parasitoid daughters that emerged from parasitised eggs. Out of an initial 512 tubes, 12 tubes were removed from the dataset because the preservation state of the T. cacoeciae mothers used to parasitise these tubes did not permit reliable measurements of hind tibia length.

Host egg incubation and data acquisition

Once parasitoid mothers were removed, host egg tubes were randomly incubated in either the current or the future regime (i.e. independently of the thermal regime they came from). This resulted in four combinations of thermal regimes (current/current, current/future, future/current, future/future), each combination being defined by one 'parental temperature' (regime within which host development, reproduction and egg laying occurred) and one 'offspring temperature' (regime within which host eggs were incubated following exposure to parasitoids). Each day, tubes of parasitised eggs were equally distributed between the two offspring temperatures for temporal randomisation. Incubation lasted 28 days before tube inspection. This duration was sufficient to enable the complete development of the host (hatching of L. botrana larvae from unparasitised eggs) and the parasitoid (emergence of T. cacoeciae daughters from parasitised eggs) until death [START_REF] Moreau | Host plant cultivar of the grapevine moth Lobesia botrana affects the life history traits of an egg parasitoid[END_REF][START_REF] Moreno | Effects of Lobesia botrana (Lepidoptera: Tortricidae) egg age, density, and UV treatment on parasitism and development of Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae)[END_REF]. No cannibalism of parasitised eggs by newly hatched L. botrana caterpillars was observed. No parasitoid diapause was expected to occur under the environmental conditionsespecially temperature and photoperiodencountered by T. cacoeciae mothers and daughters during parasitism tests and post-parasitism incubation, respectively [START_REF] Pizzol | Effect of photoperiod experienced by parents on diapause induction in Trichogramma cacoeciae[END_REF].

After the incubation period, tubes were analysed under a stereomicroscope (Stemi 508, Zeiss, Göttingen, Germany) to record (i) the 'first-day fecundity' of the host (total number of eggs laid by one L. botrana female during one single night), (ii) the 'apparent parasitism success' of the parasitoid mother (number of host eggs parasitised) and (iii) the 'apparent emergence success' of parasitoid daughters (percentage of host eggs parasitised from which an adult T. cacoeciae successfully emerged) [START_REF] Moreau | Host plant cultivar of the grapevine moth Lobesia botrana affects the life history traits of an egg parasitoid[END_REF]. For determination of apparent parasitism success, we considered an egg as parasitised when it turned from white to grey, given that such a change in colouration is widely acknowledged as a reliable indicator of parasitism by Trichogramma species [START_REF] Hutchison | Morphology and biology of Trichogrammatoidea bactrae (Hymenoptera: Trichogrammatidae), imported from Australia as a parasitoid of pink bollworm (Lepidoptera: Gelechiidae) eggs[END_REF]) and because this criterion has been employed in previous studies that used L. botrana eggs as hosts for Trichogramma species [START_REF] Moreau | Host plant cultivar of the grapevine moth Lobesia botrana affects the life history traits of an egg parasitoid[END_REF][START_REF] Pizzol | Parasitoid and host egg ages have independent impact on various biological traits in a Trichogramma species[END_REF][START_REF] Thiéry | Host plants of the polyphagous grape berry moth Lobesia botrana during larval stage modulate moth egg quality and subsequent parasitism by the parasitoid Trichogramma cacoeciae[END_REF]. Provided that blackening of the parasitised host eggs occurs at the time of parasitoid pupation [START_REF] Hutchison | Morphology and biology of Trichogrammatoidea bactrae (Hymenoptera: Trichogrammatidae), imported from Australia as a parasitoid of pink bollworm (Lepidoptera: Gelechiidae) eggs[END_REF]), our metrics did not include cases where parasitoids died before the pupal stage, and therefore provide information about the 'apparent' rather than the 'realised' parasitism of the host eggs. Apparent parasitism success was not expressed in percentages because host eggs were provided ad libitum to T. cacoeciae mothers during parasitism tests [START_REF] Moreau | Host plant cultivar of the grapevine moth Lobesia botrana affects the life history traits of an egg parasitoid[END_REF]. For determination of apparent emergence success, we considered that the parasitoid daughter successfully emerged from the parasitised host egg when the blackened egg was found empty with an emergence hole on its surface. Hence, the difference between apparent parasitism success and apparent emergence success was that the former included all cases of apparent parasitism (all blackened eggs, with or without parasitoid emergence), whereas the latter only considered those that led to the emergence of the parasitoid daughter from the host egg (empty blackened eggs with an emergence hole on their surface). Sterile host clutches (28 tubes out of a total of 500 tubes) were discarded because they were laid by unmated L. botrana females and were therefore not subject to similar paternal effects as clutches resulting from successful mating. Host clutches were deemed sterile if no caterpillars emerged from the eggs. Tubes with no parasitised eggs found after exposure to a parasitoid mother (n = 5 for current/current, n = 2 for current/future, n = 1 for future/current, n = 4 for future/future) were conserved for statistical analysis focused on apparent parasitism success as no dead parasitoid mother had been observed after the 6h of parasitism. Dead parasitoid daughters were carefully collected with a fine brush, and observed under a stereomicroscope at 100x magnification (Stemi 508, Zeiss, Göttingen, Germany) to measure the length of their left hind tibia with the same method used for mothers. As an estimation of body size, hind tibia length is positively correlated with a female's longevity and lifetime fecundity in Trichogramma species and can therefore be interpreted as a surrogate for individual performance (Doyon and Boivin 2005).

