Genetic-environment Association Research Articles

Spatial variation in genomic signatures of local adaptation during the cane toad invasion of Australia.

Adaptive evolution can facilitate species' range expansions across environmentally heterogeneous landscapes. However, serial founder effects can limit the efficacy of selection, and the evolution of increased dispersal during range expansions may result in gene flow swamping local adaptation. Here, we study how genetic drift, gene flow and selection interact during the cane toad's (Rhinella marina) invasion across the heterogeneous landscape of Australia. Following its introduction in 1935, the cane toad colonised eastern Australia and established several stable range edges. The ongoing, more rapid range expansion in north-central Australia has occurred concomitant with an evolved increase in dispersal capacity. Using reduced representation genomic data of Australian cane toads from the expansion front and from two areas of their established range, we test the hypothesis that high gene flow constrains local adaptation at the expansion front relative to established areas. Genetic analyses indicate the three study areas are genetically distinct but show similar levels of allelic richness, heterozygosity and inbreeding. Markedly higher gene flow or recency of colonisation at the expansion front have likely hindered local adaptation at the time of sampling, as indicated by reduced slopes of genetic-environment associations (GEAs) estimated using a novel application of geographically weighted regression that accounts for allele surfing; GEA slopes are significantly steeper in established parts of the range. Our work bolsters evidence supporting adaptation of invasive species post-introduction and adds novel evidence for differing strengths of evolutionary forces among geographic areas with different invasion histories.

Genetic-environment associations explain genetic differentiation and variation between western and eastern North Pacific rhinoceros auklet (Cerorhinca monocerata) breeding colonies.

Animals are strongly connected to the environments they live in and may become adapted to local environments. Examining genetic-environment associations of key indicator species, like seabirds, provides greater insights into the forces that drive evolution in marine systems. Here we examined a RADseq dataset of 19,213 SNPs for 99 rhinoceros auklets (Cerorhinca monocerata) from five western Pacific and 10 eastern Pacific breeding colonies. We used partial redundancy analyses to identify candidate adaptive loci and to quantify the effects of environmental variation on population genetic structure. We identified 262 candidate adaptive loci, which accounted for 3.0% of the observed genetic variation among western Pacific and eastern Pacific breeding colonies. Genetic variation was more strongly associated with pH and maximum current velocity, than maximum sea surface temperature. Genetic-environment associations explain genetic differences between western and eastern Pacific populations; however, genetic variation within the western and eastern Pacific Ocean populations appears to follow a pattern of isolation-by-distance. This study represents a first to quantify the relationship between environmental and genetic variation for this widely distributed marine species and provides greater insights into the evolutionary forces that act on marine species.

Rapid diversification of grey mangroves (Avicennia marina) driven by geographic isolation and extreme environmental conditions in the Arabian Peninsula.

Biological systems occurring in ecologically heterogeneous and spatially discontinuous habitats provide an ideal opportunity to investigate the relative roles of neutral and selective factors in driving lineage diversification. The grey mangroves (Avicennia marina) of Arabia occur at the northern edge of the species' range and are subject to variable, often extreme, environmental conditions, as well as historic large fluctuations in habitat availability and connectivity resulting from Quaternary glacial cycles. Here, we analyse fully sequenced genomes sampled from 19 locations across the Red Sea, the Arabian Sea and the Persian/Arabian Gulf (PAG) to reconstruct the evolutionary history of the species in the region and to identify adaptive mechanisms of lineage diversification. Population structure and phylogenetic analyses revealed marked genetic structure correlating with geographic distance and highly supported clades among and within the seas surrounding the Arabian Peninsula. Demographic modelling showed times of divergence consistent with recent periods of geographic isolation and low marine connectivity during glaciations, suggesting the presence of (cryptic) glacial refugia in the Red Sea and the PAG. Significant migration was detected within the Red Sea and the PAG, and across the Strait of Hormuz to the Arabian Sea, suggesting gene flow upon secondary contact among populations. Genetic-environment association analyses revealed high levels of adaptive divergence and detected signs of multi-loci local adaptation driven by temperature extremes and hypersalinity. These results support a process of rapid diversification resulting from the combined effects of historical factors and ecological selection and reveal mangrove peripheral environments as relevant drivers of lineage diversity.

