Divergent selection and heterogeneous genomic divergence

Levels of genetic differentiation between populations can be highly variable across the genome, with divergent selection contributing to such heterogeneous genomic divergence. For example, loci under divergent selection and those tightly physically linked to them may exhibit stronger differentiation than neutral regions with weak or no linkage to such loci. Divergent selection can also increase genome‐wide neutral differentiation by reducing gene flow (e.g. by causing ecological speciation), thus promoting divergence via the stochastic effects of genetic drift. These consequences of divergent selection are being reported in recently accumulating studies that identify: (i) ‘outlier loci’ with higher levels of divergence than expected under neutrality, and (ii) a positive association between the degree of adaptive phenotypic divergence and levels of molecular genetic differentiation across population pairs [‘isolation by adaptation’ (IBA)]. The latter pattern arises because as adaptive divergence increases, gene flow is reduced (thereby promoting drift) and genetic hitchhiking increased. Here, we review and integrate these previously disconnected concepts and literatures. We find that studies generally report 5–10% of loci to be outliers. These selected regions were often dispersed across the genome, commonly exhibited replicated divergence across different population pairs, and could sometimes be associated with specific ecological variables. IBA was not infrequently observed, even at neutral loci putatively unlinked to those under divergent selection. Overall, we conclude that divergent selection makes diverse contributions to heterogeneous genomic divergence. Nonetheless, the number, size, and distribution of genomic regions affected by selection varied substantially among studies, leading us to discuss the potential role of divergent selection in the growth of regions of differentiation (i.e. genomic islands of divergence), a topic in need of future investigation.     

Divergent selection as revealed by P(ST) and QTL-based F(ST) in three-spined stickleback (Gasterosteus aculeatus) populations along a coastal-inland gradient

Three measures of divergence, estimated at nine putatively neutral microsatellite markers, 14 quantitative traits, and seven quantitative trait loci (QTL) were compared in eight populations of the three-spined stickleback (Gasterosteus aculeatus L.) living in the Scheldt river basin (Belgium). Lowland estuarine and polder populations were polymorphic for the number of lateral plates, whereas upland freshwater populations were low-plated. The number of short gill rakers and the length of dorsal and pelvic spines gradually declined along a coastal-inland gradient. Plate number, short gill rakers and spine length showed moderate to strong signals of divergent selection between lowland and upland populations in comparison between P(ST) (a phenotypic alternative for Q(ST)) and neutral F(ST). However, such comparisons rely on the unrealistic assumption that phenotypic variance equals additive genetic variance, and that nonadditive genetic effects and environmental effects can be minimized. In order to verify this assumption and to confirm the phenotypic signals of divergence, we tested for divergent selection at the underlying QTL. For plate number, strong genetic evidence for divergent selection between lowland and upland populations was obtained based on an intron marker of the Eda gene, of which the genotype was highly congruent with plate morph. Genetic evidence for divergent selection on short gill rakers was limited to some population pairs where F(ST) at only one of two QTL was detected as an outlier, although F(ST) at both loci correlated significantly with P(ST). No genetic confirmation was obtained for divergent selection on dorsal spine length, as no outlier F(ST)s were detected at dorsal spine QTL, and no significant correlations with P(ST) were observed.     

An outlier locus relevant in habitat-mediated selection in an alpine plant across independent regional replicates

Habitat types can induce genetic responses in species and may drive adaptive differentiation and evolutionary divergence of populations. In this study, we aimed at detecting loci indicative of adaptation for different habitat types in the alpine plant Arabis alpina. We used a dataset consisting of A. alpina plants collected in scree, nutrient-rich and moist habitat types in two independent regional replicates of the European Alps (the Swiss and French Alps). Genome scans resulting in 825 amplified fragment length polymorphisms (AFLPs) followed by outlier analysis, i.e. looking for excessive differentiation between habitat types, after accounting for heterozygosity and population structure, was used to detect loci under divergent selection for habitat type within and across the alpine regions. The outlier analyses resulted in the detection of a consistent single outlier locus, which showed a higher fragment frequency in moist compared to the other habitat types in both alpine regions. In addition, a posteriori tests for hierarchical population structuring in the dataset did not detect signals confounding selection at this locus (i.e. signals of regional population structure). Thus, we consider this locus indicative of habitat-mediated selection, and we subsequently sequence-characterized and compared it to the Arabidopsis genome. The sequence was found to be a putative homologue to the SIT4 phosphatase-associated family protein. The detection of this locus in two alpine regions and the availability of its genome sequence make this locus a strong candidate worth further exploration in the habitat-mediated selection and genetic adaptation of natural populations in the alpine plant A. alpina.     

