Partitioning the effects of isolation by distance,environment, and physical barriers on genomic divergence between parapatric threespine stickleback

Genetic divergence between populations is shaped by a combination of drift, migration, and selection, yielding patterns of isolation‐by‐distance (IBD) and isolation‐by‐environment (IBE). Unfortunately, IBD and IBE may be confounded when comparing divergence across habitat boundaries. For instance, parapatric lake and stream threespine stickleback (Gasterosteus aculeatus) may have diverged due to selection against migrants (IBE), or mere spatial separation (IBD). To quantitatively partition the strength of IBE and IBD, we used recently developed population genetic software (BEDASSLE) to analyze partial genomic data from three lake‐stream clines on Vancouver Island. We find support for IBD within each of three outlet streams (unlike prior studies of lake‐stream stickleback). In addition, we find evidence for IBE (controlling for geographic distance): the genetic effect of habitat is equivalent to geographic separation of ～1.9 km of IBD. Remarkably, of our three lake‐stream pairs, IBE is strongest where migration between habitats is easiest. Such microgeographic genetic divergence would require exceptionally strong divergent selection, which multiple experiments have failed to detect. Instead, we propose that nonrandom dispersal (e.g., habitat choice) contributes to IBE. Supporting this conclusion, we show that the few migrants between habitats are a nonrandom subset of the phenotype distribution of the source population.     

Drivers of population genetic differentiation in the wild: isolation by dispersal limitation,isolation by adaptation and isolation by colonization

Empirical population genetic studies have been dominated by a neutralist view, according to which gene flow and drift are the main forces driving population genetic structure in nature. The neutralist view in essence describes a process of isolation by dispersal limitation (IBDL) that generally leads to a pattern of isolation by distance (IBD). Recently, however, conceptual frameworks have been put forward that view local genetic adaptation as an important driver of population genetic structure. Isolation by adaptation (IBA) and monopolization (M) posit that gene flow among natural populations is reduced as a consequence of local genetic adaptation. IBA stresses that effective gene flow is reduced among habitats that show dissimilar ecological characteristics, leading to a pattern of isolation by environment. In monopolization, local genetic adaptation of initial colonizing genotypes results in a reduction in gene flow that fosters the persistence of founder effects. Here, we relate these different processes driving landscape genetic structure to patterns of IBD and isolation by environment (IBE). We propose a method to detect whether IBDL, IBA and M shape genetic differentiation in natural landscapes by studying patterns of variation at neutral and non‐neutral markers as well as at ecologically relevant traits. Finally, we reinterpret a representative number of studies from the recent literature by associating patterns to processes and identify patterns associated with local genetic adaptation to be as common as IBDL in structuring regional genetic variation of populations in the wild. Our results point to the importance of quantifying environmental gradients and incorporating ecology in the analysis of population genetics.     

The influence of landscape configuration and environment on population genetic structure in a sedentary passerine: insights from loci located in different genomic regions

The study of the factors structuring genetic variation can help to infer the neutral and adaptive processes shaping the demographic and evolutionary trajectories of natural populations. Here, we analyse the role of isolation by distance (IBD), isolation by resistance (IBR, defined by landscape composition) and isolation by environment (IBE, estimated as habitat and elevation dissimilarity) in structuring genetic variation in 25 blue tit (Cyanistes caeruleus) populations. We typed 1385 individuals at 26 microsatellite loci classified into two groups by considering whether they are located into genomic regions that are actively (TL; 12 loci) or not (NTL; 14 loci) transcribed to RNA. Population genetic differentiation was mostly detected using the panel of NTL. Landscape genetic analyses showed a pattern of IBD for all loci and the panel of NTL, but genetic differentiation estimated at TL was only explained by IBR models considering high resistance for natural vegetation and low resistance for agricultural lands. Finally, the absence for IBE suggests a lack of divergent selection pressures associated with differences in habitat and elevation. Overall, our study shows that markers located in different genomic regions can yield contrasting inferences on landscape‐level patterns of realized gene flow in natural populations.     