Local adaptation and future climate vulnerability in a wild rodent

As climate change continues, species pushed outside their physiological tolerance limits must adapt or face extinction. When change is rapid, adaptation will largely harness ancestral variation, making the availability and characteristics of that variation of critical importance. Here, we used whole-genome sequencing and genetic-environment association analyses to identify adaptive variation and its significance in the context of future climates in a small Palearctic mammal, the bank vole (Clethrionomys glareolus). We found that peripheral populations of bank vole in Britain are already at the extreme bounds of potential genetic adaptation and may require an influx of adaptive variation in order to respond. Analyses of adaptive loci suggest regional differences in climate variables select for variants that influence patterns of population adaptive resilience, including genes associated with antioxidant defense, and support a pattern of thermal/hypoxic cross-adaptation. Our findings indicate that understanding potential shifts in genomic composition in response to climate change may be key to predicting species’ fate under future climates.

Genomic and common garden approaches yield complementary results for quantifying environmental drivers of local adaptation in rubber rabbitbrush, a foundational Great Basin shrub.

The spatial structure of genomic and phenotypic variation across populations reflects historical and demographic processes as well as evolution via natural selection. Characterizing such variation can provide an important perspective for understanding the evolutionary consequences of changing climate and for guiding ecological restoration. While evidence for local adaptation has been traditionally evaluated using phenotypic data, modern methods for generating and analyzing landscape genomic data can directly quantify local adaptation by associating allelic variation with environmental variation. Here, we analyze both genomic and phenotypic variation of rubber rabbitbrush (Ericameria nauseosa), a foundational shrub species of western North America. To quantify landscape genomic structure and provide perspective on patterns of local adaptation, we generated reduced representation sequencing data for 17 wild populations (222 individuals; 38,615 loci) spanning a range of environmental conditions. Population genetic analyses illustrated pronounced landscape genomic structure jointly shaped by geography and environment. Genetic‐environment association (GEA) analyses using both redundancy analysis (RDA) and a machine‐learning approach (Gradient Forest) indicated environmental variables (precipitation seasonality, slope, aspect, elevation, and annual precipitation) influenced spatial genomic structure and were correlated with allele frequency shifts indicative of local adaptation at a consistent set of genomic regions. We compared our GEA‐based inference of local adaptation with phenotypic data collected by growing seeds from each population in a greenhouse common garden. Population differentiation in seed weight, emergence, and seedling traits was associated with environmental variables (e.g., precipitation seasonality) that were also implicated in GEA analyses, suggesting complementary conclusions about the drivers of local adaptation across different methods and data sources. Our results provide a baseline understanding of spatial genomic structure for E. nauseosa across the western Great Basin and illustrate the utility of GEA analyses for detecting the environmental causes and genetic signatures of local adaptation in a widely distributed plant species of restoration significance.

Fine-grained habitat-associated genetic connectivity in an admixed population of mussels in the small isolated Kerguelen Islands

Reticulated evolution -i.e. secondary introgression / admixture between sister taxa-is increasingly recognized as playing a key role in structuring infra-specific genetic variation and revealing cryptic genetic connectivity patterns. When admixture zones coincide with ecological transitions, the connectivity patterns often follow environmental variations better than distance and introgression clines may easily be confounded with local adaptation signatures. The Kerguelen mussels is an ideal system to investigate the potential role of admixture in enhancing micro-geographic structure, as they inhabit a small isolated island in the Southern Ocean characterized by a highly heterogeneous environment. Furthermore, genomic reticulation between Northern species (M. edulis, M. galloprovincialis and M. trossulus) and Southern species (M. platensis: South America and the Kerguelen Islands; and M. planulatus: Australasia) has been suspected. Here, we extended a previous analysis by using targeted-sequencing data (51,878 SNPs) across the three Northern species and the Kerguelen population. Spatial structure in the Kerguelen was then analyzed with a panel of 33 SNPs, including SNPs that were more differentiated than the genomic average between Northern species (i.e., ancestry-informative SNPs). We first showed that the Kerguelen lineage splitted very shortly after M. edulis and M. galloprovincialis initiated speciation, and it subsequently experienced admixture with the three Northern taxa. We then demonstrated that the Kerguelen mussels were significantly differentiated over small spatial distance, and that this local genetic structure was associated with environmental variations and mostly revealed by ancestry-informative markers. Simulations of admixture in the island highlight that genetic-environment associations can be better explained by introgression clines between heterogeneously differentiated genomes than by adaptation.

