Myriam Valero

Marie-Laure Guillemin

Christophe Destombe

Bertrand Jacquemin

Claire M M Gachon

Yacine Badis

Alejandro H Buschmann

Carolina Camus

Sylvain Faugeron

Perspectives on domestication research for sustainable seaweed aquaculture

Keywords: Domestication, interaction, coevolution, algal resource management, genetic diversity, seaweed cultivation and aquaculture, marine agronomy

In this paper, we address several issues related to seaweed domestication from an evolutionary and ecological perspective. We briefly cover the history of human interactions with seaweed and assess the importance of pre-domestication evolutionary processes. The various steps of the trajectory from wild to domesticated seaweed are discussed for five crop seaweeds (i.e. Saccharina japonica (kombu), Pyropia sp. (nori), Undaria pinnatifida (wakame), Gracilaria chilensis (pellilo) and Kappaphycus sp.) to evaluate their domestication status. We show that seaweed domestication resulted from long-term interactions between humans, seaweeds, and environmental factors. This interplay has deeply modified the coastal ecosystem -sometimes with very detrimental effects (pests and invasions) -but was a key element in the evolutionary process leading to domestication. We then highlight the challenges for future research on seaweed domestication and show how better integration of knowledge on ecology and genetic 2 diversity of wild populations and on the selective pressures exerted by cultivators can promote sustainable seaweed aquaculture.

Introduction

Domestication is considered a long and complex process during which domesticators select and modify organisms that can thrive in human eco-environments and express traits of interest for human use (Tanno & Wilcox 2006;[START_REF] Larson | Current perspectives and the future of domestication studies[END_REF]. Hence, domestication involves a multi-generational relationship between humans and the target organism. Definitions of domestication vary depending on the nature of this relationship and here we adopt the recent definition by [START_REF] Zeder | Core questions in domestication research[END_REF]: "a coevolutionary, mutualistic relationship between domesticators and domesticates". Interestingly, [START_REF] Zeder | Core questions in domestication research[END_REF] draws attention to the fact that domestication should be distinguished from resource management and agriculture even if there is a continuum between these three different but overlapping processes. Management is based on the enhancement of the returns of the resource of interest, agriculture is a provisioning systems on the production and consumption of domesticates, whereas domestication is a coevolving mutualism between the manager and the managed resources. This evolutionary approach to domestication focuses on the processes that intensify a species' dependence on humans for reproduction and dispersal [START_REF] Milla | Plant domestication through an ecological lens[END_REF]. Moreover, because the evolution of a species leads to evolution of its ecological niche (according to ecological niche construction theory), domestication is also associated with ecological changes in the environment driven by humans to optimize the cultivation conditions of the domesticated species [START_REF] Smith | Neo-Darwinism, niche construction theory, and the initial domestication of plants and animals[END_REF]. "This close relationship between humans and their domesticated plants and animals is precisely one of the aspects that makes the study of domestication such a fascinating area of study" [START_REF] Gepts | Crop domestication as a long-term selection experiment[END_REF]. Full understanding of the domestication process can only be achieved within a cross-disciplinary framework that brings together genetics, evolutionary biology, ecology, and anthropology [START_REF] Larson | Current perspectives and the future of domestication studies[END_REF][START_REF] Zeder | Core questions in domestication research[END_REF][START_REF] Mckey | The evolutionary ecology of clonally propagated domesticated plants[END_REF]) and can provide important insights into general questions in evolution [START_REF]The origin of species[END_REF][START_REF] Darwin | The variation of animals and plants under domestication[END_REF]. In addition, research on the pace and biological consequences of domestication is useful for understanding present-day issues of sustainability and biodiversity loss [START_REF] Zeder | Core questions in domestication research[END_REF] and can guide the choices that are made in agriculture/aquaculture systems [START_REF] Bonneuil | Innover autrement ? La recherche face à l'avènement d'un nouveau régime de production et de régulation des savoirs en génétique végétale[END_REF].

The accelerated diversification of seaweed uses in the modern agri-food industry as well as in the pharmaceutical, textile, plastic, biofuel and other industries, is rapidly changing the way we humans interact with this natural resource [START_REF] Loureiro | Seaweed cultivation: potential and challenges of crop domestication at an unprecedented pace[END_REF]. In particular, the ever-growing need for raw materials, and the difficulty in sustainably exploiting natural populations, are forcing humans to move from gatherers/fishers to cultivators, and from cultivators to marine agronomists [START_REF] Buschmann | The status of kelp exploitation and marine agronomy, with emphasis on Macrocystis pyrifera, in Chile[END_REF]. This latter transition requires a major shift in how scientists, cultivators and farmers, and end-users interact with each other and with the resource. New cultivation processes, adapted from animal and land plant practices, are currently being developed in seaweed aquaculture [START_REF] Robinson | Genetic improvement of macroalgae: status to date and needs for the future[END_REF][START_REF] Hafting | Prospects and challenges for industrial production of seaweed bioactives[END_REF], leading humans to influence the fate of natural seaweed populations more and more. However, to what extent human activities have affected seaweed population evolutionary trajectories has yet to be investigated, because our understanding of the on-going domestication processes is only incipient.