Isolation by adaptation in Neochlamisus leaf beetles: host-related selection promotes neutral genomic divergence

This study tests how divergent natural selection promotes genomic differentiation during ecological speciation. Specifically, we use adaptive ecological divergence (here, population divergence in host plant use and preference) as a proxy for selection strength and evaluate the correlation between levels of adaptive and genetic differentiation across pairwise population comparisons. Positive correlations would reveal the pattern predicted by our hypothesis, that of 'isolation by adaptation' (IBA). Notably, IBA is predicted not only for selected loci but also for neutral loci. This may reflect the effects of divergent selection on neutral loci that are 'loosely linked' to divergently selected loci or on geneflow restriction that facilitates genetic drift at all loci, including neutral loci that are completely unlinked to those evolving under divergent selection. Here, we evaluate IBA in maple- and willow-associated populations of Neochlamisus bebbianae leaf beetles. To do so, we collected host preference data to construct adaptive divergence indices and used AFLPs (amplified fragment length polymorphisms) and mitochondrial sequences to quantify genetic differentiation. Partial Mantel tests showed significant IBA in 'pooled' analyses of putatively neutral and of putatively selected ('outlier') AFLP loci. This pattern was also recovered in 12% of 'locus-specific' analyses that separately evaluated genetic differentiation at individual neutral loci. These results provided evidence for widespread effects of selection on neutral genomic divergence. Our collective findings indicate that host-related selection may play important roles in the population genomic differentiation of both neutral and selected gene regions in herbivorous insects.     

Heterogeneous genomic differentiation between walking-stick ecotypes: "isolation by adaptation" and multiple roles for divergent selection

Genetic differentiation can be highly variable across the genome. For example, loci under divergent selection and those tightly linked to them may exhibit elevated differentiation compared to neutral regions. These represent "outlier loci" whose differentiation exceeds neutral expectations. Adaptive divergence can also increase genome-wide differentiation by promoting general barriers to neutral gene flow, thereby facilitating genomic divergence via genetic drift. This latter process can yield a positive correlation between adaptive phenotypic divergence and neutral genetic differentiation (described here as "isolation-by-adaptation"). Here, we examine both these processes by combining an AFLP genome scan of two host plant ecotypes of Timema cristinae walking-sticks with existing data on adaptive phenotypic divergence and ecological speciation in these insects. We found that about 8% of loci are outliers in multiple population comparisons. Replicated comparisons between population-pairs using the same versus different host species revealed that 1-2% of loci are subject to host-related selection specifically. Locus-specific analyses revealed that up to 10% of putatively neutral (nonoutlier) AFLP loci exhibit significant isolation-by-adaptation. Our results suggest that selection may affect differentiation directly, via linkage, or by facilitating genetic drift. They thus illustrate the varied and sometimes nonintuitive contributions of selection to heterogeneous genomic differentiation.     

A neutral view of the evolving genomic architecture of speciation

Analyses of genomewide polymorphism data have begun to shed light on speciation and adaptation. Genome scans to identify regions of the genome that are unusually different between populations or species, possibly due to divergent natural or sexual selection, are widespread in speciation genomics. Theoretical and empirical work suggests that such outlier regions may grow faster than linearly during speciation with gene flow due to a rapid transition between low and high reproductive isolation. We investigate whether this pattern could be attributed to neutral processes by simulating genomes under neutral evolution with varying amounts and timing of gene flow. Under both neutral evolution and divergent selection, simulations with little or no gene flow, or with a long allopatric period after its cessation, resulted in faster than linear growth of the proportion of the genome lying in outlier regions. Without selection, higher recent gene flow erased differentiation; with divergent selection, these same scenarios produced nonlinear growth to a plateau. Our results suggest that, given a history of gene flow, the growth of the divergent genome is informative about selection during divergence, but that in many scenarios, this pattern does not easily distinguish neutral and non‐neutral processes during speciation with gene flow.     

