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Disease emergence is accelerating in response to human activity-induced global changes. Understanding the mechanisms by which host populations can rapidly adapt to this threat will be crucial for developing future management practices. Pacific Oyster Mortality Syndrome (POMS) imposes a substantial and recurrent selective pressure on oyster populations (Crassostrea gigas). Rapid adaptation to this disease may arise through both genetic and epigenetic mechanisms. In this study, we used a combination of whole exome capture of bisulfite-converted DNA, next-generation sequencing, and (epi)genome-wide association mapping, to show that natural oyster populations differentially exposed to POMS displayed signatures of selection both in their genome (single nucleotide polymorphisms) and epigenome (CG-context DNA methylation). Consistent with higher resistance to POMS, the genes targeted by genetic and epigenetic variations were mainly related to host immunity. By combining correlation analyses, DNA methylation quantitative trait loci, and variance partitioning, we revealed that a third of the observed phenotypic variation was explained by interactions between the genetic sequence and epigenetic information, ∼14% by the genetic sequence, and up to 25% by the epigenome alone. Thus, as well as genetic adaptation, epigenetic mechanisms governing immune responses contribute significantly to the rapid adaptation of hosts to emerging infectious diseases.

Disease emergence is accelerating with global changes. Understanding by which mechanisms host populations can rapidly adapt will be crucial for management practices. Pacific oyster mortality syndrome (POMS) imposes a substantial and recurrent selective pressure on oyster populations, and rapid adaptation may arise through genetics and epigenetics. In this study, we used (epi)genome-wide association mapping to show that oysters differentially exposed to POMS displayed genetic and epigenetic signatures of selection. Consistent with higher resistance to POMS, the genes targeted included many genes in several pathways related to immunity. By combining correlation, DNA methylation quantitative trait loci, and variance partitioning, we revealed that a third of phenotypic variation was explained by interactions between the genetic and epigenetic information, ~14% by the genome, and up to 25% by the epigenome alone. Similar to genetically based adaptation, epigenetic mechanisms notably governing immune responses can contribute substantially to the rapid adaptation of hosts to emerging infectious diseases.

Phenotypic plasticity, the ability of one genotype to produce different phenotypes in different environments, plays a central role in species' response to environmental changes. Transgenerational plasticity (TGP) allows the transmission of this environmentally-induced phenotypic variation across generations, and can influence adaptation. To date, the genetic control of TGP, its long-term stability, and its potential costs remain largely unknown, mostly because empirical demonstrations of TGP across many generations in several genetic backgrounds are scarce. Here, we examined how genotype determines the TGP of phenotypic traits related to dispersal, a fundamental process in ecology and evolution. We used an experimental approach in Tetrahymena thermophila, a ciliate model-species, to determine if and how phenotypic changes expressed following a dispersal treatment are inherited over multiple generations. Our results show that morphological and movement traits associated with dispersal are plastic, and that these modifications are inherited over at least 35 generations. The fitness costs and benefits associated with these plastic changes are also transmitted to further generations. We highlight that the genotype modulates the expression and reversibility of transgenerational plasticity of dispersal-related traits and its fitness outcomes. Our study thus suggests that genotype-dependent TGP could play an important role in eco-evolutionary dynamics as dispersal determines gene flow and the long-term persistence of natural populations.

In marine species experiencing intense fishing pressures, knowledge of genetic structure and local adaptation represent a critical information to assist sustainable management. In this study, we performed a landscape genomics analysis in the American lobster to investigate the issues pertaining to the consequences of making use of putative adaptive loci to reliably infer population structure and thus more rigorously delineating biological management units in marine exploited species. Toward this end, we genotyped 14,893 single nucleotide polymorphism (SNPs) in 4,190 lobsters sampled across 96 sampling sites distributed along 1000 km in the northwest Atlantic in both Canada and the USA. As typical for most marine species, we observed a weak, albeit highly significant genetic structure. We also found that adaptive genetic variation allows detecting fine-scale population structure not resolved by neutral genetic variation alone. Using the recent genome assembly of the American lobster, we were able to map and annotate several SNPs located in functional genes potentially implicated in adaptive processes such as thermal stress response, salinity tolerance and growth metabolism pathways. Taken together, our study indicates that weak population structure in high gene flow systems can be resolved at various spatial scales, and that putatively adaptive genetic variation can substantially enhance the delineation of biological management units of marine exploited species.