In this paper, we first briefly cover the history of human interactions with seaweeds and asses the importance of pre-domestication evolutionary processes. Second, we map the progress of seaweed domestication against the typical milestones that have been identified in land plants and animals, and define what we consider as domesticated seaweeds, referring to the above-mentioned evolutionary and ecological definition of domestication. Lastly, we highlight key questions for future research on seaweed domestication and propose directions for sustainable seaweed aquaculture.

History of human interactions with seaweeds

Interactions of humans with seaweeds dates back to the Neolithic times [START_REF] Dillehay | Monte Verde: seaweed, food, medicine, and the peopling of South America[END_REF][START_REF] Erlandson | Ecology of the kelp highway: Did marine resources facilitate human dispersal from Northeast Asia to the Americas?[END_REF][START_REF] Ainis | Using non-dietary gastropods in coastal shell middens to infer kelp and seagrass harvesting and paleoenvironmental conditions[END_REF]. The most direct evidence of prehistoric human-seaweed interactions comes from the discovery of remnants of 11 seaweed species at the Monte Verde archaeological site in southern Chile [START_REF] Dillehay | Monte Verde: seaweed, food, medicine, and the peopling of South America[END_REF]. This discovery attests that seaweeds were gathered and consumed for food or medicine at least 14,500 years ago [START_REF] Dillehay | Monte Verde: seaweed, food, medicine, and the peopling of South America[END_REF]. The earliest written records of human interaction with seaweeds originate from Japan, where wild seaweed consumption was recorded approximately 1500 years ago [START_REF] Buchholz | Seaweed and man[END_REF]. According to ancient Chinese manuscripts, Ecklonia kurome growing on the coast of the East China Sea was consumed for its curative effect on goitre more than 1000 years ago [START_REF] Tseng | Laminaria mariculture in China[END_REF]). Later, Saccharina japonica (also called kombu) growing along the Japanese coast and characterized by much larger populations became the most important source of medicinal seaweed [START_REF] Tseng | Laminaria mariculture in China[END_REF]. In north-western Europe, brown seaweeds, collected at low tide or as beach wrack (also called varech and goemon), were traditionally employed as fuel, fertilizer and cattle feed but rarely as human food (except Palmaria palmata, also known as dulse) except during famines (in France and Ireland, Arzel 1987). The industrial use of harvested seaweed (mainly kelp) started during the 18 th century for soda ash used in the glass-making industry and later for the extraction of iodine and hydrocolloids [START_REF] Arzel | Les goémoniers. -Chasse-Marée[END_REF][START_REF] Forsythe | The archaeology of the kelp industry in the northern islands of Ireland[END_REF]). In Asia, seaweed cultivation for human food began in the 17 th century (nori: Pyropia ssp. as Porphyra spp., [START_REF] Wheeler | Marine agriculture: progress and problems[END_REF]). However, after World War II, the chemical industry took over commercial seaweed harvest for the extraction of polysaccharides [START_REF] Mathieson | Seaweed Aquaculture. -Mar[END_REF]. The global demand of seaweed products then focused on a reduced number of selected species for which natural stocks became insufficient for their supply (e.g. over-exploitation of Gracilaria chilensis in Chile in the 1980s, [START_REF] Buschmann | Seaweed future cultivation in Chile: perspectives and challenges[END_REF]. Encouraged by these demands and in the interest of reducing the overexploitation of natural resources, seaweed cultivation today is practiced around the world [START_REF] Rebours | Seaweeds: an opportunity for wealth and sustainable livelihood for coastal communities[END_REF]. All these human practices have likely modified the traits of harvested or cultivated seaweeds and the quality of their ecosystems. In light of this brief history, seaweed species and their uses are clearly highly specific to local practices and may have changed with time. Moreover, as for domesticated plants and animals, the management of natural populations and the ease of cultivation may have greatly influenced which species were chosen for domestication.

The typical milestones on the domestication trajectory

Though domestication is a continuous and dynamic process, common steps have been recognized both in plants and animals (Meyer & Purugganan 2012[START_REF] Larson | Current perspectives and the future of domestication studies[END_REF][START_REF] Milla | Shifts and disruptions in resource-use trait syndromes during the evolution of herbaceous crops[END_REF]and 2015). This trajectory from wild to domesticated species first begins with humans' deliberate care for wild stands, often called pre-domestication. Population management performed to meet human interests, by removing competitors or protecting stands from pests and herbivores, modify the species' environment and therefore the forms and directions of natural selection. Consequently, the target species may evolve with regard to several traits related to adaptation to the human-modified environment [START_REF] Milla | Shifts and disruptions in resource-use trait syndromes during the evolution of herbaceous crops[END_REF], and become increasingly amenable to cultivation. The second milestone is the control of (sexual or asexual) reproduction, a step that requires empirical knowledge of the local species in its environment. An immediate consequence may be a selective shift as humans started to modify (consciously or not) new traits by choosing the parental individuals. The third step is the spread of organisms among human ecosystems due to exchanges of biological material, leading to rapid geographical radiation of domesticates. During these early stages, humans exert major evolutionary forces on domesticates by amplifying dispersal and by applying selective forces -consciously or unconsciously -that critically modify the species and its ecosystem. Evolutionary divergences emerge between wild and cultivated populations all along these stages. One or several populations of founder gene pools gradually accumulate variable degrees of geographical or genetic isolation from their wild relatives (Figure 1). It is generally thought that this transition lasts several millennia [START_REF] Smith | The emergence of agriculture[END_REF][START_REF] Tanno | How fast was wild wheat domesticated?[END_REF] and occurs in different regions [START_REF] Purugganan | The nature of selection during plant domestication[END_REF][START_REF] Larson | Current perspectives and the future of domestication studies[END_REF]. Successive waves of plant domestication have been detected: the domestication of most annual crops from 9000 to 4000 BC, followed by most trees from 5000 to 2000 BC, and a third, more contemporary wave of rapid domestication of new crops (e.g. kiwi, cranberry and tropical nut trees) [START_REF] Meyer | Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops[END_REF]. Fuelled by the recent burgeoning of aquaculture around the world, involving a wider variety of organisms with a greater diversity of life forms than found in domesticated land species, the current rate of domestication of new species seems to be faster for marine than for terrestrial organisms [START_REF] Duarte | Rapid Domestication of Marine Species[END_REF]).