Different processes shape the patterns of divergence in the nuclear and chloroplast genomes of a relict tree species in East Asia

Isolation by spatial distance (IBD), environment (IBE), and historical climatic instability (IBI) are three common processes assessed in phylogeographic and/or landscape genetic studies. However, the relative contributions of these three processes with respect to spatial genetic patterns have seldom been compared. Moreover, whether the relative contribution differs in different regions or when assessed using different genetic markers has rarely been reported. Lindera obtusiloba has been found to have two sister genetic clades of chloroplast (cpDNA) and nuclear microsatellite (nSSR), both of which show discontinuous distribution in northern and southern East Asia. In this study, we used the Mantel test and multiple matrix regression with randomization (MMRR) to determine the relative contributions of IBD, IBE, and IBI with respect to L. obtusiloba populations. Independent Mantel tests and MMRR calculations were conducted for two genetic data sets (cpDNA and nSSR) and for different regions (the overall species range, and northern and southern subregions of the range). We found a significant IBI pattern in nSSR divergence for all assessed regions, whereas no clear IBI pattern was detected with respect to cpDNA. In contrast, significant (or marginal) divergent IBD patterns were detected for cpDNA in all regions, whereas although a significant IBE was apparent with respect to the overall range, the effect was not detected in the two subregions. The differences identified in nSSR and cpDNA population divergence may be related to differences in the heredity and ploidy of the markers. Compared with the southern region, the northern region showed less significant correlation patterns, which may be related to the shorter population history and restricted population range. The findings of this study serve to illustrate that comparing between markers or regions can contribute to gaining a better understanding the population histories of different genomes or within different regions of a species' range.     

Are habitat fragmentation,local adaptation and isolation‐by‐distance driving population divergence in wild rice Oryza rufipogon?

Habitat fragmentation weakens the connection between populations and is accompanied with isolation by distance (IBD) and local adaptation (isolation by adaptation, IBA), both leading to genetic divergence between populations. To understand the evolutionary potential of a population and to formulate proper conservation strategies, information on the roles of IBD and IBA in driving population divergence is critical. The putative ancestor of Asian cultivated rice (Oryza sativa) is endangered in China due to habitat loss and fragmentation. We investigated the genetic variation in 11 Chinese Oryza rufipogon populations using 79 microsatellite loci to infer the effects of habitat fragmentation, IBD and IBA on genetic structure. Historical and current gene flows were found to be rare (m_h = 0.0002–0.0013, m_c = 0.007–0.029), indicating IBD and resulting in a high level of population divergence (F_ST = 0.343). High within‐population genetic variation (H_E = 0.377–0.515), relatively large effective population sizes (N_e = 96–158), absence of bottlenecks and limited gene flow were found, demonstrating little impact of recent habitat fragmentation on these populations. Eleven gene‐linked microsatellite loci were identified as outliers, indicating local adaptation. Hierarchical AMOVA and partial Mantel tests indicated that population divergence of Chinese O. rufipogon was significantly correlated with environmental factors, especially habitat temperature. Common garden trials detected a significant adaptive population divergence associated with latitude. Collectively, these findings imply that IBD due to historical rather than recent fragmentation, followed by local adaptation, has driven population divergence in O. rufipogon.     

Isolation by environment in White‐breasted Nuthatches (Sitta carolinensis) of the Madrean Archipelago sky islands: a landscape genomics approach