The number of T. cacoeciae daughters extracted from each tube varied between zero and five, dependent on the number of daughters that had emerged from host eggs and their preservation state. Following the above selection procedure, 472 tubes were finally inspected (n = 124 for current/current, n = 122 for current/future, n = 108 for future/current, n = 118 for future/future), and hind tibia length measurements were taken from 826 parasitoid daughters collected from 373 tubes (n = 96 for current/current, n = 107 for current/future, n = 89 for future/current, n = 81 for future/future), equally distributed across the four parasitoid strains.

Statistical analyses

This study was based on a 2x2x4 full-factorial design involving three factors: 'parental temperature' (two levels), 'offspring temperature' (two levels) and 'parasitoid strain' (four levels). The pupal mass of individuals of the L. botrana parental generation (i.e. parents which produced the host eggs) was studied with an Analysis of Variance (ANOVA) incorporating temperature experienced by this generation, sex and the interaction between these two explanatory variables. Egg surface area and first-day fecundity of the host (L. botrana) were analysed with statistical models that included parental temperature as an explanatory variable, and female and male pupal mass as two covariates. For host egg surface area, an Analysis of Covariance (ANCOVA) with mixed effects was performed to account for the random effect represented by the identity of each L. botrana female and male. The data for first-day fecundity of the host did not satisfy the assumption of homoscedasticity and were therefore compared between parental thermal regimes using a Generalised Linear Model (GLM)-negative binomial error with a log link function.

For apparent parasitism success, apparent emergence success and hind tibia length of parasitoid daughters, three covariates were included in the models (pupal mass of L. botrana female and male, hind tibia length of T. cacoeciae mother). As no transformation enabled to reach normality for these discrete data, apparent parasitism success was analysed using a Generalised Linear Mixed Model (GLMM)-negative binomial error with a log link function, incorporating host parental temperature as a fixed effect and parasitoid strain as a random effect. For apparent emergence success, data were expressed in proportions and a GLMMbinomial error with a logit link function was performed to assess the fixed effects of host parental temperature, host offspring temperature and their interaction while accounting for parasitoid strain as a random effect. Lastly, variation in hind tibia length of parasitoid daughters was analysed by means of an ANCOVA with mixed effects, including host parental temperature, host offspring temperature and their interaction as fixed effects; and the identity of L. botrana female, male, parasitoid mother and parasitoid strain as random effects.

For all statistical analyses conducted, the best statistical model was selected following a stepwise backward procedure from initial models that included all simple fixed effects and their interactions. Normality and homoscedasticity were evaluated with a Shapiro-Wilk and Bartlett test, respectively. Post-hoc tests based on contrasts among the least square means were conducted to tease out significant differences. A Bonferroni correction was applied to prevent Type I errors. All statistical analyses were carried out using R software (version 3.6.1, R Development Core Team).

Results

Pupal mass, egg surface area and first-day fecundity of L. botrana host

The pupal mass of individuals from the L. botrana parental generation was influenced by the interaction between rearing temperature and sex (F1,940 = 9.11, P < 0.001). In females, the pupal mass was negatively impacted by rearing temperature: individuals that developed in the future, warmer regime were significantly lighter than those originating from the current, cooler regime. Mean values of females' pupal mass were 13.6 mg for the current regime (95% confidence interval CI95% = [13.4; 13.8], n = 246) and 13.1 mg for the future regime (CI95% = [12.9; 13.3], n = 226). In males, the pupal mass was not significantly affected by rearing temperature. Mean values of males' pupal mass were 9.4 mg for the current regime (CI95% = [9.3; 9.5], n = 246) and 9.3 mg for the future regime (CI95% = [9.2; 9.5], n = 226). The surface area of L. botrana eggs was not significantly affected by parental temperature (𝜒 1 2 = 3.45, P = 0.06). Eggs originating from the current regime had a mean surface area of 0.403 mm² (CI95% = [0.399; 0.407], n = 57) and those originating from the future regime had a mean surface area of 0.411 mm² (CI95% = [0.407; 0.415], n = 66). The first-day fecundity of L. botrana females the higher the apparent emergence success of parasitoid daughters from these eggs. As a random effect, parasitoid strain significantly affected apparent emergence success (𝜒 1 2 = 5.16,