An overlooked history of pre-domestication in seaweed

One of the first reviews on seaweed domestication focused on the development of breeding programs and genetic improvement of cultivars (van der Meer 1983). Two domesticated taxa, defined as farmed organisms morphologically or genetically differentiated from their wild ancestors as a result of human selection, were recognized: the Rhodophyta Pyropia (as Porphyra sp.) and the Phaeophyceae S. japonica (as Laminaria japonica). Other taxa listed as potentially domesticated were Chondrus crispus, Gigartina exasperata, Gracilaria tikvahiae, Kappaphycus (as Eucheuma sp.) because it was possible to select and cultivate fast-growing clones in the laboratory. Based on increased biomass production, [START_REF] Duarte | Rapid Domestication of Marine Species[END_REF] listed 19 marine plants (including seaweeds) as domesticated, all part of the latest, contemporary domestication wave mentioned above.

Although [START_REF] Duarte | Rapid Domestication of Marine Species[END_REF] included seaweeds in their review, the scarcity of relevant publications probably biased their estimation of seaweed domestication success. A critical examination of the 18 seaweed taxa reveals imprecise taxonomic status, suggesting a three-fold over-estimation of the number of species. Most of the scientific publications on seaweed domestication postdate the review by [START_REF] Duarte | Rapid Domestication of Marine Species[END_REF], and were driven by the recent rise in seaweed cultivation [START_REF] Loureiro | Seaweed cultivation: potential and challenges of crop domestication at an unprecedented pace[END_REF]. However, the importance of seaweed pre-domestication is generally overlooked, partly because marine seaweeds are highly perishable and rarely survive in archaeological records.

Below, we assess the domestication status of five cultivated seaweeds (i.e. S. japonica (Kombu), Pyropia sp. (Nori), Undaria pinnatifida (Wakame), Gracilaria chilensis (Pelillo) and eucheumatoid carrageenophytes (Kappaphycus and Eucheuma spp., Table 1) in the light of the domestication trajectory defined above. We focus on evolutionary processes such as artificial selection before cultivation, the interplay between life-history traits and domestication, cultivation-induced genetic bottlenecks, genetic and phenotypic differentiation between wild and cultivated populations, the impact of cultivation on the ecosystem as well as signatures of coevolution between human and seaweeds.

Importance of artificial selection before cultivation

Kombu, wakame and nori all originate from temperate Asia and are used mainly as food for direct human consumption whereas the two others (Pelillo and eucheumatoids) are ingredients for the global agri-food industry. Most of these crops show a long history of pre-domestication -dating back from thousands to one hundred years -characterized by the management of wild populations (see references above and Table 1). The importance of artificial selection during this period is difficult to evaluate, yet it is noteworthy that seaweed uses have changed several times (i.e. from medicinal uses to raw products for the chemistry or biochemistry industry, see references above).

Therefore, any potential selection exerted by humans in the past likely targeted characters different from the presently selected ones. In contrast, eucheumatoids have no history of pre-domestication, since harvesting started in the 1950s (with cultivation beginning in the 1960s) to supply the phycocolloid industry.