Understanding landscape processes driving patterns of population genetic differentiation and diversity has been a long‐standing focus of ecology and evolutionary biology. Gene flow may be reduced by historical, ecological or geographic factors, resulting in patterns of isolation by distance (IBD) or isolation by environment (IBE). Although IBE has been found in many natural systems, most studies investigating patterns of IBD and IBE in nature have used anonymous neutral genetic markers, precluding inference of selection mechanisms or identification of genes potentially under selection. Using landscape genomics, the simultaneous study of genomic and ecological landscapes, we investigated the processes driving population genetic patterns of White‐breasted Nuthatches (Sitta carolinensis) in sky islands (montane forest habitat islands) of the Madrean Archipelago. Using more than 4000 single nucleotide polymorphisms and multiple tests to investigate the relationship between genetic differentiation and geographic or ecological distance, we identified IBE, and a lack of IBD, among sky island populations of S. carolinensis. Using three tests to identify selection, we found 79 loci putatively under selection; of these, seven matched CDS regions in the Zebra Finch. The loci under selection were highly associated with climate extremes (maximum temperature of warmest month and minimum precipitation of driest month). These results provide evidence for IBE – disentangled from IBD – in sky island vertebrates and identify potential adaptive genetic variation.     

Isolation by distance,not incipient ecological speciation,explains genetic differentiation in an Andean songbird (Aves: Furnariidae: Cranioleuca antisiensis,Line‐cheeked Spinetail) despite near threefold body size change across an environmental gradient

During the process of ecological speciation, reproductive isolation results from divergent natural selection and leads to a positive correlation between genetic divergence and adaptive phenotypic divergence, that is, isolation by adaptation (IBA). In natural populations, phenotypic differentiation is often autocorrelated with geographic distance, making IBA difficult to distinguish from the neutral expectation of isolation by distance (IBD). We examined these two alternatives in a dramatic case of clinal phenotypic variation in an Andean songbird, the Line‐cheeked Spinetail (Cranioleuca antisiensis). At its geographic extremes, this species shows a near threefold difference in body mass (11.5 to 31.0 g) with marked plumage differences. We analysed phenotypic, environmental and genetic data (5,154 SNPs) from 172 individuals and 19 populations sampled along its linear distribution in the Andes. We found that body mass was tightly correlated with environmental temperature, consistent with local adaptation as per Bergmann's rule. Using a P_ST–F_ST analysis, we found additional support for natural selection driving body mass differentiation, but these results could also be explained by environment‐mediated phenotypic plasticity. When we assessed the relative support for patterns of IBA and IBD using variance partitioning, we found that IBD was the best explanation for genetic differentiation along the cline. Adaptive phenotypic or environmental divergence can reduce gene flow, a pattern interpreted as evidence of ecological speciation's role in diversification. Our results provide a counterexample to this interpretation. Despite conditions conducive to ecological speciation, our results suggest that dramatic size and environmental differentiation within C. antisiensis are not limiting gene flow.     

The challenge of separating signatures of local adaptation from those of isolation by distance and colonization history: The case of two white pines

Accurately detecting signatures of local adaptation using genetic‐environment associations (GEAs) requires controlling for neutral patterns of population structure to reduce the risk of false positives. However, a high degree of collinearity between climatic gradients and neutral population structure can greatly reduce power, and the performance of GEA methods in such case is rarely evaluated in empirical studies. In this study, we attempted to disentangle the effects of local adaptation and isolation by environment (IBE) from those of isolation by distance (IBD) and isolation by colonization from glacial refugia (IBC) using range‐wide samples in two white pine species. For this, SNPs from 168 genes, including 52 candidate genes for growth and phenology, were genotyped in 133 and 61 populations of Pinus strobus and P. monticola, respectively. For P. strobus and using all 153 SNPs, climate (IBE) did not significantly explained among‐population variation when controlling for IBD and IBC in redundancy analyses (RDAs). However, 26 SNPs were significantly associated with climate in single‐locus GEA analyses (Bayenv2 and LFMM), suggesting that local adaptation took place in the presence of high gene flow. For P. monticola, we found no evidence of IBE using RDAs and weaker signatures of local adaptation using GEA and F_ST outlier tests, consistent with adaptation via phenotypic plasticity. In both species, the majority of the explained among‐population variation (69 to 96%) could not be partitioned between the effects of IBE, IBD, and IBC. GEA methods can account differently for this confounded variation, and this could explain the small overlap of SNPs detected between Bayenv2 and LFMM. Our study illustrates the inherent difficulty of taking into account neutral structure in natural populations and the importance of sampling designs that maximize climatic variation, while minimizing collinearity between climatic gradients and neutral structure.     

