Genomic, stoking and conservation of the Mediterranean brown trout (Salmo trutta)

La truite commune Salmo trutta L. est l'espèce de salmonidés la plus rependue en Europe. Cette espèce présente une grande diversité phénotypique liée à son histoire évolutive complexe. Chaque année, d’intenses repeuplements ont lieu afin d’augmenter les densités locales de populations, notamment pour la pêche sportive. Des truites d’origine atlantique, domestiquées depuis des décennies, et plus récemment des souches domestiques méditerranéennes, sont largement utilisées pour repeupler les populations sauvages locales d’origine méditerranéenne dans le sud de la France. Jusqu’à présent, les conséquences des interactions génétiques, telles que l’hybridation et l’introgression d’allèles domestiques dans les populations locales résultants de ces repeuplements, étaient suivies à l’aide de marqueurs allozymes et microsatellites. Cependant, en raison de leurs nombres extrêmement réduits, ces marqueurs n’offraient qu’une représentation très partielle du génome. Ainsi, leur étude ne permet pas de rendre compte fidèlement des signatures génomiques associées aux pratiques de repeuplement, nécessaires pour comprendre les conséquences évolutives de l’introgression. L’objectif de cette thèse est donc d’étudier à l’échelle génomique les conséquences des interactions génétiques induites par l’introduction d’individus domestiques d’origines atlantique et méditerranéenne dans les populations ‘sauvages’ méditerranéennes du bassin de l’Orb. La première partie de cette thèse rend compte du développement d’environ 196000 marqueurs SNPs et d’une carte de liaison génétique haute densité chez S. trutta. Dans la deuxième partie, les outils moléculaires précédemment développés sont utilisés pour détecter à l’échelle individuelle les haplotypes introgressés et ainsi décrire le paysage génomique de l’introgression dans trois populations sauvages du bassin de l’Orb. La distribution de la taille de ces haplotypes est alors utilisée en prenant en compte les variations du taux local de recombinaison pour estimer l’âge moyen de l’introgression dans chaque population locale. Finalement, la troisième partie s’intéresse aux pressions sélectives - positives ou négatives - qui modulent le paysage génomique de l’introgression d’allèles domestiques dans les populations sauvages. Les résultats suggèrent que les conséquences de l’hybridation sur la valeur sélective des individus doivent être considérées séparément entre le court et le long terme. Ces travaux montrent que la compréhension des mécanismes évolutifs impliqués présente un intérêt majeur pour la conservation et la gestion des populations naturelles.The brown trout Salmo trutta L. is the most widely distributed salmonid species in Europe. The species presents a high level of phenotypic diversity linked to its complex evolutionary history. An Atlantic hatchery lineage, which has been domesticated for decades, and more recently a domesticated Mediterranean strain, have been largely used for restocking and enhancement of wild Mediterranean populations in southern France, especially for recreational fishing. The impact of restocking practices on brown trout genetic diversity and population genetic structure has been extensively studied with allozyme and microsatellite markers. However, the small number of genetic markers used in these studies did not allow to get a genome-wide representation of introgression. The aim of this thesis was to assess the genome-wide impact of repeated introductions of Atlantic and Mediterranean domesticated strains into wild Mediterranean populations. First, a large number of SNP markers have been developed as well as a high density genetic map for S. trutta. Secondly, the molecular tools previously developed have been used to detect introgressed haplotypes and to provide a detailed picture of introgression frequency patterns across the genome of three wild populations from the Orb drainage. The length distribution of admixture tracts was used to determine the timing of introgression, taking variation in local recombination rate into account. Finally, this study focused on the positive or negative selective forces that modulate the genome-wide landscape of introgression. Our results suggest that the consequences of hybridization on individual fitness have to be considered separately over short and long timescales. This work shows that understanding the evolutionary consequences of stocking practices is of major interest for the conservation and management of natural populations

Génomique, repeuplement et conservation chez la truite (Salmo trutta) méditerranéenne

