Detection of environmental and morphological adaptation despite high landscape genetic connectivity in a pest grasshopper (Phaulacridium vittatum)

Widespread species that exhibit both high gene flow and the capacity to occupy heterogeneous environments make excellent models for examining local selection processes along environmental gradients. Here we evaluate the influence of temperature and landscape variables on genetic connectivity and signatures of local adaptation in Phaulacridium vittatum, a widespread agricultural pest grasshopper, endemic to Australia. With sampling across a 900‐km latitudinal gradient, we genotyped 185 P. vittatum from 19 sites at 11,408 single nucleotide polymorphisms (SNPs) using ddRAD sequencing. Despite high gene flow across sites (pairwise F_ST = 0.0003–0.08), landscape genetic resistance modelling identified a positive nonlinear effect of mean annual temperature on genetic connectivity. Urban areas and water bodies had a greater influence on genetic distance among sites than pasture, agricultural areas and forest. Together, F_ST outlier tests and environmental association analysis (EAA) detected 242 unique SNPs under putative selection, with the highest numbers associated with latitude, mean annual temperature and body size. A combination of landscape genetic connectivity analysis together with EAA identified mean annual temperature as a key driver of both neutral gene flow and environmental selection processes. Gene annotation of putatively adaptive SNPs matched with gene functions for olfaction, metabolic detoxification and ultraviolet light shielding. Our results imply that this widespread agricultural pest has the potential to spread and adapt under shifting temperature regimes and land cover change.     

Cunningham's skinks show low genetic connectivity and signatures of divergent selection across its distribution

Establishing corridors of connecting habitat has become a mainstay conservation strategy to maintain gene flow and facilitate climate‐driven range shifts. Yet, little attention has been given to ascertaining the extent to which corridors will benefit philopatric species, which might exhibit localized adaptation. Measures of genetic connectivity and adaptive genetic variation across species’ ranges can help fill this knowledge gap. Here, we characterized the spatial genetic structure of Cunningham's skink (Egernia cunninghami), a philopatric species distributed along Australia's Great Dividing Range, and assessed evidence of localized adaptation. Analysis of 4,274 SNPs from 94 individuals sampled at four localities spanning 500 km and 4° of latitude revealed strong genetic structuring at neutral loci (mean F_ST ± SD = 0.603 ± 0.237) among the localities. Putatively neutral SNPs and those under divergent selection yielded contrasting spatial patterns, with the latter identifying two genetically distinct clusters. Given low genetic connectivity of the four localities, we suggest that the natural movement rate of this species is insufficient to keep pace with spatial shifts to its climate envelope, irrespective of habitat availability. In addition, our finding of localized adaptation highlights the risk of outbreeding depression should the translocation of individuals be adopted as a conservation management strategy.     

Genome‐wide single‐generation signatures of local selection in the panmictic European eel

Next‐generation sequencing and the collection of genome‐wide data allow identifying adaptive variation and footprints of directional selection. Using a large SNP data set from 259 RAD‐sequenced European eel individuals (glass eels) from eight locations between 34 and 64^oN, we examined the patterns of genome‐wide genetic diversity across locations. We tested for local selection by searching for increased population differentiation using F_ST‐based outlier tests and by testing for significant associations between allele frequencies and environmental variables. The overall low genetic differentiation found (F_ST = 0.0007) indicates that most of the genome is homogenized by gene flow, providing further evidence for genomic panmixia in the European eel. The lack of genetic substructuring was consistent at both nuclear and mitochondrial SNPs. Using an extensive number of diagnostic SNPs, results showed a low occurrence of hybrids between European and American eel, mainly limited to Iceland (5.9%), although individuals with signatures of introgression several generations back in time were found in mainland Europe. Despite panmixia, a small set of SNPs showed high genetic differentiation consistent with single‐generation signatures of spatially varying selection acting on glass eels. After screening 50 354 SNPs, a total of 754 potentially locally selected SNPs were identified. Candidate genes for local selection constituted a wide array of functions, including calcium signalling, neuroactive ligand–receptor interaction and circadian rhythm. Remarkably, one of the candidate genes identified is PERIOD, possibly related to differences in local photoperiod associated with the >30° difference in latitude between locations. Genes under selection were spread across the genome, and there were no large regions of increased differentiation as expected when selection occurs within just a single generation due to panmixia. This supports the conclusion that most of the genome is homogenized by gene flow that removes any effects of diversifying selection from each new generation.     