Population genomic evidence for multiple Pliocene refugia in a montane‐restricted harvestman (Arachnida,Opiliones, Sclerobunus robustus) from the southwestern United States

The integration of ecological niche modelling into phylogeographic analyses has allowed for the identification and testing of potential refugia under a hypothesis‐based framework, where the expected patterns of higher genetic diversity in refugial populations and evidence of range expansion of nonrefugial populations are corroborated with empirical data. In this study, we focus on a montane‐restricted cryophilic harvestman, Sclerobunus robustus, distributed throughout the heterogeneous Southern Rocky Mountains and Intermontane Plateau of southwestern North America. We identified hypothetical refugia using ecological niche models (ENMs) across three time periods, corroborated these refugia with population genetic methods using double‐digest RAD‐seq data and conducted population‐level phylogenetic and divergence dating analyses. ENMs identify two large temporally persistent regions in the mid‐latitude highlands. Genetic patterns support these two hypothesized refugia with higher genetic diversity within refugial populations and evidence for range expansion in populations found outside hypothesized refugia. Phylogenetic analyses identify five to six genetically divergent, geographically cohesive clades of S. robustus. Divergence dating analyses suggest that these separate refugia date to the Pliocene and that divergence between clades pre‐dates the late Pleistocene glacial cycles, while diversification within clades was likely driven by these cycles. Population genetic analyses reveal effects of both isolation by distance (IBD) and isolation by environment (IBE), with IBD more important in the continuous mountainous portion of the distribution, while IBE was stronger in the populations inhabiting the isolated sky islands of the south. Using model‐based coalescent approaches, we find support for postdivergence migration between clades from separate refugia.     

Genome‐wide differentiation in closely related populations: the roles of selection and geographic isolation

Population divergence in geographic isolation is due to a combination of factors. Natural and sexual selection may be important in shaping patterns of population differentiation, a pattern referred to as ‘isolation by adaptation’ (IBA). IBA can be complementary to the well‐known pattern of ‘isolation by distance’ (IBD), in which the divergence of closely related populations (via any evolutionary process) is associated with geographic isolation. The barn swallow Hirundo rustica complex comprises six closely related subspecies, where divergent sexual selection is associated with phenotypic differentiation among allopatric populations. To investigate the relative contributions of selection and geographic distance to genome‐wide differentiation, we compared genotypic and phenotypic variation from 350 barn swallows sampled across eight populations (28 pairwise comparisons) from four different subspecies. We report a draft whole‐genome sequence for H. rustica, to which we aligned a set of 9493 single nucleotide polymorphisms (SNPs). Using statistical approaches to control for spatial autocorrelation of phenotypic variables and geographic distance, we find that divergence in traits related to migratory behaviour and sexual signalling, as well as geographic distance, together explain over 70% of genome‐wide divergence among populations. Controlling for IBD, we find 42% of genomewide divergence is attributable to IBA through pairwise differences in traits related to migratory behaviour and sexual signalling alone. By (i) combining these results with prior studies of how selection shapes morphological differentiation and (ii) accounting for spatial autocorrelation, we infer that morphological adaptation plays a large role in shaping population‐level differentiation in this group of closely related populations.     

GENETIC ISOLATION BY ENVIRONMENT OR DISTANCE: WHICH PATTERN OF GENE FLOW IS MOST COMMON?

Gene flow among populations can enhance local adaptation if it introduces new genetic variants available for selection, but strong gene flow can also stall adaptation by swamping locally beneficial genes. These outcomes can depend on population size, genetic variation, and the environmental context. Gene flow patterns may align with geographic distance (IBD—isolation by distance), whereby immigration rates are inversely proportional to the distance between populations. Alternatively gene flow may follow patterns of isolation by environment (IBE), whereby gene flow rates are higher among similar environments. Finally, gene flow may be highest among dissimilar environments (counter‐gradient gene flow), the classic “gene‐swamping” scenario. Here we survey relevant studies to determine the prevalence of each pattern across environmental gradients. Of 70 studies, we found evidence of IBD in 20.0%, IBE in 37.1%, and both patterns in 37.1%. In addition, 10.0% of studies exhibited counter‐gradient gene flow. In total, 74.3% showed significant IBE patterns. This predominant IBE pattern of gene flow may have arisen directly through natural selection or reflect other adaptive and nonadaptive processes leading to nonrandom gene flow. It also precludes gene swamping as a widespread phenomenon. Implications for evolutionary processes and management under rapidly changing environments (e.g., climate change) are discussed.     

Differentiation and speciation in mountain streams: a case study in the caddisfly Rhyacophila aquitanica (Trichoptera)

Few studies have analysed the biogeography of mountain aquatic organisms, although this habitat provides stable conditions in which many species survived Pleistocene climatic oscillations, usually in the geographical vicinity of their present distribution ranges. The mountain caddisfly Rhyacophila aquitanica was selected as a model organism for this habitat type. Morphological measurements of genitalia and external characters of male individuals were obtained from almost the entire range of distribution of the species. Morphometric results were analysed by cluster analysis and multivariate statistics. Important differences were discovered among three population groups of R. aquitanica inhabiting different European mountain ranges: (i) mountain ranges north‐west of the Alps (Massif Central, Vosges, Schwarzwald and Fribourg); (ii) the southern Alps (Lombardia and Carinthia); and (iii) the western part of the southern Carpathians. This divergence suggests a long‐term isolation among these groups, which presumably took place long before the last Pleistocene glaciation, with no secondary contact among these populations. The differentiation centres of the southern Alps and Carpathian groups may have been mostly homotopic to their actual ranges, whereas the western group must have been distributed in the areas west or north‐west of the Alps with secondary expansions and disjunctions.     

Bayesian hypothesis testing supports long-distance Pleistocene migrations in a European high mountain plant (Androsace vitaliana, Primulaceae)

Colonization of the south-western European mountain ranges is suggested to have predominantly progressed from the Iberian Peninsula eastwards, but this hypothesis has never been tested in a statistical framework. Here, we test this hypothesis using Androsace vitaliana, a high elevation species with eight mostly allopatric subspecies, which is widely but disjunctly distributed across all major south-western European mountain ranges. To this end, we use plastid and nuclear sequence data as well as fingerprint (amplified fragment length polymorphisms) data and employ Bayesian methods, which allow co-estimation of genealogy and divergence times using explicit demographic models, as well as hypothesis testing via Bayes factors. Irrespective of the ambiguity concerning where A. vitaliana started to diversify – both the Alps and the mountain ranges of the Iberian Peninsula outside the Pyrenees were possible – colonization routes were not simply unidirectional, but involved Pleistocene connections between the Alps and mountain ranges of the Iberian Peninsula bypassing the interjacent Pyrenees via long-distance dispersal. In contrast, the species’ post-glacial history is shaped by regional gene pool homogenization resulting in the genetic pattern showing good congruence with geographical proximity in agreement with a vicariance model, but only partly supporting current taxonomy.     

Environmental gradients predict the genetic population structure of a coral reef fish in the Red Sea

The relatively recent fields of terrestrial landscape and marine seascape genetics seek to identify the influence of biophysical habitat features on the spatial genetic structure of populations or individuals. Over the last few years, there has been accumulating evidence for the effect of environmental heterogeneity on patterns of gene flow and connectivity in marine systems. Here, we investigate the population genetic patterns of an anemonefish, Amphiprion bicinctus, along the Saudi Arabian coast of the Red Sea. We collected nearly one thousand samples from 19 locations, spanning approximately 1500 km, and genotyped them at 38 microsatellite loci. Patterns of gene flow appeared to follow a stepping‐stone model along the northern and central Red Sea, which was disrupted by a distinct genetic break at a latitude of approximately 19°N. The Red Sea is characterized by pronounced environmental gradients along its axis, roughly separating the northern and central from the southern basin. Using mean chlorophyll‐a concentrations as a proxy for this gradient, we ran tests of isolation by distance (IBD, R² = 0.52) and isolation by environment (IBE, R² = 0.64), as well as combined models using partial Mantel tests and multiple matrix regression with randomization (MMRR). We found that genetic structure across our sampling sites may be best explained by a combined model of IBD and IBE (Mantel: R² = 0.71, MMRR: R² = 0.86). Our results highlight the potential key role of environmental patchiness in shaping patterns of gene flow in species with pelagic larval dispersal. We support growing calls for the integration of biophysical habitat characteristics into future studies of population genetic structure.     

Ecotypes of an ecologically dominant prairie grass (Andropogon gerardii) exhibit genetic divergence across the U.S. Midwest grasslands' environmental gradient

Big bluestem (Andropogon gerardii) is an ecologically dominant grass with wide distribution across the environmental gradient of U.S. Midwest grasslands. This system offers an ideal natural laboratory to study population divergence and adaptation in spatially varying climates. Objectives were to: (i) characterize neutral genetic diversity and structure within and among three regional ecotypes derived from 11 prairies across the U.S. Midwest environmental gradient, (ii) distinguish between the relative roles of isolation by distance (IBD) vs. isolation by environment (IBE) on ecotype divergence, (iii) identify outlier loci under selection and (iv) assess the association between outlier loci and climate. Using two primer sets, we genotyped 378 plants at 384 polymorphic AFLP loci across regional ecotypes from central and eastern Kansas and Illinois. Neighbour‐joining tree and PCoA revealed strong genetic differentiation between Kansas and Illinois ecotypes, which was better explained by IBE than IBD. We found high genetic variability within prairies (80%) and even fragmented Illinois prairies, surprisingly, contained high within‐prairie genetic diversity (92%). Using Bayenv 2, 14 top‐ranked outlier loci among ecotypes were associated with temperature and precipitation variables. Six of seven BayeScan F_ST outliers were in common with Bayenv 2 outliers. High genetic diversity may enable big bluestem populations to better withstand changing climates; however, population divergence supports the use of local ecotypes in grassland restoration. Knowledge of genetic variation in this ecological dominant and other grassland species will be critical to understanding grassland response and restoration challenges in the face of a changing climate.     

Long-distance dispersal vs vicariance: the origin and genetic diversity of alpine plants in the Spanish Sierra Nevada

Here, we investigated the origin and genetic diversity of four alpine plant species co-occurring in the Spanish Sierra Nevada and other high mountains in south-western Europe by analysis of amplified fragment length polymorphisms (AFLPs). In Kernera saxatilis, Silene rupestris and Gentiana alpina we found intraspecific phylogroups corresponding to mountain regions as predicted by the vicariance hypothesis. Moreover, genetic distances between Sierra Nevada and Pyrenees populations were always higher than those between populations from the Pyrenees and the south-western Alps/Massif Central. This suggests successive disruption of gene exchange between mountain ranges as postglacial climatic warming proceeded from south to north. In Papaver alpinum, our data indicate that a central Pyrenean population arose via long-distance dispersal from the Sierra Nevada, and that vicariant separation events between the Sierra Nevada and the Pyrenees and between the Pyrenees and the south-western Alps occurred simultaneously. Overall, Sierra Nevada populations of all species investigated here preserve unexpectedly high (or not exceptionally reduced) genetic diversity. This testifies to the important influence of long-term isolation, i.e. vicariance, on genetic diversity through fostering the accumulation of new mutations and/or the fixation of ancestral ones.     

Genomics of the divergence continuum in an African plant biodiversity hotspot,I: drivers of population divergence in Restio capensis (Restionaceae)

Understanding the drivers of population divergence, speciation and species persistence is of great interest to molecular ecology, especially for species‐rich radiations inhabiting the world's biodiversity hotspots. The toolbox of population genomics holds great promise for addressing these key issues, especially if genomic data are analysed within a spatially and ecologically explicit context. We have studied the earliest stages of the divergence continuum in the Restionaceae, a species‐rich and ecologically important plant family of the Cape Floristic Region (CFR) of South Africa, using the widespread CFR endemic Restio capensis (L.) H.P. Linder & C.R. Hardy as an example. We studied diverging populations of this morphotaxon for plastid DNA sequences and >14 400 nuclear DNA polymorphisms from Restriction site Associated DNA (RAD) sequencing and analysed the results jointly with spatial, climatic and phytogeographic data, using a Bayesian generalized linear mixed modelling (GLMM) approach. The results indicate that population divergence across the extreme environmental mosaic of the CFR is mostly driven by isolation by environment (IBE) rather than isolation by distance (IBD) for both neutral and non‐neutral markers, consistent with genome hitchhiking or coupling effects during early stages of divergence. Mixed modelling of plastid DNA and single divergent outlier loci from a Bayesian genome scan confirmed the predominant role of climate and pointed to additional drivers of divergence, such as drift and ecological agents of selection captured by phytogeographic zones. Our study demonstrates the usefulness of population genomics for disentangling the effects of IBD and IBE along the divergence continuum often found in species radiations across heterogeneous ecological landscapes.     

Genomic footprints of adaptation in a cooperatively breeding tropical bird across a vegetation gradient

Identifying the genetic basis of phenotypic variation and its relationship with the environment is key to understanding how local adaptations evolve. Such patterns are especially interesting among populations distributed across habitat gradients, where genetic structure can be driven by isolation by distance (IBD) and/or isolation by environment (IBE). Here, we used variation in ~1,600 high‐quality SNPs derived from paired‐end sequencing of double‐digest restriction site‐associated DNA (ddRAD‐Seq) to test hypotheses related to IBD and IBE in the Yucatan jay (Cyanocorax yucatanicus), a tropical bird endemic to the Yucatán Peninsula. This peninsula is characterized by a precipitation and vegetation gradient—from dry to evergreen tropical forests—that is associated with morphological variation in this species. We found a moderate level of nucleotide diversity (π = .008) and little evidence for genetic differentiation among vegetation types. Analyses of neutral and putatively adaptive SNPs (identified by complementary genome‐scan approaches) indicate that IBD is the most reliable explanation to account for frequency distribution of the former, while IBE has to be invoked to explain those of the later. These results suggest that selective factors acting along a vegetation gradient can promote local adaptation in the presence of gene flow in a vagile, nonmigratory and geographically restricted species. The putative candidate SNPs identified here are located within or linked to a variety of genes that represent ideal targets for future genomic surveys.     

Widespread evidence for incipient ecological speciation: a meta‐analysis of isolation‐by‐ecology

Ecologically mediated selection has increasingly become recognised as an important driver of speciation. The correlation between neutral genetic differentiation and environmental or phenotypic divergence among populations, to which we collectively refer to as isolation‐by‐ecology (IBE), is an indicator of ecological speciation. In a meta‐analysis framework, we determined the strength and commonality of IBE in nature. On the basis of 106 studies, we calculated a mean effect size of IBE with and without controlling for spatial autocorrelation among populations. Effect sizes were 0.34 (95% CI 0.24–0.42) and 0.26 (95% CI 0.13–0.37), respectively, indicating that an average of 5% of the neutral genetic differentiation among populations was explained purely by ecological contrast. Importantly, spatial autocorrelation reduced IBE correlations for environmental variables, but not for phenotypes. Through simulation, we showed how the influence of isolation‐by‐distance and spatial autocorrelation of ecological variables can result in false positives or underestimated correlations if not accounted for in the IBE model. Collectively, this meta‐analysis showed that ecologically induced genetic divergence is pervasive across time‐scales and taxa, and largely independent of the choice of molecular marker. We discuss the importance of these results in the context of adaptation and ecological speciation and suggest future research avenues.