Disentangling adaptation from drift in bottlenecked and reintroduced populations of Alpine ibex.

Identifying local adaptation in bottlenecked species is essential for conservation management. Selection detection methods have an important role in species management plans, assessments of adaptive capacity, and looking for responses to climate change. Yet, the allele frequency changes exploited in selection detection methods are similar to those caused by the strong neutral genetic drift expected during a bottleneck. Consequently, it is often unclear what accuracy selection detection methods have across bottlenecked populations. In this study, simulations were used to explore if signals of selection could be confidently distinguished from genetic drift across 23 bottlenecked and reintroduced populations of Alpine ibex (Capra ibex). The meticulously recorded demographic history of the Alpine ibex was used to generate comprehensive simulated SNP data. The simulated SNPs were then used to benchmark the confidence we could place in outliers identified in empirical Alpine ibex RADseq derived SNP data. Within the simulated data set, the false positive rates were high for all selection detection methods (F ST outlier scans and Genetic‐Environment Association analyses) but fell substantially when two or more methods were combined. True positive rates were consistently low and became negligible with increased stringency. Despite finding many outlier loci in the empirical Alpine ibex SNPs, none could be distinguished from genetic drift‐driven false positives. Unfortunately, the low true positive rate also prevents the exclusion of recent local adaptation within the Alpine ibex. The baselines and stringent approach outlined here should be applied to other bottlenecked species to ensure the risk of false positive, or negative, signals of selection are accounted for in conservation management plans.

The influence of history, geography and environment on patterns of diversification in the western terrestrial garter snake

AbstractAimA central aim of biogeography is to understand how biodiversity is generated and maintained across landscapes. Here, we establish phylogenetic and population genetic patterns in a widespread reptile to quantify the influence of historical biogeography and current environmental variation on patterns of genetic diversity.LocationWestern North America.TaxonWestern terrestrial garter snake, Thamnophis elegans.MethodsWe used double‐digest RADseq to estimate phylogenetic relationships and characterize population genetic structure across the three widespread subspecies of T. elegans: T. e. vagrans (wandering garter snake), T. e. elegans (mountain garter snake) and T. e. terrestris (coast garter snake). We assessed patterns of dispersal and vicariance across biogeographic regions using ancestral area reconstruction (AAR) and deviations from isolation‐by‐distance across the landscape using estimated effective migration surfaces (EEMS). We identified environmental variables potentially shaping local adaptation in regional lineages using genetic‐environment association (GEA) analyses.ResultsWe recovered three well‐differentiated genetic groups that correspond to the three subspecies. AAR analyses inferred the eastern Cascade Range as the ancestral area, with dispersal to both the east and west across western North America. Populations of T. e. elegans displayed a latitudinal gradient in genetic variation across the Sierra Nevada and northern California, while populations of T. e. terrestris show discrete genetic breaks consistent with well‐known biogeographic barriers. Lastly, GEA analyses identified allele frequency shifts at loci associated with a common set of environmental variables in both T. e. elegans and T. e. terrestris.Main ConclusionT. elegans is composed of distinct evolutionary lineages, each with its own geographic range and history of diversification. T. e. elegans and T. e. terrestris show unique patterns of diversification as populations dispersed from east to west and while adapting to the new environments they colonized. Historical events, landscape features and environmental variation have all contributed to patterns of differentiation in T. elegans.

Opportunities and challenges in assessing climate change vulnerability through genomics

By investigating how past selection has affected allele frequencies across space, genomic tools are providing new insights into adaptive evolutionary processes. Now researchers are considering how this genomic information can be used to predict the future vulnerability of species under climate change. Genomic vulnerability assessments show promise, but challenges remain.

Copy number variants outperform SNPs to reveal genotype-temperature association in a marine species.