Water availability drives signatures of local adaptation in whitebark pine (Pinus albicaulis Engelm.) across fine spatial scales of the Lake Tahoe Basin,USA

Patterns of local adaptation at fine spatial scales are central to understanding how evolution proceeds, and are essential to the effective management of economically and ecologically important forest tree species. Here, we employ single and multilocus analyses of genetic data (n = 116 231 SNPs) to describe signatures of fine‐scale adaptation within eight whitebark pine (Pinus albicaulis Engelm.) populations across the local extent of the environmentally heterogeneous Lake Tahoe Basin, USA. We show that despite highly shared genetic variation (F_ST = 0.0069), there is strong evidence for adaptation to the rain shadow experienced across the eastern Sierra Nevada. Specifically, we build upon evidence from a common garden study and find that allele frequencies of loci associated with four phenotypes (mean = 236 SNPs), 18 environmental variables (mean = 99 SNPs), and those detected through genetic differentiation (n = 110 SNPs) exhibit significantly higher signals of selection (covariance of allele frequencies) than could be expected to arise, given the data. We also provide evidence that this covariance tracks environmental measures related to soil water availability through subtle allele frequency shifts across populations. Our results replicate empirical support for theoretical expectations of local adaptation for populations exhibiting strong gene flow and high selective pressures and suggest that ongoing adaptation of many P. albicaulis populations within the Lake Tahoe Basin will not be constrained by the lack of genetic variation. Even so, some populations exhibit low levels of heritability for the traits presumed to be related to fitness. These instances could be used to prioritize management to maintain adaptive potential. Overall, we suggest that established practices regarding whitebark pine conservation be maintained, with the additional context of fine‐scale adaptation.     

Selection and localised genetic structure in the threatened Manauense Harlequin Frog (Bufonidae: Atelopus manauensis)

Knowledge of genome-wide variation and the processes influencing gene flow are critical to managing threatened species. Here, we characterise genetic diversity and the environmental features associated with connectivity for a narrowly distributed and threatened Amazonian frog, Atelopus manauensis. We sampled 94 individuals throughout the upper, middle and lower courses from each of the five major rivers covering the species’ known geographic range and genotyped each individual at 3859 single nucleotide polymorphisms (SNPs). Genetic variation was significantly subdivided into six groups, each mostly containing individuals sampled within the same major river system. The genetic distances among these groups increased with geographic distance, and open forests and the extremities of the altitude gradient were associated with less genetic connectivity. Using F_ST outlier approaches and environmental association analyses, we identified SNPs indicative of localised adaptation, with 28 SNPs significantly associated with forest biomass and altitude. Evidence of divergent selection among the six genetic clusters suggests the presence of six Evolutionary Significant Units (ESUs). Overall, the ESUs were characterized by low contemporary effective population sizes (N_E?<?100) suggesting that genetic variation will be lost by random genetic drift. We demonstrate surprisingly high levels of divergence across the limited distribution of A. manauensis and suggest that each of the six adaptively divergent lineages be considered in conservation planning.

     

Genome-wide SNPs detect fine-scale genetic structure in threatened populations of squirrel glider Petaurus norfolcensis

Australian arboreal mammals are experiencing significant population declines, particularly due to land clearing and resulting habitat fragmentation. The squirrel glider, Petaurus norfolcensis, is a threatened species in New South Wales, with a stronghold population in the Lake Macquarie Local Government Area (LGA) where fragmentation due to urbanization is an ongoing problem for the species conservation. Here we report on the use of squirrel glider mitochondrial (385 bp cytochrome b gene, 70 individuals) and nuclear DNA (6,834 SNPs, 87 individuals) markers to assess their population genetic structure and connectivity across 14 locations sampled in the Lake Macquarie LGA. The mitochondrial DNA sequences detected evidence of a historical genetic bottleneck, while the genome-wide SNPs detected significant population structure in the Lake Macquarie squirrel glider populations at scales as fine as one kilometer. There was no evidence of inbreeding within patches, however there were clear effects of habitat fragmentation and biogeographical barriers on gene flow. A least cost path analysis identified thin linear corridors that have high priority for conservation. These areas should be protected to avoid further isolation of squirrel glider populations and the loss of genetic diversity through genetic drift.