Impact of life-history traits on the process of domestication

The development of massive cultures for seaweed crops was facilitated by the control of their life cycle (either sexual reproduction or vegetative propagation). Wild populations of Gracilaria and eucheumatoids show an isomorphic sexual life cycle with both haploid gametophytes and diploid tetrasporophytes growing from spores. These seaweeds are characterized by a perennial holdfast that naturally produces several fronds, each of which can live independently and propagate vegetatively when detached from the parental thallus. For these seaweeds, cultivation techniques have usually relied only on vegetative propagation techniques although in vitro shedding of carpospores from wild plants to generate new "seeds" have been attempted [START_REF] Buschmann | Red algal farming in Chile: a review[END_REF][START_REF] Luhan | Growing the reproductive cells (carpospores) of the seaweed, Kappaphycus striatum, in the laboratory until outplanting in the field and maturation to tetrasporophyte[END_REF], Table 1). The other seaweeds (e.g. Pyropia, Saccharina and Undaria) have heteromorphic life cycles in which a single upright frond grows from the holdfast. For these species, natural populations are maintained by sexual reproduction (i.e. spore production, although asexual spores can be produced in some species such as P. haitanensis, [START_REF] Wang | a study on the cultivation of the vegetative cells and protoplasts of P. haitanensis I. [J]. -Oceano[END_REF]. For these species, multi-step cultivation techniques are required to ensure the successful development of each stage of the life cycle in each stage-specific environmental condition [START_REF] Santelices | A conceptual framework for marine agronomy[END_REF]. Progress in aquaculture initially depended heavily on methods for raising sporelings, such as the one developed in the 1950s for Saccharina [START_REF] Zhang | Breeding of an elite Laminaria variety 90-1 through inter-specific gametophyte crossing[END_REF], Table 1). The development of Pyropia cultivation also clearly relied on the understanding and control of the life cycle: the cultivated organism, the macroscopic gametophyte, is based on a microscopic sporophyte (the conchocelis phase; Drew 1949); prior to this publication in 1949, the culture of gametophytes relied exclusively on the capture of wild spores [START_REF] Patwary | Genetics and breeding of cultivated seaweeds[END_REF]. The control of sexual reproduction eliminates a large amount of uncertainty due to the seasonal fluctuation of natural propagule availability, and allows the development of breeding programmes (for review, see [START_REF] Blouin | Porphyra: a marine crop shaped by stress[END_REF]. In haploid-diploid seaweeds, the manipulation of clonal propagation of some life-history stages can facilitate genetic selection. For example, in the brown algae Macrocystis pyrifera, the microscopic gametophytic phase can be cloned and stored as germplasm [START_REF] Buschmann | The status of kelp exploitation and marine agronomy, with emphasis on Macrocystis pyrifera, in Chile[END_REF][START_REF] Barrento | Germplasm banking of the giant kelp: Our biological insurance in a changing environment[END_REF], and repeatedly used in multiple crossing events with varying levels of genetic relatedness.

As in terrestrial plants [START_REF] Meyer | Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops[END_REF], these cultivated seaweeds are probably characterized by a shift in their reproductive strategy (i.e. from outcrossing to selffertilizing or from sexual reproduction to vegetative propagation) between wild populations and cultivated stands. This differentiation in reproduction is a strong evidence for domestication. The shift from sexual reproduction in the wild to vegetative propagation in cultivated farms has been demonstrated for Gracilaria [START_REF] Guillemin | Genetic variation in wild and cultivated populations of the haploid diploid red alga Gracilaria chilensis: How farming practices favor asexual reproduction and heterozygosity[END_REF]) and probably also occurred in Kappaphycus [START_REF] Ask | Advances in cultivation technology of commercial eucheumatoid species: a review with suggestions for future research[END_REF] (Table 1). Clonal propagation enables farmers to selectively multiply superior genotypes and maintain desired phenotypes that would otherwise be lost by recombination during sexual reproduction. In addition, it prevents recombination between selected strains and their wild relatives. Interestingly, unconscious selection during the domestication process favoured diploidy in Gracilaria [START_REF] Guillemin | Genetic variation in wild and cultivated populations of the haploid diploid red alga Gracilaria chilensis: How farming practices favor asexual reproduction and heterozygosity[END_REF][START_REF] Guillemin | Evidence of reproductive cost in the triphasic life history of the red alga Gracilaria chilensis (Gracilariales, Rhodophyta)[END_REF]. Due to its genetic advantage (because heterozygosis only operates in diploids, haploids are hemizygous for all genes), selection for diploidy may be the rule in vegetatively propagated haploid-diploid species [START_REF] Guillemin | Genetic variation in wild and cultivated populations of the haploid diploid red alga Gracilaria chilensis: How farming practices favor asexual reproduction and heterozygosity[END_REF], Krueger Hardfield et al. 2016). Clonal propagation has agronomic advantages, such as more rapid growth and greater survival rates (i.e. trade-off between fertility, growth and survival, in Gracilaria: [START_REF] Guillemin | Evidence of reproductive cost in the triphasic life history of the red alga Gracilaria chilensis (Gracilariales, Rhodophyta)[END_REF]in Kappaphycus: Hurtado et al. 2015). Therefore, selection against sexual reproduction is probably strong in vegetatively propagated seaweeds. However, the exclusive use of clonal propagation for crop maintenance, by selecting for sterility, may preclude further breeding improvements [START_REF] Myles | Genetic structure and domestication history of the grape[END_REF]).

In the three sexually reproducing crops, the difference in mating system between natural populations and cultivated stands is poorly documented. These haploid-diploid dioecious species display unisexual male and female gametophytes. In such species, selfing can occur by cross-fertilization between two gametophytes arising from a single sporophyte [START_REF] Krueger-Hadfield | O father where art thou? Paternity analyses in a natural population of the haploid-diploid seaweed Chondrus crispus[END_REF]. Inbreeding and selfing are the predominant mating system in cultivated stands, because of (1) the simplicity of the breeding protocol and (2) the cost of sampling and germplasm maintenance. For example, plantlets depend on germplasm collections based on a limited number of parental individuals in Undaria [START_REF] Liu | Breeding, economic traits evaluation, and commercial cultivation of a new Saccharina variety B Huangguan No. 1[END_REF], in Saccharina [START_REF] Zhang | Breeding of an elite Laminaria variety 90-1 through inter-specific gametophyte crossing[END_REF], Li et al. 2016) and in Pyropia [START_REF] Bi | Genetic diversity of wild population of Pyropia haitanensis based on SSR analysis[END_REF]) (Table 1).

