Genetic analysis of differentiation among breeding ponds reveals a candidate gene for local adaptation in Rana arvalis

One of the main questions in evolutionary and conservation biology is how geographical and environmental features of the landscape shape neutral and adaptive genetic variation in natural populations. The identification of genomic polymorphisms that account for adaptive variation can aid in finding candidate loci for local adaptation. Consequently, a comparison of spatial patterns in neutral markers and loci under selection may help disentangle the effects of gene flow, genetic drift and selection at the landscape scale. Many amphibians breed in wetlands, which differ in environmental conditions and in the degree of isolation, enhancing the potential for local adaptation. We used microsatellite markers to measure genetic differentiation among 17 local populations of Rana arvalis breeding in a network of wetlands. We found that locus RC08604 deviated from neutral expectations, suggesting that it is a good candidate for directional selection. We used a genetic network analysis to show that the allele distribution in this locus is correlated with habitat characteristics, whereas this was not the case at neutral markers that displayed a different allele distribution and population network in the study area. The graph approach illustrated the genomic heterogeneity (neutral loci vs. the candidate locus for directional selection) of gene exchange and genetic divergence among populations under directional selection. Limited gene flow between wetlands was only observed at the candidate genomic region under directional selection. RC08604 is partially located inside an up‐regulated thyroid‐hormone receptor (TRβ) gene coordinating the expression of other genes during metamorphosis and appears to be linked with variation in larval life‐history traits found among R. arvalis populations. We suggest that directional selection on genes coding larval life‐history traits is strong enough to maintain the divergence in these genomic regions, reducing the effective recombination of locally adapted alleles but not in other regions of the genome. Integrating this knowledge into conservation plans at the landscape scale will improve the design of management strategies to preserve adaptive genetic diversity in wetland networks.     

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.     

Evidence for morphological and adaptive genetic divergence between lake and stream habitats in European minnows (Phoxinus phoxinus, Cyprinidae)

Natural selection drives local adaptation, potentially even at small temporal and spatial scales. As a result, adaptive genetic and phenotypic divergence can occur among populations living in different habitats. We investigated patterns of differentiation between contrasting lake and stream habitats in the cyprinid fish European minnow (Phoxinus phoxinus) at both the morphological and genomic levels using geometric morphometrics and AFLP markers, respectively. We also used a spatial correlative approach to identify AFLP loci associated with environmental variables representing potential selective forces responsible for adaptation to divergent habitats. Our results identified different morphologies between lakes and streams, with lake fish presenting a deeper body and caudal peduncle compared to stream fish. Body shape variation conformed to a priori predictions concerning biomechanics and swimming performance in lakes vs. streams. Moreover, morphological differentiation was found to be associated with several environmental variables, which could impose selection on body and caudal peduncle shape. We found adaptive genetic divergence between these contrasting habitats in the form of 'outlier' loci (2.9%) whose genetic divergence exceeded neutral expectations. We also detected additional loci (6.6%) not associated with habitat type (lake vs. stream), but contributing to genetic divergence between populations. Specific environmental variables related to trophic dynamics, landscape topography and geography were associated with several neutral and outlier loci. These results provide new insights into the morphological divergence and genetic basis of adaptation to differentiated habitats.     

Parallel and nonparallel genome‐wide divergence among replicate population pairs of freshwater and anadromous Atlantic salmon

Little is known about the genetic basis differentiating resident and anadromous forms found in many salmonid species. Using a medium‐density SNP array, we documented genomic diversity and divergence at 2336 genetically mapped loci among three pairs of North American anadromous and freshwater Atlantic salmon populations. Our results show that across the genome, freshwater populations have lower diversity and a smaller proportion of private polymorphism relative to anadromous populations. Moreover, differentiation was more pronounced among freshwater than among anadromous populations at multiple spatial scales, suggesting a large effect of genetic drift in these isolated freshwater populations. Using nonhierarchical and hierarchical genome scans, we identified hundreds of markers spread across the genome that are potentially under divergent selection between anadromous and freshwater populations, but few outlier loci were repeatedly found in all three freshwater–anadromous comparisons. Similarly, a sliding window analysis revealed numerous regions of high divergence that were nonparallel among the three comparisons. These last results show little evidence for the parallel evolution of alleles selected for in freshwater populations, but suggest nonparallel adaptive divergence at many loci of small effects distributed through the genome. Overall, this study emphasizes the important role of genetic drift in driving genome‐wide reduction in diversity and divergence in freshwater Atlantic salmon populations and suggests a complex multigenic basis of adaptation to resident and anadromous strategies with little parallelism.     