P = 0.02).
The hind tibia length of T. cacoeciae daughters that emerged from parasitised L.

botrana eggs was impacted by host parental temperature (𝜒 1 2 = 8.55, P < 0.001), but not by host offspring temperature (𝜒 1 2 = 0.40, P = 0.53) or by the interaction between these two factors (𝜒 1 2 = 0.02, P = 0.89). Larger parasitoid daughters emerged from host eggs originating from the future regime in comparison with host eggs laid in the current regime (Fig. 3). None of the three covariates included in the model (pupal mass of L. botrana female and male, hind tibia length of T. cacoeciae mother) significantly affected the hind tibia length of parasitoid daughters. As a random effect, parasitoid strain significantly affected the hind tibia length of T. cacoeciae daughters (𝜒 1 2 = 61.7, P < 0.001).

Discussion

The purpose of this work was to assess the relative importance of parental and direct thermal effects in determining the outcomes of the interaction between eggs of the European grapevine moth L. botrana and the oophagous parasitoid T. cacoeciae. Our most striking result was the considerable effect of host parental temperature, that is, temperature experienced by host parental generation, on parasitoid apparent emergence success and hind tibia length on emergence. Trichogramma cacoeciae experienced lower emergence rates, but displayed higher hind tibia length on emergence, from host eggs originating from warm conditions (laid in the future regime) compared with eggs produced under cold conditions (laid in the current regime). By contrast with parental effects, direct thermal effects did not perceptibly modulate the outcomes of the host-parasitoid interaction. These findings match our initial expectation that the interaction between freshly laid host eggs and an oophagous parasitoid should be primarily determined by indirect, parental effects. Our results emphasise the importance of accounting for such parental thermal effects with the aim to predict the future of trophic dynamics under global warming scenario. Interestingly, the modulation exerted by host parental temperature on the outcomes of the interaction was consistent over the four parasitoid strains included in the study, even if each strain displayed its own characteristics in terms of performance when parasitising L. botrana eggs (e.g. apparent parasitism and emergence success, hind tibia length of emerged parasitoid daughters). From an evolutionary perspective, this raises the question as to whether natural populations of T.

cacoeciae experiencing a set of contrasting ecological conditions might respond in different ways to a rise in mean temperature, that is, whether parasitoid thermal adaptation may shape the evolutionary trajectory of the interaction in the context of climate change.

Two non-mutually exclusive hypotheses might account for the effects of host parental temperature on parasitoid apparent emergence success and hind tibia length on emergence.

First, parasitoids are constrained by the limited amount of food contained in their single host, and might fail to complete their development if host eggs laid in the future regime provide an insufficient quantity or quality of nutritional resources (i.e. resource-based hypothesis) [START_REF] Farahani | The effect of host nutritional quality on multiple components of Trichogramma brassicae fitness[END_REF]. Whether this hypothesis is fully relevant to explain our results remains questionable, provided that we did not observe any effect of parental temperature on L. botrana egg surface area as a surrogate of host nutritional quality for the parasitoid. In addition, the resource-based hypothesis poorly explains differences regarding the hind tibia length of emerged parasitoids observed. Indeed, host eggs of low nutritional quality should produce smaller adult parasitoids [START_REF] Farahani | The effect of host nutritional quality on multiple components of Trichogramma brassicae fitness[END_REF]), while we instead observed a higher hind tibia length of T. cacoeciae daughters emerging from host eggs produced in warm conditions. As a next step, biochemical assays of the quantities of several energetic metabolites eggs are provisioned with (e.g. proteins, lipids, glycogen, soluble carbohydrates) would be needed to assess more thoroughly the plausibility of this resource-based explanatory hypothesis (Geister et al. 2009).