Protection of freshwater fish diversity is a global conservation priority in face of its alarming decline in the last decades. A crucial step to protect freshwater fish diversity is the production of prompt and precise evaluation of community composition and spatial distribution. Metabarcoding of environmental DNA (eDNA metabarcoding) generally surpasses traditional methods for documenting diversity and community composition in aquatic environments. Nevertheless, empirical evidence evaluating how eDNA transportation in water affect community composition and structure via eDNA metabarcoding data remains scarce. Using a brown trout (Salmo trutta) cage transplant experiment in the St. Lawrence River (Canada), a large fluvial system, we tested the detection and relative abundance of species’ eDNA along 15 sampling locations. We detected brown trout eDNA in five localities up to 5,000 m from the cage, but only one sampling location situated 10 m downstream and in the direct line of the cage was affected at the community composition level. This locality showed a relative abundance of brown trout eDNA of 13.1%, while the four others showed a relative abundance under 1.0%. K-means cluster analysis confirmed the impact of brown trout eDNA on community composition by separating this locality from all others. Based on species loading of a redundancy analysis, we showed that this different k-means group was associated with the high relative abundance of brown trout. No evidence of transport effect of brown trout eDNA on fish community composition was observed in any other sampling locations. Together, our results support the view that eDNA metabarcoding can be both a conveyor belt of biodiversity information and a precise tool to study the composition and structure of fish communities in river.

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.

Across a species range, multiple sources of environmental heterogeneity, at both small and large scales, create complex landscapes of selection, which may challenge adaptation, particularly when gene flow is high. One key to multidimensional adaptation may reside in the heterogeneity of recombination along the genome. Structural variants, like chromosomal inversions, reduce recombination, increasing linkage disequilibrium among loci at a potentially massive scale. In this study, we examined how chromosomal inversions shape genetic variation across a species range and ask how their contribution to adaptation in the face of gene flow varies across geographic scales. We sampled the seaweed fly Coelopa frigida along a bioclimatic gradient stretching across 10 degrees of latitude, a salinity gradient, and a range of heterogeneous, patchy habitats. We generated a chromosome-level genome assembly to analyze 1,446 low-coverage whole genomes collected along those gradients. We found several large nonrecombining genomic regions, including putative inversions. In contrast to the collinear regions, inversions and low-recombining regions differentiated populations more strongly, either along an ecogeographic dine or at a fine-grained scale. These genomic regions were associated with environmental factors and adaptive phenotypes, albeit with contrasting patterns. Altogether, our results highlight the importance of recombination in shaping adaptation to environmental heterogeneity at local and large scales.

There is growing evidence that anthropogenic landscapes can strongly influence the evolution of dispersal, particularly through fragmentation, and may drive organisms into an evolutionary trap by suppressing dispersal. However, the influence on dispersal evolution of anthropogenic variation in habitat patch turnover has so far been largely overlooked. In this study, we examined how human‐driven variation in patch persistence affects dispersal rates and distances, determines dispersal‐related phenotypic specialization, and drives neutral genetic structure in spatially structured populations. We addressed this issue in an amphibian, Bombina variegata, using an integrative approach combining capture–recapture modeling, demographic simulation, common garden experiments, and population genetics. B. variegata reproduces in small ponds that occur either in habitat patches that are persistent (i.e., several decades or more), located in riverine environments with negligible human activity, or in patches that are highly temporary (i.e., a few years), created by logging operations in intensively harvested woodland. Our capture–recapture models revealed that natal and breeding dispersal rates and distances were drastically higher in spatially structured populations (SSPs) in logging environments than in riverine SSPs. Population simulations additionally showed that dispersal costs and benefits drive the fate of logging SSPs, which cannot persist without dispersal. The common garden experiments revealed that toadlets reared in laboratory conditions have morphological and behavioral specialization that depends on their habitat of origin. Toadlets from logging SSPs were found to have higher boldness and exploration propensity than those from riverine SSPs, indicating transgenerationally transmitted dispersal syndromes. We also found contrasting patterns of neutral genetic diversity and gene flow in riverine and logging SSPs, with genetic diversity and effective population size con

Gene flow has tremendous importance on local adaptation, by influencing the fate of de novo mutations, maintaining standing genetic variation, and driving adaptive introgression. Furthermore, structural variation as chromosomal rearrangements may facilitate adaptation despite high gene flow. However, our understanding of evolutionary mechanisms impending or favoring local adaptation in the presence of gene flow is still limited to a restricted number of study systems. In this study, we examined how demographic history, shared ancestral polymorphism, and gene flow among glacial lineages contribute to local adaptation to sea conditions in a marine fish, the capelin (Mallotus villosus). We first assembled a 490 Mbp draft genome of M. villosus to map our RAD sequence reads. Then, we used a large dataset of genome-wide single nucleotide polymorphisms (25,904 filtered SNPs) genotyped in 1,310 individuals collected from 31 spawning sites in the northwest Atlantic. We reconstructed the history of divergence among three glacial lineages and showed that they likely diverged from 3.8 to 1.8 MyA and experienced secondary contacts. Within each lineage, our analyses provided evidence for large Ne and high gene flow among spawning sites. Within the NWA lineage, we detected a polymorphic chromosomal rearrangement leading to the occurrence of three haplogroups. Genotype-environment associations revealed molecular signatures of local adaptation to environmental conditions prevailing at spawning sites. Our study also suggests that, both shared polymorphism among lineages, resulting from standing genetic variation or introgression, and chromosomal rearrangements may contribute to local adaptation in the presence of high gene flow.