     

Local adaptation at range edges: comparing elevation and latitudinal gradients

Local adaptation at range edges influences species’ distributions and how they respond to environmental change. However, the factors that affect adaptation, including gene flow and local selection pressures, are likely to vary across different types of range edge. We performed a reciprocal transplant experiment to investigate local adaptation in populations of Plantago lanceolata and P. major from central locations in their European range and from their latitudinal and elevation range edges (in northern Scandinavia and Swiss Alps, respectively). We also characterized patterns of genetic diversity and differentiation in populations using molecular markers. Range‐centre plants of P. major were adapted to conditions at the range centre, but performed similarly to range‐edge plants when grown at the range edges. There was no evidence for local adaptation when comparing central and edge populations of P. lanceolata. However, plants of both species from high elevation were locally adapted when compared with plants from high latitude, although the reverse was not true. This asymmetry was associated with greater genetic diversity and less genetic differentiation over the elevation gradient than over the latitudinal gradient. Our results suggest that adaptation in some range‐edge populations could increase their performance following climate change. However, responses are likely to differ along elevation and latitudinal gradients, with adaptation more likely at high‐elevation. Furthermore, based upon these results, we suggest that gene flow is unlikely to constrain adaptation in range‐edge populations of these species.     

The number of breeders explains genetic connectivity in an endangered bird

Connectivity is central to ecology and evolution as it focuses on the movement of individuals or genes across landscapes. Genetic connectivity approaches aim to understand gene flow but often estimate it indirectly based on metrics of genetic differentiation, which can also be affected by other evolutionary forces such as genetic drift. Gene flow and genetic drift are driven by separate ecological mechanisms with potentially differing effects on genetic differentiation and interpretations of genetic connectivity. The ecological mechanisms contributing to gene flow and genetic drift are primarily effective dispersal, or movement followed by successful reproduction, and the number of breeders in a local population, N_b, respectively. Yet, rarely are these ecological mechanisms and genetic connectivity measured simultaneously across landscapes. We examine the roles of effective dispersal and N_b on genetic connectivity across the entire range of the endangered snail kite (Rostrhamus sociabilis plumbeus), between 2006–2015. We find that both N_b and effective dispersal are important predictors of genetic connectivity across this landscape, but that N_b has a 3 × stronger effect on genetic connectivity. Furthermore, N_b is positively correlated with heterozygosity and allelic richness within patches, suggesting a potentially important role of genetic drift, in addition to gene flow, on genetic connectivity. These results emphasize that conservation efforts should focus on not only between‐patch processes of movement but also within‐patch processes regarding habitat quality and local population size for increasing genetic connectivity.     

Conservation genomics of anadromous Atlantic salmon across its North American range: outlier loci identify the same patterns of population structure as neutral loci

Anadromous Atlantic salmon (Salmo salar) is a species of major conservation and management concern in North America, where population abundance has been declining over the past 30 years. Effective conservation actions require the delineation of conservation units to appropriately reflect the spatial scale of intraspecific variation and local adaptation. Towards this goal, we used the most comprehensive genetic and genomic database for Atlantic salmon to date, covering the entire North American range of the species. The database included microsatellite data from 9142 individuals from 149 sampling locations and data from a medium‐density SNP array providing genotypes for >3000 SNPs for 50 sampling locations. We used neutral and putatively selected loci to integrate adaptive information in the definition of conservation units. Bayesian clustering with the microsatellite data set and with neutral SNPs identified regional groupings largely consistent with previously published regional assessments. The use of outlier SNPs did not result in major differences in the regional groupings, suggesting that neutral markers can reflect the geographic scale of local adaptation despite not being under selection. We also performed assignment tests to compare power obtained from microsatellites, neutral SNPs and outlier SNPs. Using SNP data substantially improved power compared to microsatellites, and an assignment success of 97% to the population of origin and of 100% to the region of origin was achieved when all SNP loci were used. Using outlier SNPs only resulted in minor improvements to assignment success to the population of origin but improved regional assignment. We discuss the implications of these new genetic resources for the conservation and management of Atlantic salmon in North America.     

Divergent and linked selection shape patterns of genomic differentiation between European and North American Atlantic salmon (Salmo salar)

As populations diverge many processes can shape genomic patterns of differentiation. Regions of high differentiation can arise due to divergent selection acting on selected loci, genetic hitchhiking of nearby loci, or through repeated selection against deleterious alleles (linked background selection); this divergence may then be further elevated in regions of reduced recombination. Atlantic salmon (Salmo salar) from Europe and North America diverged >600,000 years ago and despite some evidence of secondary contact, the majority of genetic data indicate substantial divergence between lineages. This deep divergence with potential gene flow provides an opportunity to investigate the role of different mechanisms that shape the genomic landscape during early speciation. Here, using 184,295 single nucleotide polymorphisms (SNPs) and 80 populations, we investigate the genomic landscape of differentiation across the Atlantic Ocean with a focus on highly differentiated regions and the processes shaping them. We found evidence of high (mean F_ST = 0.26) and heterogeneous genomic differentiation between continents. Genomic regions associated with high trans‐Atlantic differentiation ranged in size from single loci (SNPs) within important genes to large regions (1–3 Mbp ) on four chromosomes (Ssa06, Ssa13, Ssa16 and Ssa19). These regions showed signatures consistent with selection, including high linkage disequilibrium, despite no significant reduction in recombination. Genes and functional enrichment of processes associated with differentiated regions may highlight continental differences in ocean navigation and parasite resistance. Our results provide insight into potential mechanisms underlying differences between continents, and evidence of near‐fixed and potentially adaptive trans‐Atlantic differences concurrent with a background of high genome‐wide differentiation supports subspecies designation in Atlantic salmon.     

Ocean circulation model predicts high genetic structure observed in a long‐lived pelagic developer

Understanding the movement of genes and individuals across marine seascapes is a long‐standing challenge in marine ecology and can inform our understanding of local adaptation, the persistence and movement of populations, and the spatial scale of effective management. Patterns of gene flow in the ocean are often inferred based on population genetic analyses coupled with knowledge of species' dispersive life histories. However, genetic structure is the result of time‐integrated processes and may not capture present‐day connectivity between populations. Here, we use a high‐resolution oceanographic circulation model to predict larval dispersal along the complex coastline of western Canada that includes the transition between two well‐studied zoogeographic provinces. We simulate dispersal in a benthic sea star with a 6–10 week pelagic larval phase and test predictions of this model against previously observed genetic structure including a strong phylogeographic break within the zoogeographical transition zone. We also test predictions with new genetic sampling in a site within the phylogeographic break. We find that the coupled genetic and circulation model predicts the high degree of genetic structure observed in this species, despite its long pelagic duration. High genetic structure on this complex coastline can thus be explained through ocean circulation patterns, which tend to retain passive larvae within 20–50 km of their parents, suggesting a necessity for close‐knit design of Marine Protected Area networks.     

Distance,elevation and environment as drivers of diversity and divergence in bumble bees across latitude and altitude

Identifying drivers of dispersal limitation and genetic differentiation is a key goal in biogeography. We examine patterns of population connectivity and genetic diversity using restriction site‐associated DNA sequencing (RADseq) in two bumble bee species, Bombus vosnesenskii and Bombus bifarius, across latitude and altitude in mountain ranges from California, Oregon and Washington, U.S.A. Bombus vosnesenskii, which occurs across a broader elevational range at most latitudes, exhibits little population structure while B. bifarius, which occupies a relatively narrow higher elevation niche across most latitudes, exhibits much stronger population differentiation, although gene flow in both species is best explained by isolation with environmental niche resistance. A relationship between elevational habitat breadth and genetic diversity is also apparent, with B. vosnesenskii exhibiting relatively consistent levels of genetic diversity across its range, while B. bifarius has reduced genetic diversity at low latitudes, where it is restricted to high‐elevation habitat. The results of this study highlight the importance of the intersect between elevational range and habitat suitability in influencing population connectivity and suggest that future climate warming will have a fragmenting effect even on populations that are presently well connected, as they track their thermal niches upward in montane systems.     

Spatial genetic analysis of two polyploid macrophytes reveals high connectivity in a modified wetland

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Adaptive genetic variation distinguishes Chilean blue mussels (Mytilus chilensis) from different marine environments

Chilean mussel populations have been thought to be panmictic with limited genetic structure. Genotyping‐by‐sequencing approaches have enabled investigation of genomewide variation that may better distinguish populations that have evolved in different environments. We investigated neutral and adaptive genetic variation in Mytilus from six locations in southern Chile with 1240 SNPs obtained with RAD‐seq. Differentiation among locations with 891 neutral SNPs was low (F_ST = 0.005). Higher differentiation was obtained with a panel of 58 putative outlier SNPs (F_ST = 0.114) indicating the potential for local adaptation. This panel identified clusters of genetically related individuals and demonstrated that much of the differentiation (~92%) could be attributed to the three major regions and environments: extreme conditions in Patagonia, inner bay influenced by aquaculture (Reloncaví), and outer bay (Chiloé Island). Patagonia samples were most distinct, but additional analysis carried out excluding this collection also revealed adaptive divergence between inner and outer bay samples. The four locations within Reloncaví area were most similar with all panels of markers, likely due to similar environments, high gene flow by aquaculture practices, and low geographical distance. Our results and the SNP markers developed will be a powerful tool supporting management and programs of this harvested species.     

Genomic islands of divergence linked to ecotypic variation in sockeye salmon

Regions of the genome displaying elevated differentiation (genomic islands of divergence) are thought to play an important role in local adaptation, especially in populations experiencing high gene flow. However, the characteristics of these islands as well as the functional significance of genes located within them remain largely unknown. Here, we used data from thousands of SNPs aligned to a linkage map to investigate genomic islands of divergence in three ecotypes of sockeye salmon (Oncorhynchus nerka) from a single drainage in southwestern Alaska. We found ten islands displaying high differentiation among ecotypes. Conversely, neutral structure observed throughout the rest of the genome was low and not partitioned by ecotype. One island on linkage group So13 was particularly large and contained six SNPs with F_ST > 0.14 (average F_ST of neutral SNPs = 0.01). Functional annotation revealed that the peak of this island contained a nonsynonymous mutation in a gene involved in growth in other species (TULP4). The islands that we discovered were relatively small (80–402 Kb), loci found in islands did not show reduced levels of diversity, and loci in islands displayed slightly elevated linkage disequilibrium. These attributes suggest that the islands discovered here were likely generated by divergence hitchhiking; however, we cannot rule out the possibility that other mechanisms may have produced them. Our results suggest that islands of divergence serve an important role in local adaptation with gene flow and represent a significant advance towards understanding the genetic basis of ecotypic differentiation.     

From global to local genetic structuring in the red gorgonian Paramuricea clavata: the interplay between oceanographic conditions and limited larval dispersal

Defining the scale of connectivity among marine populations and identifying the barriers to gene flow are tasks of fundamental importance for understanding the genetic structure of populations and for the design of marine reserves. Here, we investigated the population genetic structure at three spatial scales of the red gorgonian Paramuricea clavata (Cnidaria, Octocorallia), a key species dwelling in the coralligenous assemblages of the Mediterranean Sea. Colonies of P. clavata were collected from 39 locations across the Mediterranean Sea from Morocco to Turkey and analysed using microsatellite loci. Within three regions (Medes, Marseille and North Corsica), sampling was obtained from multiple locations and at different depths. Three different approaches (measures of genetic differentiation, Bayesian clustering and spatially explicit maximum‐difference algorithm) were used to determine the pattern of genetic structure. We identified genetic breaks in the spatial distribution of genetic diversity, which were concordant with oceanographic conditions in the Mediterranean Sea. We revealed a high level of genetic differentiation among populations and a pattern of isolation by distance across the studied area and within the three regions, underlining short effective larval dispersal in this species. We observed genetic differentiation among populations in the same locality dwelling at different depths, which may be explained by local oceanographic conditions and which may allow a process of local adaptation of the populations to their environment. We discuss the implications of our results for the conservation of the species, which is exposed to various threats.     

RAD genotyping reveals fine‐scale genetic structuring and provides powerful population assignment in a widely distributed marine species,the American lobster (Homarus americanus)

Deciphering genetic structure and inferring connectivity in marine species have been challenging due to weak genetic differentiation and limited resolution offered by traditional genotypic methods. The main goal of this study was to assess how a population genomics framework could help delineate the genetic structure of the American lobster (Homarus americanus) throughout much of the species’ range and increase the assignment success of individuals to their location of origin. We genotyped 10 156 filtered SNPs using RAD sequencing to delineate genetic structure and perform population assignment for 586 American lobsters collected in 17 locations distributed across a large portion of the species’ natural distribution range. Our results revealed the existence of a hierarchical genetic structure, first separating lobsters from the northern and southern part of the range (F_CT = 0.0011; P‐value = 0.0002) and then revealing a total of 11 genetically distinguishable populations (mean F_ST = 0.00185; CI: 0.0007–0.0021, P‐value < 0.0002), providing strong evidence for weak, albeit fine‐scale population structuring within each region. A resampling procedure showed that assignment success was highest with a subset of 3000 SNPs having the highest F_ST. Applying Anderson's (Molecular Ecology Resources, 2010, 10, 701) method to avoid ‘high‐grading bias’, 94.2% and 80.8% of individuals were correctly assigned to their region and location of origin, respectively. Lastly, we showed that assignment success was positively associated with sample size. These results demonstrate that using a large number of SNPs improves fine‐scale population structure delineation and population assignment success in a context of weak genetic structure. We discuss the implications of these findings for the conservation and management of highly connected marine species, particularly regarding the geographic scale of demographic independence.     

Genetic isolation of the sorghum plant bug <Emphasis Type="Italic">Stenotus rubrovittatus</Emphasis> (Hemiptera: Miridae) in Fukushima and Ibaraki prefectures

Population subdivision and connectivity within a distribution range are important factors to consider in the development of a management strategy to control widespread pest species. Damage by sorghum plant bug, Stenotus rubrovittatus (Matsumura), has rapidly spread across Japan over the last 10 years. To characterize the fine-scale population structure of this bug and investigate the boundaries of genetic isolation, we analyzed the population structure of 21 local populations within a 72 km × 200 km area around Fukushima and Ibaraki prefectures. Polymorphism of six microsatellite markers implied that S. rubrovittatus in the study area was divided into northern and southern genetic groups segregated by the 37.3°N line of latitude. The boundary between the two groups, defined by microsatellites, was almost consistent with the range limit of one mitochondrial lineage of the same species. Our result indicated that isolation between these two genetic groups was mediated by historical and ecological origins, and was maintained during the last 10 years when there were rapid outbreaks of this species on rice within the study area.     

The population genomic signature of environmental association and gene flow in an ecologically divergent tree species Metrosideros polymorpha (Myrtaceae)

Genomewide markers enable us to study genetic differentiation within a species and the factors underlying it at a much higher resolution than before, which advances our understanding of adaptation in organisms. We investigated genomic divergence in Metrosideros polymorpha, a woody species that occupies a wide range of ecological habitats across the Hawaiian Islands and shows remarkable phenotypic variation. Using 1659 single nucleotide polymorphism (SNP) markers annotated with the genome assembly, we examined the population genetic structure and demographic history of nine populations across five elevations and two ages of substrates on Mauna Loa, the island of Hawaii. The nine populations were differentiated into two genetic clusters distributed on the lower and higher elevations and were largely admixed on the middle elevation. Demographic modelling revealed that the two genetic clusters have been maintained in the face of gene flow, and the effective population size of the high‐altitude cluster was much smaller. A F_ST‐based outlier search among the 1659 SNPs revealed that 34 SNPs (2.05%) were likely to be under divergent selection and the allele frequencies of 21 of them were associated with environmental changes along elevations, such as temperature and precipitation. This study shows a genomic mosaic of M. polymorpha, in which contrasting divergence patterns were found. While most genomic polymorphisms were shared among populations, a small fraction of the genome was significantly differentiated between populations in diverse environments and could be responsible for the dramatic adaptation to a wide range of environments.     

Shared ancestral polymorphisms and chromosomal rearrangements as potential drivers of local adaptation in a marine fish

Gene flow has tremendous importance for 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 the evolutionary mechanisms impending or favouring 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 data set 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 probably diverged from 3.8 to 1.8 million years ago and experienced secondary contacts. Within each lineage, our analyses provided evidence for large N_e and high gene flow among spawning sites. Within the Northwest Atlantic 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 polymorphisms among lineages, resulting from standing genetic variation or introgression, and chromosomal rearrangements may contribute to local adaptation in the presence of high gene flow.