Copy number variants (CNVs) are a major component of genotypic and phenotypic variation in genomes. To date, our knowledge of genotypic variation and evolution has largely been acquired by means of single nucleotide polymorphism (SNPs) analyses. Until recently, the adaptive role of structural variants (SVs) and particularly that of CNVs has been overlooked in wild populations, partly due to their challenging identification. Here, we document the usefulness of Rapture, a derived reduced-representation shotgun sequencing approach, to detect and investigate copy number variants (CNVs) alongside SNPs in American lobster (Homarus americanus) populations. We conducted a comparative study to examine the potential role of SNPs and CNVs in local adaptation by sequencing 1,141 lobsters from 21 sampling sites within the southern Gulf of St. Lawrence, which experiences the highest yearly thermal variance of the Canadian marine coastal waters. Our results demonstrated that CNVs account for higher genetic differentiation than SNP markers. Contrary to SNPs, for which no significant genetic-environment association was found, 48 CNV candidates were significantly associated with the annual variance of sea surface temperature, leading to the genetic clustering of sampling locations despite their geographic separation. Altogether, we provide a strong empirical case that CNVs putatively contribute to local adaptation in marine species and unveil stronger spatial signal of population structure than SNPs. Our study provides the means to study CNVs in nonmodel species and highlights the importance of considering structural variants alongside SNPs to enhance our understanding of ecological and evolutionary processes shaping adaptive population structure.

Genome‐wide signals of drift and local adaptation during rapid lineage divergence in a songbird

The formation of independent evolutionary lineages involves neutral and selective factors, and understanding their relative roles in population divergence is a fundamental goal of speciation research. Correlations between allele frequencies and environmental variability can reveal the role of selection, yet the relative contribution of drift can be difficult to establish. Recently diversified taxa like the Oregon junco (Aves, Passerellidae, Junco hyemalis oreganus) of western North America provide ideal scenarios to apply genetic-environment association analyses (GEA) while controlling for population structure. Analysis of genome-wide SNP loci revealed marked genetic structure consisting of differentiated populations in isolated, dry southern mountain ranges, and less divergent, recently expanded populations in humid northern latitudes. We used correlations between genomic and environmental variance to test for three specific modes of evolutionary divergence: (a) drift in geographic isolation, (b) differentiation along continuous selective gradients and (c) isolation-by-adaptation. We found evidence of strong drift in southern mountains, but also signals of local adaptation driven by temperature, precipitation, elevation and vegetation, especially when controlling for population history. We identified numerous variants under selection scattered across the genome, suggesting that local adaptation can promote rapid differentiation when acting over multiple independent loci.

Introgression from related species reveals fine-scale structure in an isolated population of mussels and causes patterns of genetic-environment associations

A recommendation of: Christelle Fraïsse, Anne Haguenauer, Karin Gerard, Alexandra Anh-Thu Weber, Nicolas Bierne, Anne Chenuil Fine-grained habitat-associated genetic connectivity in an admixed population of mussels in the small isolated Kerguelen Islands https://doi.org/10.1101/239244

Navigating the Interface Between Landscape Genetics and Landscape Genomics.

As next-generation sequencing data become increasingly available for non-model organisms, a shift has occurred in the focus of studies of the geographic distribution of genetic variation. Whereas landscape genetics studies primarily focus on testing the effects of landscape variables on gene flow and genetic population structure, landscape genomics studies focus on detecting candidate genes under selection that indicate possible local adaptation. Navigating the transition between landscape genomics and landscape genetics can be challenging. The number of molecular markers analyzed has shifted from what used to be a few dozen loci to thousands of loci and even full genomes. Although genome scale data can be separated into sets of neutral loci for analyses of gene flow and population structure and putative loci under selection for inference of local adaptation, there are inherent differences in the questions that are addressed in the two study frameworks. We discuss these differences and their implications for study design, marker choice and downstream analysis methods. Similar to the rapid proliferation of analysis methods in the early development of landscape genetics, new analytical methods for detection of selection in landscape genomics studies are burgeoning. We focus on genome scan methods for detection of selection, and in particular, outlier differentiation methods and genetic-environment association tests because they are the most widely used. Use of genome scan methods requires an understanding of the potential mismatches between the biology of a species and assumptions inherent in analytical methods used, which can lead to high false positive rates of detected loci under selection. Key to choosing appropriate genome scan methods is an understanding of the underlying demographic structure of study populations, and such data can be obtained using neutral loci from the generated genome-wide data or prior knowledge of a species' phylogeographic history. To this end, we summarize recent simulation studies that test the power and accuracy of genome scan methods under a variety of demographic scenarios and sampling designs. We conclude with a discussion of additional considerations for future method development, and a summary of methods that show promise for landscape genomics studies but are not yet widely used.