The brown trout Salmo trutta L. is the most widely distributed salmonid species in Europe. The species presents a high level of phenotypic diversity linked to its complex evolutionary history. An Atlantic hatchery lineage, which has been domesticated for decades, and more recently a domesticated Mediterranean strain, have been largely used for restocking and enhancement of wild Mediterranean populations in southern France, especially for recreational fishing. The impact of restocking practices on brown trout genetic diversity and population genetic structure has been extensively studied with allozyme and microsatellite markers. However, the small number of genetic markers used in these studies did not allow to get a genome-wide representation of introgression. The aim of this thesis was to assess the genome-wide impact of repeated introductions of Atlantic and Mediterranean domesticated strains into wild Mediterranean populations. First, a large number of SNP markers have been developed as well as a high density genetic map for S. trutta. Secondly, the molecular tools previously developed have been used to detect introgressed haplotypes and to provide a detailed picture of introgression frequency patterns across the genome of three wild populations from the Orb drainage. The length distribution of admixture tracts was used to determine the timing of introgression, taking variation in local recombination rate into account. Finally, this study focused on the positive or negative selective forces that modulate the genome-wide landscape of introgression. Our results suggest that the consequences of hybridization on individual fitness have to be considered separately over short and long timescales. This work shows that understanding the evolutionary consequences of stocking practices is of major interest for the conservation and management of natural populations.La truite commune Salmo trutta L. est l'espèce de salmonidés la plus rependue en Europe. Cette espèce présente une grande diversité phénotypique liée à son histoire évolutive complexe. Chaque année, d’intenses repeuplements ont lieu afin d’augmenter les densités locales de populations, notamment pour la pêche sportive. Des truites d’origine atlantique, domestiquées depuis des décennies, et plus récemment des souches domestiques méditerranéennes, sont largement utilisées pour repeupler les populations sauvages locales d’origine méditerranéenne dans le sud de la France. Jusqu’à présent, les conséquences des interactions génétiques, telles que l’hybridation et l’introgression d’allèles domestiques dans les populations locales résultants de ces repeuplements, étaient suivies à l’aide de marqueurs allozymes et microsatellites. Cependant, en raison de leurs nombres extrêmement réduits, ces marqueurs n’offraient qu’une représentation très partielle du génome. Ainsi, leur étude ne permet pas de rendre compte fidèlement des signatures génomiques associées aux pratiques de repeuplement, nécessaires pour comprendre les conséquences évolutives de l’introgression. L’objectif de cette thèse est donc d’étudier à l’échelle génomique les conséquences des interactions génétiques induites par l’introduction d’individus domestiques d’origines atlantique et méditerranéenne dans les populations ‘sauvages’ méditerranéennes du bassin de l’Orb. La première partie de cette thèse rend compte du développement d’environ 196000 marqueurs SNPs et d’une carte de liaison génétique haute densité chez S. trutta. Dans la deuxième partie, les outils moléculaires précédemment développés sont utilisés pour détecter à l’échelle individuelle les haplotypes introgressés et ainsi décrire le paysage génomique de l’introgression dans trois populations sauvages du bassin de l’Orb. La distribution de la taille de ces haplotypes est alors utilisée en prenant en compte les variations du taux local de recombinaison pour estimer l’âge moyen de l’introgression dans chaque population locale. Finalement, la troisième partie s’intéresse aux pressions sélectives - positives ou négatives - qui modulent le paysage génomique de l’introgression d’allèles domestiques dans les populations sauvages. Les résultats suggèrent que les conséquences de l’hybridation sur la valeur sélective des individus doivent être considérées séparément entre le court et le long terme. Ces travaux montrent que la compréhension des mécanismes évolutifs impliqués présente un intérêt majeur pour la conservation et la gestion des populations naturelles

Associative Overdominance and Negative Epistasis Shape Genome-Wide Ancestry Landscape in Supplemented Fish Populations

The interplay between recombination rate, genetic drift and selection modulates variation in genome-wide ancestry. Understanding the selective processes at play is of prime importance toward predicting potential beneficial or negative effects of supplementation with domestic strains (i.e., human-introduced strains). In a system of lacustrine populations supplemented with a single domestic strain, we documented how population genetic diversity and stocking intensity produced lake-specific patterns of domestic ancestry by taking the species’ local recombination rate into consideration. We used 552 Brook Charr (Salvelinus fontinalis) from 22 small lacustrine populations, genotyped at ~32,400 mapped SNPs. We observed highly variable patterns of domestic ancestry between each of the 22 populations without any consistency in introgression patterns of the domestic ancestry. Our results suggest that such lake-specific ancestry patterns were mainly due to variable associative overdominance (AOD) effects among populations (i.e., potential positive effects due to the masking of possible deleterious alleles in low recombining regions). Signatures of AOD effects were also emphasized by highly variable patterns of genetic diversity among and within lakes, potentially driven by predominant genetic drift in those small isolated populations. Local negative effects such as negative epistasis (i.e., potential genetic incompatibilities between the native and the introduced population) potentially reflecting precursory signs of outbreeding depression were also observed at a chromosomal scale. Consequently, in order to improve conservation practices and management strategies, it became necessary to assess the consequences of supplementation at the population level by taking into account both genetic diversity and stocking intensity when available

Using Haplotype Information for Conservation Genomics

International audienceThe particular combinations of alleles that define haplotypes along individual chromosomes can be determined with increasing ease and accuracy by using current sequencing technologies. Beyond allele frequencies, haplotype data collected in population samples contain information about the history of allelic associations in gene genealogies, and this is of tremendous potential for conservation genomics. We provide an overview of how haplotype information can be used to assess historical demography, gene flow, selection, and the evolutionary outcomes of hybridization across different timescales relevant to conservation issues. We address technical aspects of applying such approaches to nonmodel species. We conclude that there is much to be gained by integrating haplotype-based analyses in future conservation genomics studies

Genomic consequences of a recent three-way admixture in supplemented wild brown trout populations revealed by local ancestry tracts

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Redundancy analysis, genome-wide association studies, and the pigmentation of brown trout (Salmo trutta L.)