Targeted selection of particular traits (frond length and weight, mannitol, alginate, morphology of the blade and tolerance to higher temperature; [START_REF] Li | Trait evaluation and trial cultivation of Dongfang No. 2, the hybrid of a male gametophyte clone of Laminaria longissima (Laminariales, Phaeophyta) and a female one of L. japonica[END_REF], Li et al. 2016, Zhang et al. 2007) combined with consecutive inbreeding or selfing, gave rise to the first varieties or strains in Saccharina. Little is known, about the importance of selfing in the wild for this species, although population genetics tools are available to examine this question [START_REF] Liu | Genetic diversity and structure within and between wild and cultivated Saccharina japonica (Laminariales, Phaeophyta) revealed by SSR markers[END_REF]). However, a reduction in productivity of some of these strains has been observed, and has been attributed to inbreeding depression [START_REF] Liu | Breeding, economic traits evaluation, and commercial cultivation of a new Saccharina variety B Huangguan No. 1[END_REF].

Clearly, further studies are required to estimate the effects of a shift in the mating system from outcrossing to selfing.

Dispersal outside of their native range for cultivation: consequences on genetic and phenotypic diversity

All cultivated crops have been actively dispersed outside of their native range distribution by humans (Table 1). In vegetatively propagated domesticates, transport over large geographic distances has generated extreme bottlenecks during crop foundation. In Gracilaria, reduction in genetic diversity due to a cultivation bottleneck and subsequent clonal propagation has been detected in farms [START_REF] Guillemin | Genetic variation in wild and cultivated populations of the haploid diploid red alga Gracilaria chilensis: How farming practices favor asexual reproduction and heterozygosity[END_REF]. The cultivation of eucheumatoids now involves 20 tropical countries, often based on small quantities of plants collected in the Philippines [START_REF] Hurtado | Developments in production technology of Kappaphycus in the Philippines: more than four decades of farming[END_REF]. The genetic diversity of cultivars is thus probably extremely reduced compared to natural sexual populations [START_REF] Halling | Introduction of Asian strains and low genetic variation in farmed seaweeds: indications for new management practices[END_REF]. For crops based on a reduced number of strains, clonality rapidly narrows their genetic background and can lead to greater susceptibility to pathogens, as observed for Gracilaria [START_REF] Leonardi | Diversity, phenomenology and epidemiology of epiphytism in farmed Gracilaria chilensis (Rhodophyta) in northern Chile[END_REF], Pyropia [START_REF] Kim | A revaluation of algal diseases in Korean Pyropia (Porphyra) sea farms and their economic impact[END_REF]) and eucheumatoids (Loureiro et al. 2015).

Such effects of reduced genetic diversity in cultivated stands compared to natural populations has also been reported for some of the three sexually reproducing species (in Saccharina: [START_REF] Liu | Genetic diversity and structure within and between wild and cultivated Saccharina japonica (Laminariales, Phaeophyta) revealed by SSR markers[END_REF], Table 1). The case of Undaria is somewhat different since this species has become invasive in introduced areas [START_REF] Voisin | Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects[END_REF] and references in Table 1). A comparison between cultivated Undaria stands and natural (or escaped to the wild) populations within their natural range and in their introduced range shows that genetic diversity depends on introduction history (i.e. single or multiple introductions, [START_REF] Voisin | Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects[END_REF], Table 1). In conclusion, it is clear that the genetic variability of domesticated seaweeds over their natural distribution range has been very poorly explored [START_REF] Zuccarello | Systematics and genetic variation in commercial shape Kappaphycus and shape Eucheuma (Solieriaceae, Rhodophyta)[END_REF], Loureiro et al. 2015[START_REF] Barrento | Germplasm banking of the giant kelp: Our biological insurance in a changing environment[END_REF]. Regardless of the criteria used to select strains from natural variants, the lack of general knowledge on the environmental and genetic drivers of phenotypic diversity suggests that many other interesting traits may be found in the wild stock. In this context, other domestication strategies are being developed for terrestrial species to both minimize the rate of loss of genetic diversity and to encourage local farmers to develop their own local set of cultivars or landraces [START_REF] Thomas | Seed exchanges, a key to analyze crop diversity dynamics in farmer-led on-farm conservation[END_REF]. This approach can be useful for seaweeds that are still mostly managed worldwide by small local fisher communities, such as Kappaphycus [START_REF] Msuya | Impact of environmental changes on farmed seaweed and farmers: the case of Songo Island, Tanzania[END_REF] and Gracilaria [START_REF] Buschmann | Red algal farming in Chile: a review[END_REF].