Genomewide evidence of environmentally mediated secondary contact of European green crab (Carcinus maenas) lineages in eastern North America.

Genetic‐environment associations are increasingly revealed through population genomic data and can occur through a number of processes, including secondary contact, divergent natural selection, or isolation by distance. Here, we investigate the influence of the environment, including seasonal temperature and salinity, on the population structure of the invasive European green crab (Carcinus maenas) in eastern North America. Green crab populations in eastern North America are associated with two independent invasions, previously shown to consist of distinct northern and southern ecotypes, with a contact zone in southern Nova Scotia, Canada. Using a RAD‐seq panel of 9,137 genomewide SNPs, we detected 41 SNPs (0.49%) whose allele frequencies were highly correlated with environmental data. A principal components analysis of 25 environmental variables differentiated populations into northern, southern, and admixed sites in concordance with the observed genomic spatial structure. Furthermore, a spatial principal components analysis conducted on genomic and geographic data revealed a high degree of global structure (p < .0001) partitioning a northern and southern ecotype. Redundancy and partial redundancy analyses revealed that among the environmental variables tested, winter sea surface temperature had the strongest association with spatial structuring, suggesting that it is an important factor defining range and expansion limits of each ecotype. Understanding environmental thresholds associated with intraspecific diversity will facilitate the ability to manage current and predict future distributions of this aquatic invasive species.

Genomics and telemetry suggest a role for migration harshness in determining overwintering habitat choice, but not gene flow, in anadromous Arctic Char.

Migration is a ubiquitous life history trait with profound evolutionary and ecological consequences. Recent developments in telemetry and genomics, when combined, can bring significant insights on the migratory ecology of nonmodel organisms in the wild. Here, we used this integrative approach to document dispersal, gene flow and potential for local adaptation in anadromous Arctic Char from six rivers in the Canadian Arctic. Acoustic telemetry data from 124 tracked individuals indicated asymmetric dispersal, with a large proportion of fish (72%) tagged in three different rivers migrating up the same short river in the fall. Population genomics data from 6,136 SNP markers revealed weak, albeit significant, population differentiation (average pairwise FST =0.011) and asymmetric dispersal was also revealed by population assignments. Approximate Bayesian computation simulations suggested the presence of asymmetric gene flow, although in the opposite direction to that observed from the telemetry data, suggesting that dispersal does not necessarily lead to gene flow. These observations suggested that Arctic Char home to their natal river to spawn, but may overwinter in rivers with the shortest migratory route to minimize the costs of migration in nonbreeding years. Genome scans and genetic-environment associations identified 90 outlier markers putatively under selection, 23 of which were in or near a gene. Of these, at least four were involved in muscle and cardiac function, consistent with the hypothesis that migratory harshness could drive local adaptation. Our study illustrates the power of integrating genomics and telemetry to study migrations in nonmodel organisms in logistically challenging environments such as the Arctic.

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.

Finding the Genomic Basis of Local Adaptation: Pitfalls, Practical Solutions, and Future Directions.

Uncovering the genetic and evolutionary basis of local adaptation is a major focus of evolutionary biology. The recent development of cost-effective methods for obtaining high-quality genome-scale data makes it possible to identify some of the loci responsible for adaptive differences among populations. Two basic approaches for identifying putatively locally adaptive loci have been developed and are broadly used: one that identifies loci with unusually high genetic differentiation among populations (differentiation outlier methods) and one that searches for correlations between local population allele frequencies and local environments (genetic-environment association methods). Here, we review the promises and challenges of these genome scan methods, including correcting for the confounding influence of a species' demographic history, biases caused by missing aspects of the genome, matching scales of environmental data with population structure, and other statistical considerations. In each case, we make suggestions for best practices for maximizing the accuracy and efficiency of genome scans to detect the underlying genetic basis of local adaptation. With attention to their current limitations, genome scan methods can be an important tool in finding the genetic basis of adaptive evolutionary change.