International audiencePigmentation variation in the polytypic brown trout (Salmo trutta) has an unknown genomic basis. Using redundancy analyses and genome-wide association studies, authors showed that pigmentation has a large polygenic basis in this species, based on hundreds of loci known to be associated to colour. Redundancy analysis also showed that backcrossed wild trout converged to a locally adaptive Mediterranean pigmentation pattern despite the release of Atlantic hatchery fish

A Dense Brown Trout ( Salmo trutta ) Linkage Map Reveals Recent Chromosomal Rearrangements in the Salmo Genus and the Impact of Selection on Linked Neutral Diversity

International audienceHigh-density linkage maps are valuable tools for conservation and eco-evolutionary issues. Insalmonids, a complex rediploidization process consecutive to an ancient whole genome duplication eventmakes linkage maps of prime importance for investigating the evolutionary history of chromosomerearrangements. Here, we developed a high-density consensus linkage map for the brown trout (Salmotrutta), a socioeconomically important species heavily impacted by human activities. A total of 3977 ddRADmarkers were mapped and ordered in 40 linkage groups using sex- and lineage-averaged recombinationdistances obtained from two family crosses. Performing map comparison betweenS. truttaand its sisterspecies,S. salar, revealed extensive chromosomal rearrangements. Strikingly, all of the fusion andfissionevents that occurred after theS. salar/S. truttaspeciation happened in the Atlantic salmon branch, whereasthe brown trout remained closer to the ancestral chromosome structure. Using the strongly conservedsynteny within chromosome arms, we aligned the brown trout linkage map to the Atlantic salmon genomesequence to estimate the local recombination rate inS. truttaat 3721 loci. A significant positive correlationbetween recombination rate and within-population nucleotide diversity (p) was found, indicating thatselection constrains variation at linked neutral sites in brown trout. This new high-density linkage mapprovides a useful genomic resource for future aquaculture, conservation, and eco-evolutionary studies inbrown trou

Strong parallel differential gene expression induced by hatchery rearing weakly associated with methylation signals in adult Coho Salmon ( O. kisutch )

Human activities and resource exploitation led to a massive decline of wild salmonid populations, consequently numerous conservation programs have been developed to supplement wild populations. However, many studies documented reduced fitness of hatchery-born relative to wild fish. Here, by using both RNA sequencing and Whole Genome Bisulfite Sequencing (WGBS), we show that of hatchery and wild born adult Coho Salmon (Oncorhynchus kisutch) originating from two previously studied river systems, early-life hatchery rearing environment induced significant and parallel gene expression differentiation is maintained until Coho come back to their natal river for reproduction. A total of 3,643 genes differentially expressed and 859 co-expressed genes were down-regulated in parallel in hatchery born fish from both rivers relative to their wild congeners. Among those genes, 26 displayed a significant relationship between gene expression and the median gene body methylation and 669 single CpG displayed a significant correlation between methylation level and the associated gene expression. The link between methylation and gene expression was weak suggesting that DNA methylation is not the only player in mediating hatchery-related expression differences. Yet, significant gene expression differentiation was observed despite 18 month spent in a common environment (i.e. the sea). Finally, the differentiation is observed in parallel in two different river system, highlighting the fact that early life environment may account for at least some of the reduced fitness of the hatchery salmon in the wild. These results illustrate the relevance and importance of considering both epigenome and transcriptome to evaluate the costs and benefits of large-scale supplementation programs

Epigenomic modifications induced by hatchery rearing persist in germ line cells of adult salmon after their oceanic migration

Human activities induce direct or indirect selection pressure on natural population and may ultimately affect population’s integrity. While numerous conservation programs aimed to minimize human‐induced genomic variation, human‐induced environmental variation may generate epigenomic variation potentially affecting fitness through phenotypic modifications. Major questions remain pertaining to how much epigenomic variation arises from environmental heterogeneity, whether this variation can persist throughout life, and whether it can be transmitted across generations. We performed whole genome bisulfite sequencing (WGBS) on the sperm of genetically indistinguishable hatchery and wild born migrating adults of Coho salmon (Oncorhynchus kisutch) from two geographically distant rivers at different epigenome scales. Our results showed that coupling WGBS with fine scale analyses (local and chromosomal) allows the detection of parallel early‐life hatchery‐induced epimarks that differentiate wild from hatchery‐reared salmon. Four chromosomes and 183 differentially methylated regions (DMRs) displayed a significant signal of methylation differentiation between hatchery and wild born Coho salmon. Moreover, those early‐life epimarks persisted in germ‐line cells despite about 1.5 year spent in the ocean following release from hatchery, opening the possibility for transgenerational inheritance. Our results strengthen the hypothesis that epigenomic modifications environmentally‐induced during early‐life development persist in germ cells of adults until reproduction, which could potentially impact their fitness

Using genome-wide ancestry pattern in European sea bass to assess phenotypic variation and ensure sustainable aquaculture

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