Our understanding of phenotypic changes associated with plant domestication and their possible genetic basis comes from a very low number of well-studied crop models that reproduce sexually [START_REF] Meyer | Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops[END_REF]). Nevertheless, due to recombination, artificial selection in sexual species is more complex and slower than in vegetatively propagated species. It is clear from the literature that asexual plant crops encompass a much broader range of adaptations than sexual ones [START_REF] Mckey | The evolutionary ecology of clonally propagated domesticated plants[END_REF]. The evolution of domesticated adaptations can be observed after only a few generations of asexual cultivation [START_REF] Meyer | Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops[END_REF]. When recombination occurs, selection associated with domestication should reduce diversity in some restricted regions of the genome, namely those that contain genes controlling traits of human interest [START_REF] Wang | The limits of selection during maize domestication[END_REF]. Conversely, because clonal reproduction mimics a complete physical linkage over the entire genome, intense selection acting on genes controlling traits of human interest affect the whole genome.

Interestingly, in their review, [START_REF] Mckey | The evolutionary ecology of clonally propagated domesticated plants[END_REF] demonstrate that traditional cultivation practices of clonal domesticated plants allow recurrent recruitment of a small amount of sexually produced seeds. These practices thus ensure the maintenance of genotypic diversity and the regular reintroduction of recombination. With the methods of nextgeneration sequencing, it is now possible to examine genome-wide patterns of polymorphism to identify genomic regions that show signatures of selection [START_REF] Beaumont | Identifying adaptive genetic divergence among populations from genome scans[END_REF][START_REF] Nielsen | Molecular signatures of natural selection[END_REF].

Impact of cultivation on the ecosystem

Intensive farming and domestication are commonly accompanied by profound and often irreversible consequences for the environment. Firstly, the commercial introduction of non-native species or genotypes across continents has resulted in many examples of invasion. Cultivars are usually selected for their tolerance to a large set of environmental conditions and fast growth; once selected for, such all-purpose phenotypes represent a risk for native coastal communities where they can compete with, and sometimes outcompete native species (Figure 2). This is the case of Undaria that has proven suitable for cultivation in many different regions, and is now rapidly expanding its range -owing to human-mediated, long-distance transportation -even in regions where it is not cultivated [START_REF] Voisin | Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects[END_REF][START_REF] Grulois | Mosaic genetic structure and sustainable establishment of the invasive kelp Undaria pinnatifida within a bay (Bay of St-Malo, Brittany)[END_REF]. Biological invasions may strongly modify native seaweed diversity by direct competition and also by increasing the probability of introducing associated pests. The introduction of seaweeds for aquaculture purposes can introduce new pathogens and act as reservoirs for local ones (see Figure 2).

A second risk is through the so-called "crop-to-wild" gene flow, well documented in agriculture [START_REF] Ellstrand | Current knowledge of gene flow in plants: implications for transgene flow[END_REF], 2013[START_REF] Campbell | Weed evolution after crop gene introgression: greater survival and fecundity of hybrids in a new environment[END_REF]. Importantly, for recently domesticated species, an increase in the rate of domestication leads to an increase in the strength of genetic sweeps and diminishes the reproductive isolation of domesticates with their wild counterparts. This pattern is expected because selective sweeps affect only the genomic regions related to the trait conferring the advantage in the new, cultivated environment, whereas the genomic regions determining reproductive isolation are not affected. Such crop-to-wild gene flow can promote the massive spread of the selected alleles, potentially leading to genetic erosion of native populations (Figure 2). In Norway, the cumulative introgression of farmed salmon genotypes ranges from 2% to more than 40% in wild populations [START_REF] Glover | Atlantic salmon populations invaded by farmed escapees: quantifying genetic introgression with a Bayesian approach and SNPs[END_REF]. A high level of introgression can thus be observed in some wild Norwegian populations only four decades after farming started.

Likewise, hybridization of cultivated seaweeds with native stocks can result in an impoverishment of local genetic diversity, further impacting ecosystem resilience [START_REF] Hutchings | The nature of fisheries-and farming-induced evolution[END_REF]. However, to date, gene flow from seaweed breeds into native stocks has been virtually unmeasured. The rapid development of fish, shellfish, and crustacean aquaculture over the past few decades further highlights a third risk that needs to be anticipated. For example, the white spot syndrome virus, first discovered in shrimp farms in the early 1990s, spread globally in less than a decade and now affects roughly 100 wild crustacean species, whose populations may act as reservoirs and vectors (Figure 2). In any agricultural or aquaculture system, pests typically reduce production yields by a fifth to a third, a rule that also holds true for cultivated seaweeds [START_REF] Gachon | Algal diseases: spotlight on a black box[END_REF].

Because the use of pesticides is inappropriate [and illegal?] in open sea aquaculture, cultivated stands can also act as a reservoir for pests and pathogens that will further affect surrounding natural populations. In all aquaculture sectors, raising awareness of pests and diseases consistently engenders regulations that restrict the movement of broodstock [START_REF] Stentiford | Crustacean diseases in European legislation: implications for importing and exporting nations[END_REF]) and imposes rigorous monitoring for symptoms of infectious diseases.

Signal of co-evolution between human and domesticated seaweed

The long-term domesticate-domesticator interaction eventually leads to mutualistic coevolution (Zeder 2015 and references below). The best-documented examples are the evolution of lactose tolerance in European adults, linked to the appearance of dairy products in their diet during the Neolithic [START_REF] Beja-Pereira | Geneculture coevolution between cattle milk protein genes and human lactase genes[END_REF] and the increase in the copy number of salivary amylase genes, related to plant domestication [START_REF] Perry | Diet and the evolution of human amylase gene copy number variation[END_REF]).