A second hypothesis, positing differences in egg immunity (i.e. immunity-based hypothesis), can be formulated to explain the importance of host parental temperature for the host-parasitoid relationship. There is a growing body of evidence showing that eggs of lepidopteran hosts are able to mount an immune response to fend off a myriad of invaders, and the efficiency of this endogenous immune barrier is an integral component of their suitability for parasitoids [START_REF] Hilker | Innate immunity: eggs of Manduca sexta are able to respond to parasitism by Trichogramma evanescens[END_REF][START_REF] Trauer-Kizilelma | Impact of transgenerational immune priming on the defence of insect eggs against parasitism[END_REF].

Host immune defences against parasitism are modulated by parental experience [START_REF] Triggs | Parental diet has strong transgenerational effects on offspring immunity[END_REF][START_REF] Trauer-Kizilelma | Impact of transgenerational immune priming on the defence of insect eggs against parasitism[END_REF], including parental exposure to a brief thermal stress (cold snap or heat spike) (Eggert et al. 2015). In our study, L. botrana parents might have faced daily stressful thermal conditions in the future regimewhich included temperatures up to 30.5°C for 4hwhile a decline in the performance of caterpillars of this species has been pointed out at temperatures exceeding 25°C [START_REF] Iltis | When warmer means weaker: high temperatures reduce behavioural and immune defences of the larvae of a major grapevine pest[END_REF][START_REF] Iltis | Are life-history traits equally affected by global warming? A case study combining a multi-trait approach with fine-grain climate modeling[END_REF]. Such temporarily stressful temperatures met by the host parental generation might have promoted egg immunological defences, and could be potentially responsible for the negative effects of host parental temperature on parasitoid apparent emergence success. With respect to this immunity-based hypothesis, the proximate cause of the positive effect of host parental temperature on T. cacoeciae hind tibia length remains unknown at this stage. The reason could, for instance, involve a selective pressure exerted by the high immunity of eggs laid in warm conditions acting in favour of the largest parasitoid individuals. Such a phenomenon might occur if the efficiency of host encapsulation and melanisation processes decreases as the size of the foreign body to be encapsulated increases [START_REF] Pomfret | Immunity and the expression of a secondary sexual trait in a horned beetle[END_REF]. Hence, the largest parasitoid individuals could be more prone to survive the immune reaction expressed by their host. Considering that host egg immunity should operate during the first steps of the parasitism process, that is, acting on the early-life stages of Trichogramma parasitoids [START_REF] Hilker | Innate immunity: eggs of Manduca sexta are able to respond to parasitism by Trichogramma evanescens[END_REF][START_REF] Trauer-Kizilelma | Impact of transgenerational immune priming on the defence of insect eggs against parasitism[END_REF], one way to test the immunity-based hypothesis may consist of investigating the effects of host parental temperature on the early mortality of the parasitoid, before the blackening of the parasitised host eggs occurring at the time of parasitoid pupation [START_REF] Hutchison | Morphology and biology of Trichogrammatoidea bactrae (Hymenoptera: Trichogrammatidae), imported from Australia as a parasitoid of pink bollworm (Lepidoptera: Gelechiidae) eggs[END_REF]. If this hypothesis is valid, a higher percentage of dead parasitoid eggs and larvae should be expected from host eggs originating from warm conditions compared with host eggs laid in cold conditions.

By contrast with parental thermal effects, direct thermal effects did not contribute to modulate the outcomes of the host-parasitoid interaction measured. In our study, host eggs were exposed to parasitoids shortly after being laid by L. botrana females (within 12h).

Hence, these freshly laid eggs experienced the direct thermal effects occurring before parasitism for a very short duration, which could mitigate the importance of these direct thermal effects in influencing egg suitability for the parasitoid. It would be worth investigating whether the absence of direct thermal effects would persist using host eggs older than 12h. This is especially relevant considering that temperature primarily mediates embryonic development in insects [START_REF] Howe | Temperature effects on embryonic development in insects[END_REF], and that the egg developmental stage in turn impacts most egg traits related with their susceptibility to Trichogramma parasitoids. For instance, the egg nutritional resources are progressively consumed for embryonic growth in a temperature-dependent manner (Geister et al. 2009), hence direct thermal effects acting prior to parasitism may influence the amounts of reserves available for parasitoid development.

Furthermore, in lepidopteran host eggs, the mechanisms underlying the host immune reaction to parasitoid attack could differ depending on the stage of host embryonic development. Host eggs at an early stage of embryogenesis presumably lack an immediately functional immune system [START_REF] Strand | Immunological basis for compatibility in parasitoid-host relationships[END_REF] and seem to rely on the upregulation of immune-related genes as an inducible response triggered by parasitoid oviposition (Abdel-latief and Hilker 2008).

However, host eggs at a more advanced developmental stage could acquire an operating immune system through the appearance of immune cells involved in encapsulation and melanisation of parasitoid eggs [START_REF] Nardi | Embryonic origins of the two main classes of hemocytes -granular cells and plasmatocytes -in Manduca sexta[END_REF]. Thus, the nature and possibly the efficiency of the immune barrier mounted by the eggs against parasitic infection could depend on the modulation of the egg development by temperatures encountered prior to parasitism.

In summary, our study lends support to the hypothesis that temperatures experienced by a host parental generation affect the outcomes of a host-parasitoid interaction through parental thermal effects, regardless of the temperature at which the host-parasitoid complex was incubated (i.e. direct thermal effects). Transgenerational plasticity should play a major role in ensuring the local persistence of species in face of global warming [START_REF] Sgrò | What can plasticity contribute to insect responses to climate change?[END_REF]Donelson et al. 2018). However, species do not respond in isolation to climate disturbance, as they tightly depend on each other through ecological linkages, particularly in cases of obligate associations such as host-parasitoid trophic relationships [START_REF] Jeffs | Effects of climate warming on host-parasitoid interactions[END_REF]. In this regard, our study is the first to demonstrate that parental thermal effects might influence during summer (15-July to 15-Aug) over recent period (1995)(1996)(1997)(1998)(1999)(2000)(2001)(2002)(2003)(2004)(2005)(2006)(2007)(2008)(2009)(2010)(2011)(2012)(2013)(2014). The future regime forecasts the summer thermal conditions that might be observed in Burgundy by the end of the century (2081-2100), positing massive and growing future emissions of greenhouse gas.

This regime is based on the predictions given by six combinations of climate models.

Figure legends Figure 1

 legends1 Figure legends

Figure 2

 2 Figure 2 Effects of the combination of host parental temperature (thermal regime within

Figure 3

 3 Figure 3 Effects of the combination of host parental temperature (thermal regime within

Figure 1 Figure 2 Figure 3

 123 Figure1

Acknowledgements

We are grateful to thank Géraldine Groussier for providing the parasitoid strains used in the experiments, Sébastien Zito and Benjamin Bois for providing the climatic data. We acknowledge the valuable contribution of Alexandre Bauer, Aude Balourdet, Hugo Baali, Léa

was positively impacted by their rearing temperature (𝜒 1 2 = 36.4, P < 0.001). Females reared in the future regime produced 19% more eggs within 12h than females reared in the current regime. Mean values of first-day fecundity were 63 eggs for females reared in the current regime (CI95% = [60; 65], n = 246) and 75 eggs for females which developed in the future regime (CI95% = [71; 78], n = 226). Only first-day fecundity was affected by the covariates included in the models and this relationship was positive: it increased with female pupal mass (𝜒 1 2 = 6.31, P = 0.01, slope = 0.03) and male pupal mass (𝜒 1 2 = 4.27, P = 0.04, slope = 0.03).

Apparent parasitism success, apparent emergence success and hind tibia length of parasitoid daughters Apparent parasitism success was not significantly affected by host parental temperature (𝜒 1 2 = 0.28, P = 0.60). Among the three covariates included in the model (pupal mass of L. botrana female and male, hind tibia length of T. cacoeciae mother), apparent parasitism success was only positively influenced by the hind tibia length of T. cacoeciae mother (𝜒 1 2 = 9.80, P < 0.001, slope = 0.01): the largest mothers parasitised significantly more eggs over 6 hours than the smallest ones. As a random effect, parasitoid strain significantly affected apparent parasitism success (𝜒 2 2 = 17.8, P < 0.001).

Apparent emergence success was modulated by host parental temperature (𝜒 1 2 = 9.44, P < 0.001), but not by host offspring temperature (𝜒 1 2 = 0.39, P = 0.53) or by the interaction between these two factors (𝜒 1 2 = 2.62, P = 0.11). A lower percentage of parasitoid daughters emerged from host eggs originating from the future regime compared with host eggs coming from the current regime (Fig. 2). Among the three covariates included in the model (pupal mass of L. botrana female and male, hind tibia length of T. cacoeciae mother), apparent emergence success was only positively influenced by the pupal mass of L. botrana female (𝜒 1 2 = 40.0, P < 0.001, slope = 0.47): the heavier the L. botrana female that laid the host eggs,

Compliance with ethical standards

Conflict of interest: The authors declare they have no conflict of interest.

Ethical approval: All applicable institutional and/or national guidelines for the care and use of animals were followed.

Data availability: Data will be made publicly available at Dryad once the paper accepted.

Lepidoptera. Curr Zool 62:489-499 . doi: 10.1093/cz/zow029 687