Divergence in coloration and ecological speciation in the Anolis marmoratus species complex

Adaptive divergence in coloration is expected to produce reproductive isolation in species that use colourful signals in mate choice and species recognition. Indeed, many adaptive radiations are characterized by differentiation in colourful signals, suggesting that divergent selection acting on coloration may be an important component of speciation. Populations in the Anolis marmoratus species complex from the Caribbean island of Guadeloupe display striking divergence in the colour and pattern of adult males that occurs over small geographic distances, suggesting strong divergent selection. Here we test the hypothesis that divergence in coloration results in reduced gene flow among populations. We quantify variation in adult male coloration across a habitat gradient between mesic and xeric habitats, use a multilocus coalescent approach to infer historical demographic parameters of divergence, and examine gene flow and population structure using microsatellite variation. We find that colour variation evolved without geographic isolation and in the face of gene flow, consistent with strong divergent selection and that both ecological and sexual selection are implicated. However, we find no significant differentiation at microsatellite loci across populations, suggesting little reproductive isolation and high levels of contemporary gene exchange. Strong divergent selection on loci affecting coloration probably maintains clinal phenotypic variation despite high gene flow at neutral loci, supporting the notion of a porous genome in which adaptive portions of the genome remain fixed whereas neutral portions are homogenized by gene flow and recombination. We discuss the impact of these findings for studies of colour evolution and ecological speciation.     

Genetic evidence for ecological divergence in kokanee salmon

The evolution of locally adapted phenotypes among populations that experience divergent selective pressures is a central mechanism for generating and maintaining biodiversity. Recently, the advent of high‐throughput DNA sequencing technology has provided tools for investigating the genetic basis of this process in natural populations of nonmodel organisms. Kokanee, the freshwater form of sockeye salmon (Oncorhynchus nerka), occurs as two reproductive ecotypes, which differ in spawning habitat (tributaries vs. shorelines); however, outside of the spawning season the two ecotypes co‐occur in many lakes and lack diagnostic morphological characteristics. We used restriction site‐associated DNA (RAD) sequencing to identify 6145 SNPs and genotype kokanee from multiple spawning sites in Okanagan Lake (British Columbia, Canada). Outlier tests revealed 18 loci putatively under divergent selection between ecotypes, all of which exhibited temporally stable allele frequencies within ecotypes. Six outliers were annotated to sequences in the NCBI database, two of which matched genes associated with early development. There was no evidence for neutral genetic differentiation; however, outlier loci demonstrated significant structure with respect to ecotype and had high assignment accuracy in mixed composition simulations. The absence of neutral structure combined with a small number of highly divergent outlier loci is consistent with theoretical predictions for the early stages of ecological divergence. These outlier loci were then applied to a realistic fisheries scenario in which additional RAD sequencing was used to genotype kokanee collected by trawl in Okanagan Lake, providing preliminary evidence that this approach may be an effective tool for conservation and management.     

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.     

Genome scans reveal candidate regions involved in the adaptation to host plant in the pea aphid complex

A major goal in evolutionary biology is to uncover the genetic basis of adaptation. Divergent selection exerted on ecological traits may result in adaptive population differentiation and reproductive isolation and affect differentially the level of genetic divergence along the genome. Genome‐wide scan of large sets of individuals from multiple populations is a powerful approach to identify loci or genomic regions under ecologically divergent selection. Here, we focused on the pea aphid, a species complex of divergent host races, to explore the organization of the genomic divergence associated with host plant adaptation and ecological speciation. We analysed 390 microsatellite markers located at variable distances from predicted genes in replicate samples of sympatric populations of the pea aphid collected on alfalfa, red clover and pea, which correspond to three common host‐adapted races reported in this species complex. Using a method that accounts for the hierarchical structure of our data set, we found a set of 11 outlier loci that show higher genetic differentiation between host races than expected under the null hypothesis of neutral evolution. Two of the outliers are close to olfactory receptor genes and three other nearby genes encoding salivary proteins. The remaining outliers are located in regions with genes of unknown functions, or which functions are unlikely to be involved in interactions with the host plant. This study reveals genetic signatures of divergent selection across the genome and provides an inventory of candidate genes responsible for plant specialization in the pea aphid, thereby setting the stage for future functional studies.     

Environmental versus Anthropogenic Effects on Population Adaptive Divergence in the Freshwater Snail Lymnaea stagnalis

Repeated pesticide contaminations of lentic freshwater systems located within agricultural landscapes may affect population evolution in non-target organisms, especially in species with a fully aquatic life cycle and low dispersal ability. The issue of evolutionary impact of pollutants is therefore conceptually important for ecotoxicologists. The impact of historical exposure to pesticides on genetic divergence was investigated in the freshwater gastropod Lymnaea stagnalis, using a set of 14 populations from contrasted environments in terms of pesticide and other anthropogenic pressures. The hypothesis of population adaptive divergence was tested on 11 life-history traits, using Q _ST -F _ST comparisons. Despite strong neutral differentiation (mean F _ST = 0.291), five adult traits or parameters were found to be under divergent selection. Conversely, two early expressed traits showed a pattern consistent with uniform selection or trait canalization, and four adult traits appeared to evolve neutrally. Divergent selection patterns were mostly consistent with a habitat effect, opposing pond to ditch and channel populations. Comparatively, pesticide and other human pressures had little correspondence with evolutionary patterns, despite hatching rate impairment associated with global anthropogenic pressure. Globally, analyses revealed high genetic variation both at neutral markers and fitness-related traits in a species used as model in ecotoxicology, providing empirical support for the need to account for genetic and evolutionary components of population response in ecological risk assessment.     

Continental-Scale Footprint of Balancing and Positive Selection in a Small Rodent (Microtus arvalis)

Genetic adaptation to different environmental conditions is expected to lead to large differences between populations at selected loci, thus providing a signature of positive selection. Whereas balancing selection can maintain polymorphisms over long evolutionary periods and even geographic scale, thus leads to low levels of divergence between populations at selected loci. However, little is known about the relative importance of these two selective forces in shaping genomic diversity, partly due to difficulties in recognizing balancing selection in species showing low levels of differentiation. Here we address this problem by studying genomic diversity in the European common vole (Microtus arvalis) presenting high levels of differentiation between populations (average F _ST = 0.31). We studied 3,839 Amplified Fragment Length Polymorphism (AFLP) markers genotyped in 444 individuals from 21 populations distributed across the European continent and hence over different environmental conditions. Our statistical approach to detect markers under selection is based on a Bayesian method specifically developed for AFLP markers, which treats AFLPs as a nearly codominant marker system, and therefore has increased power to detect selection. The high number of screened populations allowed us to detect the signature of balancing selection across a large geographic area. We detected 33 markers potentially under balancing selection, hence strong evidence of stabilizing selection in 21 populations across Europe. However, our analyses identified four-times more markers (138) being under positive selection, and geographical patterns suggest that some of these markers are probably associated with alpine regions, which seem to have environmental conditions that favour adaptation. We conclude that despite favourable conditions in this study for the detection of balancing selection, this evolutionary force seems to play a relatively minor role in shaping the genomic diversity of the common vole, which is more influenced by positive selection and neutral processes like drift and demographic history.     

Selection and genomic differentiation during ecological speciation: isolating the contributions of host association via a comparative genome scan of Neochlamisus bebbianae leaf beetles

This study uses a comparative genome scan to evaluate the contributions of host plant related divergent selection to genetic differentiation and ecological speciation in maple- and willow-associated populations of Neochlamisus bebbianae leaf beetles. For each of 15 pairwise population comparisons, we identified "outlier loci" whose strong differentiation putatively reflects divergent selection. Of 447 AFLP loci, 15% were outliers across multiple population comparisons, and low linkage disequilibrium indicated that these outliers derived from multiple regions of the genome. Outliers were further classified as "host-specific" if repeatedly observed in "different-host" population comparisons but never in "same-host" comparisons. Outliers exhibiting the opposite pattern were analogously classified as "host-independent." Host-specific outliers represented 5% of all loci and were more frequent than host-independent outliers, thus revealing a large role for host-adaptation in population genomic differentiation. Evidence that host-related selection can promote divergence despite gene flow was provided by population trees. These were structured by host-association when datasets included host-specific outliers, but not when based on neutral loci, which united sympatric populations. Lastly, three host-specific outliers were highly differentiated in all nine different-host comparisons. Because host-adaptation promotes reproductive isolation in these beetles, these loci provide promising candidate gene regions for future molecular studies of ecological speciation.     

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.     

AFLP genome scans suggest divergent selection on colour patterning in allopatric colour morphs of a cichlid fish

Genome scan-based tests for selection are directly applicable to natural populations to study the genetic and evolutionary mechanisms behind phenotypic differentiation. We conducted AFLP genome scans in three distinct geographic colour morphs of the cichlid fish Tropheus moorii to assess whether the extant, allopatric colour pattern differentiation can be explained by drift and to identify markers mapping to genomic regions possibly involved in colour patterning. The tested morphs occupy adjacent shore sections in southern Lake Tanganyika and are separated from each other by major habitat barriers. The genome scans revealed significant genetic structure between morphs, but a very low proportion of loci fixed for alternative AFLP alleles in different morphs. This high level of polymorphism within morphs suggested that colour pattern differentiation did not result exclusively from neutral processes. Outlier detection methods identified six loci with excess differentiation in the comparison between a bluish and a yellow-blotch morph and five different outlier loci in comparisons of each of these morphs with a red morph. As population expansions and the genetic structure of Tropheus make the outlier approach prone to false-positive signals of selection, we examined the correlation between outlier locus alleles and colour phenotypes in a genetic and phenotypic cline between two morphs. Distributions of allele frequencies at one outlier locus were indeed consistent with linkage to a colour locus. Despite the challenges posed by population structure and demography, our results encourage the cautious application of genome scans to studies of divergent selection in subdivided and recently expanded populations.     

Natural selection drives parallel divergence in the mountain plant Heliosperma pusillum s.l

The evolution of species or ecotypes can occur gradually through neutral and adaptive genetic changes. To explore the influence of natural selection during early phases of divergence, morphological and ecological discontinuity and its adaptive significance were investigated in six pairs of alpine and independently evolved montane populations of Heliosperma pusillum s.l.; the latter are usually taxonomically recognised at the species rank in spite of their highly debatable taxonomic value. We tested whether environmental conditions – characterised by Landolt indicator values from vegetation surveys and temperature measurements – and morphology of alpine and montane populations differ discretely and in parallel across six population pairs. By reciprocal transplantation experiments in natural environments in two population pairs and in climate chambers for five population pairs we compared fitness of native versus non‐native individuals. Alpine and montane populations differed in environmental conditions and morphology within each pair. Morphological differentiation occurred in parallel and correlated with environmental, but not with genetic distances. In both environments, native individuals had higher establishment success and plant size. Differentiation of the independently evolved montane populations is driven by natural selection and parallel, independent adaptation in response to drought, lower irradiance and higher, less fluctuating temperatures in montane populations. Our study system exemplifies rapid, parallel evolution leading to morphologically and ecologically strongly divergent, though fully interfertile, ecotypes.     

Effects of assortative mate choice on the genomic and morphological structure of a hybrid zone between two bird subspecies

Phenotypic differentiation plays an important role in the formation and maintenance of reproductive barriers. In some cases, variation in a few key aspects of phenotype can promote and maintain divergence; hence, the identification of these traits and their associations with patterns of genomic divergence is crucial for understanding the patterns and processes of population differentiation. We studied hybridization between the alba and personata subspecies of the white wagtail (Motacilla alba), and quantified divergence and introgression of multiple morphological traits and 19,437 SNP loci on a 3,000 km transect. Our goal was to identify traits that may contribute to reproductive barriers and to assess how variation in these traits corresponds to patterns of genome‐wide divergence. Variation in only one trait—head plumage patterning—was consistent with reproductive isolation. Transitions in head plumage were steep and occurred over otherwise morphologically and genetically homogeneous populations, whereas cline centres for other traits and genomic ancestry were displaced over 100 km from the head cline. Field observational data show that social pairs mated assortatively by head plumage, suggesting that these phenotypes are maintained by divergent mating preferences. In contrast, variation in all other traits and genetic markers could be explained by neutral diffusion, although weak ecological selection cannot be ruled out. Our results emphasize that assortative mating may maintain phenotypic differences independent of other processes shaping genome‐wide variation, consistent with other recent findings that raise questions about the relative importance of mate choice, ecological selection and selectively neutral processes for divergent evolution.     

When can ecological speciation be detected with neutral loci?

It is not yet clear under what conditions empirical studies can reliably detect progress toward ecological speciation through the analysis of allelic variation at neutral loci. We use a simulation approach to investigate the range of parameter space under which such detection is, and is not, likely. We specifically test for the conditions under which divergent natural selection can cause a ‘generalized barrier to gene flow’ that is present across the genome. Our individual‐based numerical simulations focus on how population divergence at neutral loci varies in relation to recombination rate with a selected locus, divergent selection on that locus, migration rate and population size. We specifically test whether genetic differences at neutral markers are greater between populations in different environments than between populations in similar environments. We find that this expected signature of ecological speciation can be detected under part of the parameter space, most consistently when divergent selection is strong and migration is intermediate. By contrast, the expected signature of ecological speciation is not reliably detected when divergent selection is weak or migration is low or high. These findings provide insights into the strengths and weaknesses of using neutral markers to infer ecological speciation in natural systems.     

Outlier SNP markers reveal fine‐scale genetic structuring across European hake populations (Merluccius merluccius)

Shallow population structure is generally reported for most marine fish and explained as a consequence of high dispersal, connectivity and large population size. Targeted gene analyses and more recently genome‐wide studies have challenged such view, suggesting that adaptive divergence might occur even when neutral markers provide genetic homogeneity across populations. Here, 381 SNPs located in transcribed regions were used to assess large‐ and fine‐scale population structure in the European hake (Merluccius merluccius), a widely distributed demersal species of high priority for the European fishery. Analysis of 850 individuals from 19 locations across the entire distribution range showed evidence for several outlier loci, with significantly higher resolving power. While 299 putatively neutral SNPs confirmed the genetic break between basins (F_CT = 0.016) and weak differentiation within basins, outlier loci revealed a dramatic divergence between Atlantic and Mediterranean populations (F_CT range 0.275–0.705) and fine‐scale significant population structure. Outlier loci separated North Sea and Northern Portugal populations from all other Atlantic samples and revealed a strong differentiation among Western, Central and Eastern Mediterranean geographical samples. Significant correlation of allele frequencies at outlier loci with seawater surface temperature and salinity supported the hypothesis that populations might be adapted to local conditions. Such evidence highlights the importance of integrating information from neutral and adaptive evolutionary patterns towards a better assessment of genetic diversity. Accordingly, the generated outlier SNP data could be used for tackling illegal practices in hake fishing and commercialization as well as to develop explicit spatial models for defining management units and stock boundaries.     

Evidence of local adaptation despite strong drift in a Neotropical patchily distributed bromeliad

Both genetic drift and divergent selection are predicted to be drivers of population differentiation across patchy habitats, but the extent to which these forces act on natural populations to shape traits is strongly affected by species’ ecological features. In this study, we infer the genomic structure of Pitcairnia lanuginosa, a widespread herbaceous perennial plant with a patchy distribution. We sampled populations in the Brazilian Cerrado and the Central Andean Yungas and discovered and genotyped SNP markers using double-digest restriction-site associated DNA sequencing. In addition, we analyzed ecophysiological traits obtained from a common garden experiment and compared patterns of phenotypic and genetic divergence (P_ST–F_ST comparisons) in a subset of populations from the Cerrado. Our results from molecular analyses pointed to extremely low genetic diversity and a remarkable population differentiation, supporting a major role of genetic drift. Approximately 0.3% of genotyped SNPs were flagged as differentiation outliers by at least two distinct methods, and Bayesian generalized linear mixed models revealed a signature of isolation by environment in addition to isolation by distance for high-differentiation outlier SNPs among the Cerrado populations. P_ST–F_ST comparisons suggested divergent selection on two ecophysiological traits linked to drought tolerance. We showed that these traits vary among populations, although without any particular macro-spatial pattern, suggesting local adaptation to differences in micro-habitats. Our study shows that selection might be a relevant force, particularly for traits involved in drought stress, even for populations experiencing strong drift, which improves our knowledge on eco-evolutionary processes acting on non-continuously distributed species.Subject terms: Population genetics, Speciation