Such co-evolution is likely in progress for seaweeds: a recent comparative gut metagenome analysis revealed that Japanese populations host a bacterium encoding horizontally-acquired porphyranase and algarase, conferring higher digestive ability in this population compared to a control population [START_REF] Hehemann | Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota[END_REF]. Studies of domestication in seaweed may thus bring additional clues on how cultural practices may drive selection in humans.

Conclusion

From the examples discussed above, it appears that domestication resulted from a longterm interaction between humans, seaweeds and environmental factors for species such as Gracilaria (Figure 3), whereas it was only initiated recently for eucheumatoids (Parker et al. 1974). Even if the recent development of aquaculture suggests fast domestication is affecting seaweeds, the literature suggests a long history of local practices developed by farmers which probably led to pre-domestication and selection of landraces (Figure 1). Some seaweed crops now depend on humans for their reproduction/propagation, and, likewise, some human social structures depend on seaweed resources. This strong interaction has deeply modified the coastal ecosystem, sometimes leading to very detrimental effects (pests and invasions, Figure 2). Further research on seaweed domestication needs to better integrate these different aspects through multidisciplinary approaches. To conclude, we would like to propose some lines of research on the seaweed domestication process that may help the development of sustainable seaweed aquaculture.

Understanding which traits and environmental factors are involved in pre-domestication may help breeders and cultivators to select better parental strains for their germplasms, thus optimizing seaweed selection. Furthermore, this selection process may be a cornerstone for the future sustainability of seaweed aquaculture. Ecophysiological experiments on cultivated seaweeds have been conducted for several decades, but should be considered in light of the evolutionary adaptations that can contribute to an efficient cultivation system. For instance, the existence of phenotypic plasticity versus local adaptation in shaping the phenotypic variance is largely unexplored, although large phenotypic variance is often reported in association with environmental heterogeneity.

The actual heritabilities of traits of interest and the genetic correlations between traits or between life stages of the complex, haploid-diploid life cycle are thus far ignored. This raises the importance of developing the quantitative genetics for complex life cycles.

The "green revolution" of the mid-20 th century provided significant yield improvement [START_REF] Khush | Green revolution: the way forward[END_REF], at the cost of genetic depression of breeds and massive pesticide and fertilizer use. For increased sustainability, new alternative models based on selection of local variants aim to maintain the genetic diversity necessary for adapting to future climate risks and meeting food security needs [START_REF] Fowler | Shattering: food, politics, and the loss of genetic diversity[END_REF][START_REF] Jarvis | A global perspective of the richness and evenness of traditional crop-variety diversity maintained by farming communities[END_REF].

Because cultivated seaweeds are either wild species or at the very early stages of domestication, the search for a stable, elite phenotype may prove difficult because of the large genetic variance expected in all the traits related to the success of a strain in a cultivation system. In addition, it is likely that high spatio-temporal variability hinders the sustainable use of an elite cultivar because the marine environment cannot be manipulated as easily as terrestrial agricultural landscapes are for water, nutrient supply and pest control. Therefore, elite cultivars should be designed only for indoor cultivation systems, whereas the breeding strategy for mariculture systems should take the constraints of environmental variability into account and exploit rather than reduce the genetic variance of specific traits. Molecular-assisted breeding holds much promise to mitigate the issue of genetic erosion; acquiring in-depth knowledge on polymorphisms in populations can help identify native genetic genotypes containing desirable traits for "à la carte" introgression into local cultivars. Complementary regional efforts to develop fullgenotype diversity germplasms should be developed to have backup conservation strategies [START_REF] Barrento | Germplasm banking of the giant kelp: Our biological insurance in a changing environment[END_REF].

Thirdly, suitable regulations need to be developed to accompany new cultivation endeavours, in accordance with detailed assessments of the potential environmental risks and a clear understanding of conflicting socio-economic interests (Figure 2; [START_REF] Fröcklin | Seaweed mariculture as a development project in Zanzibar, East Africa: A price too high to pay?[END_REF]. Utmost caution must be applied because of the dispersive characteristics of the marine environment and the lack of reproductive isolation between crop and wild seaweed, for example when considering the potential utilization of transgenesis. Existing European and national regulations restrict the release of organisms in the open sea to endemic strains (e.g. European Regulations No. 708/2007, No. 535/2008and No. 506/2008 amending Annex IV to Council Regulation (EC) No. 708/2007). In such environmental assessments, it is also important to foresee that regulations can be circumvented, as illustrated by the inadvertent introduction of an invasive alga and viruses alongside illegal introductions of the Pacific oyster in Europe [START_REF] Mineur | Positive feedback loop between introductions of non-native marine species and cultivation of oysters in Europe[END_REF], and the illegal cultivation of Kappaphycus alvarezii in northern Brazil [START_REF] Araujo | Molecular identification of the exotic lineage of Kappaphycus alvarezii (Rhodophyta, Solieriaceae) cultivated in the tropical region of Brazil[END_REF] .