The geography of introgression in a patchy environment and the thorn in the side of ecological speciation

Abstract When incompletely isolated taxa coexist in a patchy environment (e.g. mosaic hybrid zones, host-race complexes), patterns of variation may differ between selected traits/genes and neutral markers. While the genetic structure of selected traits/loci tends to coincide with habitat variables (producing Genetic-Environment Association or GEA), genetic differentiation at neutral loci unlinked to any selected locus rather depends on geographic connectivity at a large scale (e.g. Isolation-By-Distance or IBD), although these loci often display GEA at a small scale. This discrepancy has been repeatedly taken as evidence for parallel primary divergence driven by local adaptation. We argue that this interpretation needs to be addressed more thoroughly by considering the alternative hypothesis that speciation was initiated in allopatry and secondary introgression has subsequently erased the signal of past differentiation at neutral loci. We present a model of neutral introgression after secondary contact in a mosaic hybrid zone, which describes how GEAs dissipate with time and how neutral variation self-organizes according to the environmental and geographic structures. We show that although neutral loci can be affected by environmental selection, they are often more affected by history and connectivity: the neutral structure retains the initial geographic separation more than it correlates with the environment during the colonization and introgression phases, and then converges to a migration-drift balance, the most frequent outcome of which is GEA at a local scale but IBD at a large scale. This is the exact pattern usually attributed to parallel ecological speciation. Introgression is heterogeneous in space and depends on the landscape structure (e.g. it is faster in small patches, which are more impacted by immigration). Furthermore, there is no directionality in the association and it is possible to observe reversed GEAs between distant regions. We argue that the history of differentiation should ideally be reconstructed with selected loci or neutral loci linked to them, not neutral ones, and review some case studies for which the hypothesis of a long co-existence of co-adapted genetic backgrounds might have been refuted too hastily.

The coupling hypothesis: why genome scans may fail to map local adaptation genes

Genomic scans of multiple populations often reveal marker loci with greatly increased differentiation between populations. Often this differentiation coincides in space with contrasts in ecological factors, forming a genetic-environment association (GEA). GEAs imply a role for local adaptation, and so it is tempting to conclude that the strongly differentiated markers are themselves under ecologically based divergent selection, or are closely linked to loci under such selection. Here, we highlight an alternative and neglected explanation: intrinsic (i.e. environment-independent) pre- or post-zygotic genetic incompatibilities rather than local adaptation can be responsible for increased differentiation. Intrinsic genetic incompatibilities create endogenous barriers to gene flow, also known as tension zones, whose location can shift over time. However, tension zones have a tendency to become trapped by, and therefore to coincide with, exogenous barriers due to ecological selection. This coupling of endogenous and exogenous barriers can occur easily in spatially subdivided populations, even if the loci involved are unlinked. The result is that local adaptation explains where genetic breaks are positioned, but not necessarily their existence, which can be best explained by endogenous incompatibilities. More precisely, we show that (i) the coupling of endogenous and exogenous barriers can easily occur even when ecological selection is weak; (ii) when environmental heterogeneity is fine-grained, GEAs can emerge at incompatibility loci, but only locally, in places where habitats and gene pools are sufficiently intermingled to maintain linkage disequilibria between genetic incompatibilities, local-adaptation genes and neutral loci. Furthermore, the association between the locally adapted and intrinsically incompatible alleles (i.e. the sign of linkage disequilibrium between endogenous and exogenous loci) is arbitrary and can form in either direction. Reviewing results from the literature, we find that many predictions of our model are supported, including endogenous genetic barriers that coincide with environmental boundaries, local GEA in mosaic hybrid zones, and inverted or modified GEAs at distant locations. We argue that endogenous genetic barriers are often more likely than local adaptation to explain the majority of Fst-outlying loci observed in genome scan approaches - even when these are correlated to environmental variables.