Low but significant genetic differentiation underlies biologically meaningful phenotypic divergence in a large Atlantic salmon population

Despite decades of research assessing the genetic structure of natural populations, the biological meaning of low yet significant genetic divergence often remains unclear due to a lack of associated phenotypic and ecological information. At the same time, structured populations with low genetic divergence and overlapping boundaries can potentially provide excellent models to study adaptation and reproductive isolation in cases where high‐resolution genetic markers and relevant phenotypic and life history information are available. Here, we combined single nucleotide polymorphism (SNP)‐based population inference with extensive phenotypic and life history data to identify potential biological mechanisms driving fine‐scale subpopulation differentiation in Atlantic salmon (Salmo salar) from the Teno River, a major salmon river in Europe. Two sympatrically occurring subpopulations had low but significant genetic differentiation (F_ST = 0.018) and displayed marked differences in the distribution of life history strategies, including variation in juvenile growth rate, age at maturity and size within age classes. Large, late‐maturing individuals were virtually absent from one of the two subpopulations, and there were significant differences in juvenile growth rates and size at age after oceanic migration between individuals in the respective subpopulations. Our findings suggest that different evolutionary processes affect each subpopulation and that hybridization and subsequent selection may maintain low genetic differentiation without hindering adaptive divergence.     

Landscape genetics and hierarchical genetic structure in Atlantic salmon: the interaction of gene flow and local adaptation

Disentangling evolutionary forces that may interact to determine the patterns of genetic differentiation within and among wild populations is a major challenge in evolutionary biology. The objective of this study was to assess the genetic structure and the potential influence of several ecological variables on the extent of genetic differentiation at multiple spatial scales in a widely distributed species, the Atlantic salmon, Salmo salar . A total of 2775 anadromous fish were sampled from 51 rivers along the North American Atlantic coast and were genotyped using 13 microsatellites. A Bayesian analysis clustered these populations into seven genetically and geographically distinct groups, characterized by different environmental and ecological factors, mainly temperature. These groups were also characterized by different extent of genetic differentiation among populations. Dispersal was relatively high and of the same magnitude within compared to among regional groups, which contrasted with the maintenance of a regional genetic structure. However, genetic differentiation was lower among populations exchanging similar rates of local as opposed to inter-regional migrants, over the same geographical scale. This raised the hypothesis that gene flow could be constrained by local adaptation at the regional scale. Both coastal distance and temperature regime were found to influence the observed genetic structure according to landscape genetic analyses. The influence of other factors such as latitude, river length and altitude, migration tactic, and stocking was not significant at any spatial scale. Overall, these results suggested that the interaction between gene flow and thermal regime adaptation mainly explained the hierarchical genetic structure observed among Atlantic salmon populations.     

Determinants of hierarchical genetic structure in Atlantic salmon populations: environmental factors vs. anthropogenic influences

Disentangling the effects of natural environmental features and anthropogenic factors on the genetic structure of endangered populations is an important challenge for conservation biology. Here, we investigated the combined influences of major environmental features and stocking with non‐native fish on the genetic structure and local adaptation of Atlantic salmon (Salmo salar) populations. We used 17 microsatellite loci to genotype 975 individuals originating from 34 French rivers. Bayesian analyses revealed a hierarchical genetic structure into five geographically distinct clusters. Coastal distance, geological substrate and river length were strong predictors of population structure. Gene flow was higher among rivers with similar geologies, suggesting local adaptation to geological substrate. The effect of river length was mainly owing to one highly differentiated population that has the farthest spawning grounds off the river mouth (up to 900 km) and the largest fish, suggesting local adaptation to river length. We detected high levels of admixture in stocked populations but also in neighbouring ones, implying large‐scale impacts of stocking through dispersal of non‐native individuals. However, we found relatively few admixed individuals suggesting a lower fitness of stocked fish and/or some reproductive isolation between wild and stocked individuals. When excluding stocked populations, genetic structure increased as did its correlation with environmental factors. This study overall indicates that geological substrate and river length are major environmental factors influencing gene flow and potential local adaptation among Atlantic salmon populations but that stocking with non‐native individuals may ultimately disrupt these natural patterns of gene flow among locally adapted populations.     

Environmental adaptation in Chinook salmon (Oncorhynchus tshawytscha) throughout their North American range

Landscape genomics is a rapidly growing field with recent advances in both genotyping efficiency and statistical analyses that provide insight towards local adaptation of populations under varying environmental and selective pressure. Chinook salmon (Oncorhynchus tshawytscha) are a broadly distributed Pacific salmon species, occupying a diversity of habitats throughout the northeastern Pacific with pronounced variation in environmental and climate features but little is understood regarding local adaptation in this species. We used a multivariate method, redundancy analysis (RDA), to identify polygenic correlations between 19 703 SNP loci and a suite of environmental variables in 46 collections of Chinook salmon (1956 total individuals) distributed throughout much of its North American range. Models in RDA were conducted on both rangewide and regional scales by hierarchical partitioning of the populations into three distinct genetic lineages. Our results indicate that between 5.8 and 21.8% of genomic variation can be accounted for by environmental features, and 566 putatively adaptive loci were identified as targets of environmental adaptation. The most influential drivers of adaptive divergence included precipitation in the driest quarter of the year (Rangewide and North Coastal Lineage, anova P = 0.002 and 0.01, respectively), precipitation in the wettest quarter of the year (Interior Columbia River Stream‐Type Lineage, anova P = 0.03), variation in mean diurnal range in temperature (South Coastal Lineage, anova P = 0.005), and migration distance (Rangewide, anova P = 0.001). Our results indicate that environmental features are strong drivers of adaptive genomic divergence in this species, and provide a foundation to investigate how Chinook salmon might respond to global environmental change.     

Oxygen concentration drives local adaptation in the greenlip abalone (Haliotis laevigata)

Understanding adaptation has become one of the major biological questions especially in the light of rapid environmental changes induced by climate change. Ocean temperatures are rising which triggers massive changes in water chemistry and thereby alters the living environment of all marine organisms. Studying adaptation, however, can be tricky because spatial genetic patterns might also occur due to random effects, for example, genetic drift. Genetic drift is reduced in very large and well‐connected populations, such as in broadcast marine spawning organisms. Here, spatial genetic divergence is likely to be produced by selection. In this issue of Molecular Ecology, Sandoval‐Castillo et al. (2018) investigated patterns of spatial genetic divergence and their association with environmental factors in the greenlip abalone (Haliotis laevigata). This commercially important species of mollusc is a broadcast spawner with large population sizes, rendering genetic drift an unlikely factor in the genetic divergence of wild populations. Sandoval‐Castillo et al. (2018) used a ddRAD genomic approach to test for genetic divergence between sampled populations while also measuring different environmental factors, for example, water temperature and oxygen content. The majority of identified SNPs was putatively neutral and showed only low levels of genetic divergence between field sites. However, 323 candidate adaptive markers were identified that clearly separated the individuals into five different clusters. These genetic clusters correlated with environmental clusters mainly determined by water temperature and (correlated) oxygen concentration. Gene annotation of the candidate SNPs revealed a large proportion of loci being involved in biological processes influenced by oxygen availability. The study by Sandoval‐Castillo et al. (2018) in this issue of Molecular Ecology exemplifies the benefits of combining genomic studies with ecological data. It is a great starting point for more detailed (gene function, physiology) as well as broader (biodiversity) investigations that might help us to better understand adaptation and predict ecosystems' resilience and resistance to environmental disturbances. In addition, this information can be applied to implement optimal conservation regime policies and sustainable harvesting strategies, hopefully protecting biodiversity as well as commercial interests in marine life.     

Chromosome polymorphisms track trans‐Atlantic divergence and secondary contact in Atlantic salmon

Pleistocene glaciations drove repeated range contractions and expansions shaping contemporary intraspecific diversity. Atlantic salmon (Salmo salar) in the western and eastern Atlantic diverged >600,000 years before present, with the two lineages isolated in different southern refugia during glacial maxima, driving trans‐Atlantic genomic and karyotypic divergence. Here, we investigate the genomic consequences of glacial isolation and trans‐Atlantic secondary contact using 108,870 single nucleotide polymorphisms genotyped in 80 North American and European populations. Throughout North America, we identified extensive interindividual variation and discrete linkage blocks within and between chromosomes with known trans‐Atlantic differences in rearrangements: Ssa01/Ssa23 translocation and Ssa08/Ssa29 fusion. Spatial genetic analyses suggest independence of rearrangements, with Ssa01/Ssa23 showing high European introgression (>50%) in northern populations indicative of post‐glacial trans‐Atlantic secondary contact, contrasting with low European ancestry genome‐wide (3%). Ssa08/Ssa29 showed greater intrapopulation diversity, suggesting a derived chromosome fusion polymorphism that evolved within North America. Evidence of potential selection on both genomic regions suggests that the adaptive role of rearrangements warrants further investigation in Atlantic salmon. Our study highlights how Pleistocene glaciations can influence large‐scale intraspecific variation in genomic architecture of northern species.     

Machine‐learning‐based detection of adaptive divergence of the stream mayfly Ephemera strigata populations

Adaptive divergence is a key mechanism shaping the genetic variation of natural populations. A central question linking ecology with evolutionary biology is how spatial environmental heterogeneity can lead to adaptive divergence among local populations within a species. In this study, using a genome scan approach to detect candidate loci under selection, we examined adaptive divergence of the stream mayfly Ephemera strigata in the Natori River Basin in northeastern Japan. We applied a new machine‐learning method (i.e., random forest) besides traditional distance‐based redundancy analysis (dbRDA) to examine relationships between environmental factors and adaptive divergence at non‐neutral loci. Spatial autocorrelation analysis based on neutral loci was employed to examine the dispersal ability of this species. We conclude the following: (a) E. strigata show altitudinal adaptive divergence among the populations in the Natori River Basin; (b) random forest showed higher resolution for detecting adaptive divergence than traditional statistical analysis; and (c) separating all markers into neutral and non‐neutral loci could provide full insight into parameters such as genetic diversity, local adaptation, and dispersal ability.     

Population‐genomic approach reveals adaptive floral divergence in discrete populations of a hawk moth‐pollinated violet

Local adaptation to contrasting biotic or abiotic environments is an important evolutionary step that presumably precedes floral diversification at the species level, yet few studies have demonstrated the adaptive nature of intraspecific floral divergence in wild plant populations. We combine a population‐genomic approach with phenotypic information on floral traits to examine whether the differentiation in metric floral traits exhibited by 14 populations of the southern Spanish hawk moth‐pollinated violet Viola cazorlensis reflects adaptive divergence. Screening of many amplified fragment length polymorphism (AFLP) loci using a multiple‐marker‐based neutrality test identified nine outlier loci (2.6% of the total) that departed from neutral expectations and were potentially under selection. Generalized analysis of molecular variance revealed significant relationships between genetic distance and population divergence in three floral traits when genetic distance was based on outlier loci, but not when it was based on neutral ones. Population means of floral traits were closely correlated with population scores on the first principal coordinate axis of the genetic distance matrix using outlier loci, and with the allelic frequencies of four of the outlier loci. Results strongly support the adaptive nature of intraspecific floral divergence exhibited by V. cazorlensis and illustrate the potential of genome scans to identify instances of adaptive divergence when used in combination with phenotypic information.     

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.     

Chromosomal fusion and life history‐associated genomic variation contribute to within‐river local adaptation of Atlantic salmon

Chromosomal inversions have been implicated in facilitating adaptation in the face of high levels of gene flow, but whether chromosomal fusions also have similar potential remains poorly understood. Atlantic salmon are usually characterized by population structure at multiple spatial scales; however, this is not the case for tributaries of the Miramichi River in North America. To resolve genetic relationships between populations in this system and the potential for known chromosomal fusions to contribute to adaptation, we genotyped 728 juvenile salmon using a 50 K SNP array. Consistent with previous work, we report extremely weak overall population structuring (Global F_ST = 0.004) and failed to support hierarchical structure between the river's two main branches. We provide the first genomic characterization of a previously described polymorphic fusion between chromosomes 8 and 29. Fusion genomic characteristics included high LD, reduced heterozygosity in the fused homokaryotes, and strong divergence between the fused and the unfused rearrangement. Population structure based on fusion karyotype was five times stronger than neutral variation (F_ST = 0.019), and the frequency of the fusion was associated with summer precipitation supporting a hypothesis that this rearrangement may contribute local adaptation despite weak neutral differentiation. Additionally, both outlier variation among populations and a polygenic framework for characterizing adaptive variation in relation to climate identified a 250‐Kb region of chromosome 9, including the gene six6 that has previously been linked to age‐at‐maturity and run‐timing for this species. Overall, our results indicate that adaptive processes, independent of major river branching, are more important than neutral processes for structuring these populations.     

Conserving marine biodiversity: insights from life-history trait candidate genes in Atlantic cod (Gadus morhua)

Recent technological developments have facilitated an increased focus on identifying genomic regions underlying adaptive trait variation in natural populations, and it has been advocated that this information should be important for designating population units for conservation. In marine fishes, phenotypic studies have suggested adaptation through divergence of life-history traits among natural populations, but the distribution of adaptive genetic variation in these species is still relatively poorly known. In this study, we extract information about the geographical distribution of genetic variation for 33 single nucleotide polymorphisms (SNPs) associated with life-history trait candidate genes, and compare this to variation in 70 putatively neutral SNPs in Atlantic cod (Gadus morhua). We analyse samples covering the major population complexes in the eastern Atlantic and find strong evidence for non-neutral levels and patterns of population structuring for several of the candidate gene-associated markers, including two SNPs in the growth hormone 1 gene. Thus, this study aligns with findings from phenotypic studies, providing molecular data strongly suggesting that these or closely linked genes are under selection in natural populations of Atlantic cod. Furthermore, we find that patterns of variation in outlier markers do not align with those observed at selectively neutral markers, and that outlier markers identify conservation units on finer geographical scales than those revealed when analysing only neutral markers. Accordingly, results also suggest that information about adaptive genetic variation will be useful for targeted conservation and management in this and other marine species.     

Temporal change in genetic integrity suggests loss of local adaptation in a wild Atlantic salmon (Salmo salar) population following introgression by farmed escapees

In some wild Atlantic salmon populations, rapid declines in numbers of wild returning adults has been associated with an increase in the prevalence of farmed salmon. Studies of phenotypic variation have shown that interbreeding between farmed and wild salmon may lead to loss of local adaptation. Yet, few studies have attempted to assess the impact of interbreeding at the genome level, especially among North American populations. Here, we document temporal changes in the genetic makeup of the severely threatened Magaguadavic River salmon population (Bay of Fundy, Canada), a population that might have been impacted by interbreeding with farmed salmon for nearly 20 years. Wild and farmed individuals caught entering the river from 1980 to 2005 were genotyped at 112 single-nucleotide polymorphisms (SNPs), and/or eight microsatellite loci, to scan for potential shifts in adaptive genetic variation. No significant temporal change in microsatellite-based estimates of allele richness or gene diversity was detected in the wild population, despite its precipitous decline in numbers over the last two decades. This might reflect the effect of introgression from farmed salmon, which was corroborated by temporal change in linkage-disequilibrium. Moreover, SNP genome scans identified a temporal decrease in candidate loci potentially under directional selection. Of particular interest was a SNP previously shown to be strongly associated with an important quantitative trait locus for parr mark number, which retained its genetic distinctiveness between farmed and wild fish longer than other outliers. Overall, these results indicate that farmed escapees have introgressed with wild Magaguadavic salmon resulting in significant alteration of the genetic integrity of the native population, including possible loss of adaptation to wild conditions.     

Riverscape genomics of a threatened fish across a hydroclimatically heterogeneous river basin

Understanding how natural selection generates and maintains adaptive genetic diversity in heterogeneous environments is key to predicting the evolutionary response of populations to rapid environmental change. Detecting selection in complex spatial environments remains challenging, especially for threatened species where the effects of strong genetic drift may overwhelm signatures of selection. We carried out a basinwide riverscape genomic analysis in the threatened southern pygmy perch (Nannoperca australis), an ecological specialist with low dispersal potential. High‐resolution environmental data and 5162 high‐quality filtered SNPs were used to clarify spatial population structure and to assess footprints of selection associated with a steep hydroclimatic gradient and with human disturbance across the naturally and anthropogenically fragmented Murray–Darling Basin (Australia). Our approach included F_ST outlier tests to define neutral loci, and a combination of spatially explicit genotype–environment association analyses to identify candidate adaptive loci while controlling for the effects of landscape structure and shared population history. We found low levels of genetic diversity and strong neutral population structure consistent with expectations based on spatial stream hierarchy and life history. In contrast, variables related to precipitation and temperature appeared as the most important environmental surrogates for putatively adaptive genetic variation at both regional and local scales. Human disturbance also influenced the variation in candidate loci for adaptation, but only at a local scale. Our study contributes to understanding of adaptive evolution along naturally and anthropogenically fragmented ecosystems. It also offers a tangible example of the potential contributions of landscape genomics for informing in situ and ex situ conservation management of biodiversity.     

The demographic history of Atlantic salmon (Salmo salar) across its distribution range reconstructed from approximate Bayesian computations*

Understanding the dual roles of demographic and selective processes in the buildup of population divergence is one of the most challenging tasks in evolutionary biology. Here, we investigated the demographic history of Atlantic salmon across the entire species range using 2035 anadromous individuals from North America and Eurasia. By combining results from admixture graphs, geo‐genetic maps, and an Approximate Bayesian Computation (ABC) framework, we validated previous hypotheses pertaining to secondary contact between European and Northern American populations, but also identified secondary contacts in European populations from different glacial refugia. We further identified the major sources of admixture from the southern range of North America into more northern populations along with a strong signal of secondary gene flow between genetic regional groups. We hypothesize that these patterns reflect the spatial redistribution of ancestral variation across the entire North American range. Results also support a role for linked selection and differential introgression that likely played an underappreciated role in shaping the genomic landscape of species in the Northern hemisphere. We conclude that studies between partially isolated populations should systematically include heterogeneity in selective and introgressive effects among loci to perform more rigorous demographic inferences of the divergence process.     

A Genome Scan for Genes Underlying Microgeographic-Scale Local Adaptation in a Wild Arabidopsis Species

Adaptive divergence at the microgeographic scale has been generally disregarded because high gene flow is expected to disrupt local adaptation. Yet, growing number of studies reporting adaptive divergence at a small spatial scale highlight the importance of this process in evolutionary biology. To investigate the genetic basis of microgeographic local adaptation, we conducted a genome-wide scan among sets of continuously distributed populations of Arabidopsis halleri subsp. gemmifera that show altitudinal phenotypic divergence despite gene flow. Genomic comparisons were independently conducted in two distinct mountains where similar highland ecotypes are observed, presumably as a result of convergent evolution. Here, we established a de novo reference genome and employed an individual-based resequencing for a total of 56 individuals. Among 527,225 reliable SNP loci, we focused on those showing a unidirectional allele frequency shift across altitudes. Statistical tests on the screened genes showed that our microgeographic population genomic approach successfully retrieve genes with functional annotations that are in line with the known phenotypic and environmental differences between altitudes. Furthermore, comparison between the two distinct mountains enabled us to screen out those genes that are neutral or adaptive only in either mountain, and identify the genes involved in the convergent evolution. Our study demonstrates that the genomic comparison among a set of genetically connected populations, instead of the commonly-performed comparison between two isolated populations, can also offer an effective screening for the genetic basis of local adaptation.     

Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in atlantic salmon (Salmo salar L.)

The prediction that selection affects the genome in a locus-specific way also affecting flanking neutral variation, known as genetic hitchhiking, enables the use of polymorphic markers in noncoding regions to detect the footprints of selection. However, as the strength of the selective footprint on a locus depends on the distance from the selected site and will decay with time due to recombination, the utilization of polymorphic markers closely linked to coding regions of the genome should increase the probability of detecting the footprints of selection as more gene-containing regions are covered. The occurrence of highly polymorphic microsatellites in the untranslated regions of expressed sequence tags (ESTs) is a potentially useful source of gene-associated polymorphisms which has thus far not been utilized for genome screens in natural populations. In this study, we searched for the genetic signatures of divergent selection by screening 95 genomic and EST-derived mini- and microsatellites in eight natural Atlantic salmon, Salmo salar L., populations from different spatial scales inhabiting contrasting natural environments (salt-, brackish, and freshwater habitat). Altogether, we identified nine EST-associated microsatellites, which exhibited highly significant deviations from the neutral expectations using different statistical methods at various spatial scales and showed similar trends in separate population samples from different environments (salt-, brackish, and freshwater habitats) and sea areas (Barents vs. White Sea). We consider these ESTs as the best candidate loci affected by divergent selection, and hence, they serve as promising genes associated with adaptive divergence in Atlantic salmon. Our results demonstrate that EST-linked microsatellite genome scans provide an efficient strategy for discovering functional polymorphisms, especially in nonmodel organisms.