In conclusion, research on seaweed domestication should be oriented towards management practices and breeding strategies that allow the maintenance of the domesticates' evolutionary potential. This may include the choice of source populations and the selection of varieties suitable for sustainable agricultural systems in the context of spatial and temporal environmental variability, given the difficulty to standardize cultivation conditions in the open sea. Optimization of phenotypic variance (and the underlying genetic diversity), rather than minimizing it to homogenize the production, will require a paradigm shift in breeding strategies and a new definition of research goals.

Ultimately, the dynamic management of seaweed diversity should promote the development of innovative sustainable aquaculture ecosystems that can adapt to the specificities of the marine environment. For seaweeds cultivated exclusively through vegetative propagation, i.e. repeated cutting of young branches from the same plant to form 'plantlets' (as performed for Kappaphycus and Gracilaria), the domestication process can be far more faster and completed in less than 50 years. Further to their domestication, these two seaweeds represent a limited genetic stock [START_REF] Hurtado | Cultivation of tropical red seaweeds in the BIMP-EAGA region[END_REF], Guillemin et al. 2008). escapees may also compete with native plants for habitat and reproduction. Therefore, research needs to encompass the development of breeding techniques that maximize yield and biodiversity, the identification and management of pathogens, and the determination of wild genetic resources. For each species, the relative importance of each interaction needs to be assessed, taking into account the biology and life history of the species and the difficulties of biological containment in the marine environment. -Worldwide impact as an invasive species (Red listed) 24 -Escaped from cultivated farms 22,29 -Gene flow between wild and cultivated populations 23,,30,32 -High socio-economic impact 32 -Food 33 Sahoo & Yarish, [START_REF] Hwang | Cultivation of a hybrid of free-living gametophytes between Undariopsis peterseniana and Undaria pinnatifida: morphological aspects and cultivation period[END_REF][START_REF] Perez | Culture expérimentale de l'algue Undaria pinnatifida sur les côtes de France[END_REF][START_REF] Grulois | Mosaic genetic structure and sustainable establishment of the invasive kelp Undaria pinnatifida within a bay (Bay of St-Malo, Brittany)[END_REF]Schaffelke et al., Saito 1975[START_REF] Gao | Genetic differentiation of hightemperature tolerance in the kelp Undaria pinnatifida sporophytes from geographically separated populations along the Pacific coast of Japan[END_REF]Shibneva et al., Voisin et al., 2005[START_REF] Shan | Breeding of an elite cultivar Haibao No. 1 of Undaria pinnatifida (Phaeophyceae) through gametophyte clone crossing and consecutive selection[END_REF]) [START_REF] Uwai | Intraspecific genetic diversity of Undaria pinnatifida in Japan, based on the mitochondrial cox3 gene and the ITS1 of nrDNA[END_REF][START_REF] Floc | The Japanese brown alga Undaria pinnatifida on the coast of France and its possible establishment in European waters[END_REF][START_REF] Schaffelke | Impacts of introduced seaweeds[END_REF] Yamanaka & Akiyama 1993 ? -Diversification of fishing activities 51 -Detrimental effect of epiphytism on biomass production 50, 51 -Genetic depletion of both natural and wild populations due to overharvesting and genetic bottlenecks 43, 49

Eucheumatoids

Figure 1 :

 1 Figure 1: An overview of the domestication process in seaweeds, and the demographic, genetic and phenotypic changes involved (modified from Glemin et al. 2009).

Fig. 2 .

 2 Fig. 2. Effect of cultivation on the ecosystem: interaction between wild populations and cultivated stands. Three types of biological interactions between wild and cultivated stocks may contribute to the environmental footprint of seaweed domestication: Genetic selection and subsequent crop-to-wild gene flow may affect both allelic frequencies and genetic structure in wild populations. Pathogens can also mediate similar interactions;

Figure 3 :

 3 Figure 3: Domestication results from the interactions of seaweed, humans and environmental factors. All three factors are required for domestication to take place (adapted from Gepts 2010).

Table 1 : Domestication stages and main characteristics of seaweed crops. Species Management of wild populations Control of sexual reproduction or vegetative propagation for cultivation Aquaculture: moving individuals from the wild to human ecosystems

 1

	Geographical radiation of	Conscious selection	Unconscious	Landraces	Cultivars	Modification of human	Ref
	domesticated species	(Phenotypic traits)	selection			ecosystems (Invasion,
	(founder effect,		(Phenotypic			pest, gene flow
	differentiation between		traits, tradeoff)			between wild and
	wild and cultivated)					cultivated populations,
						decrease of genetic
						diversity)

Acknowledgments:

MV, CD, BJ, MLG and SF benefited from the support of the French National Research Agency with regard to an investment expenditure programme IDEALG (ANR-10-BTBR-04), and from the international research network BioDiversity, Evolution and Biotechnology of Marine Algae (GDRI No.0803). AHB, CC and SF were supported by CONICYT grant FB-0001 and SF by Iniciativa Cientifica Milenio grant ICM P10-033F. CMMG and YB were funded by the UK NERC Global Seaweed project (IOF Pump-priming + scheme, NE/L013223/1).

FONDECYT grant No. 1130797 (CONICYT) to MLG is also acknowledged.

References: