Do highly divergent loci reside in genomic regions affecting reproductive isolation? A test using next-generation sequence data in Timema stick insects

ABSTRACT: BACKGROUND: Genetic divergence during speciation with gene flow is heterogeneous across the genome, with some regions exhibiting stronger differentiation than others. Exceptionally differentiated regions are often assumed to experience reduced introgression, i.e., reduced flow of alleles from one population into another because such regions are affected by divergent selection or cause reproductive isolation. In contrast, the remainder of the genome can be homogenized by high introgression. Although many studies have documented variation across the genome in genetic differentiation, there are few tests of this hypothesis that explicitly quantify introgression. Here, we provide such a test using 38,304 SNPs in populations of Timema cristinae stick insects. We quantify whether loci that are highly divergent between geographically separated ('allopatric') populations exhibit unusual patterns of introgression in admixed populations. To the extent this is true, highly divergent loci between allopatric populations contribute to reproductive isolation in admixed populations. RESULTS: As predicted, we find a substantial association between locus-specific divergence between allopatric populations and locus-specific introgression in admixed populations. However, many loci depart from this relationship, sometimes strongly so. We also report evidence for selection against foreign alleles due to local adaptation. CONCLUSIONS: Loci that are strongly differentiated between allopatric populations sometimes contribute to reproductive isolation in admixed populations. However, geographic variation in selection and local adaptation, in aspects of genetic architecture (such as organization of genes, recombination rate variation, number and effect size of variants contributing to adaptation, etc.), and in stochastic evolutionary processes such as drift can cause strong differentiation of loci that do not always contribute to reproductive isolation. The results have implications for the theory of 'genomic islands of speciation'.     

The genomic consequences of adaptive divergence and reproductive isolation between species of manakins

The processes of adaptation and speciation are expected to shape genomic variation within and between diverging species. Here we analyze genomic heterogeneity of genetic differentiation and introgression in a hybrid zone between two bird species (Manacus candei and M. vitellinus) using 59 100 SNPs, a whole genome assembly, and Bayesian models. Measures of genetic differentiation () and introgression (genomic cline center [α] and rate [β]) were highly heterogeneous among loci. We identified thousands of loci with elevated parameter estimates, some of which are likely to be associated with variation in fitness in Manacus populations. To analyze the genomic organization of differentiation and introgression, we mapped SNPs onto a draft assembly of the M. vitellinus genome. Estimates of , α, and β were autocorrelated at very short physical distances (< 100 bp), but much less so beyond this. In addition, average statistical associations (linkage disequilibrium) between SNPs were generally low and were not higher in admixed populations than in populations of the parental species. Although they did not occur with a constant probability across the genome, loci with elevated , α, and β were not strongly co-localized in the genome. Contrary to verbal models that predict clustering of loci involved in adaptation and isolation in discrete genomic regions, these results are consistent with the hypothesis that genetic regions involved in adaptive divergence and reproductive isolation are scattered throughout the genome. We also found that many loci were characterized by both exceptional genetic differentiation and introgression, consistent with the hypothesis that loci involved in isolation are also often characterized by a history of divergent selection. However, the concordance between isolation and differentiation was only partial, indicating a complex architecture and history of loci involved in isolation.     

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.     

Bayesian estimation of genomic clines

We developed a Bayesian genomic cline model to study the genetic architecture of adaptive divergence and reproductive isolation between hybridizing lineages. This model quantifies locus‐specific patterns of introgression with two cline parameters that describe the probability of locus‐specific ancestry as a function of genome‐wide admixture. ‘Outlier’ loci with extreme patterns of introgression relative to most of the genome can be identified. These loci are potentially associated with adaptive divergence or reproductive isolation. We simulated genetic data for admixed populations that included neutral introgression, as well as loci that were subject to directional, epistatic or underdominant selection, and analysed these data using the Bayesian genomic cline model. Under many demographic conditions, underdominance or directional selection had detectable and predictable effects on cline parameters, and ‘outlier’ loci were greatly enriched for genetic regions affected by selection. We also analysed previously published genetic data from two transects through a hybrid zone between Mus domesticus and M. musculus. We found considerable variation in rates of introgression across the genome and particularly low rates of introgression for two X‐linked markers. There were similarities and differences in patterns of introgression between the two transects, which likely reflects a combination of stochastic variability because of genetic drift and geographic variation in the genetic architecture of reproductive isolation. By providing a robust framework to quantify and compare patterns of introgression among genetic regions and populations, the Bayesian genomic cline model will advance our understanding of the genetics of reproductive isolation and the speciation process.     

THE EFFICACY OF DIVERGENCE HITCHHIKING IN GENERATING GENOMIC ISLANDS DURING ECOLOGICAL SPECIATION

Genes under divergent selection flow less readily between populations than other loci. This observation has led to verbal “divergence hitchhiking” models of speciation in which decreased interpopulation gene flow surrounding loci under divergent selection can generate large regions of differentiation within the genome (genomic islands). The efficacy of this model in promoting speciation depends on the size of the region affected by divergence hitchhiking. Empirical evidence is mixed, with examples of both large and small genomic islands. To address these empirical discrepancies and to formalize the theory, we present mathematical models of divergence hitchhiking, which examine neutral differentiation around selected sites. For a single locus under selection, regions of differentiation do not extend far along a chromosome away from a selected site unless both effective population sizes and migration rates are low. When multiple loci are considered, regions of differentiation can be larger. However, with many loci under selection, genome‐wide divergence occurs and genomic islands are erased. The results show that divergence hitchhiking can generate large regions of differentiation, but that the conditions under which this occurs are limited. Thus, speciation may often require multifarious selection acting on many, isolated and physically unlinked genes. How hitchhiking promotes further adaptive divergence warrants consideration.     

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.     

Genomics of Divergence along a Continuum of Parapatric Population Differentiation

The patterns of genomic divergence during ecological speciation are shaped by a combination of evolutionary forces. Processes such as genetic drift, local reduction of gene flow around genes causing reproductive isolation, hitchhiking around selected variants, variation in recombination and mutation rates are all factors that can contribute to the heterogeneity of genomic divergence. On the basis of 60 fully sequenced three-spined stickleback genomes, we explore these different mechanisms explaining the heterogeneity of genomic divergence across five parapatric lake and river population pairs varying in their degree of genetic differentiation. We find that divergent regions of the genome are mostly specific for each population pair, while their size and abundance are not correlated with the extent of genome-wide population differentiation. In each pair-wise comparison, an analysis of allele frequency spectra reveals that 25–55% of the divergent regions are consistent with a local restriction of gene flow. Another large proportion of divergent regions (38–75%) appears to be mainly shaped by hitchhiking effects around positively selected variants. We provide empirical evidence that alternative mechanisms determining the evolution of genomic patterns of divergence are not mutually exclusive, but rather act in concert to shape the genome during population differentiation, a first necessary step towards ecological speciation.     

GENOME DIVERGENCE AND THE GENETIC ARCHITECTURE OF BARRIERS TO GENE FLOW BETWEEN LYCAEIDES IDAS AND L. MELISSA

Genome divergence during speciation is a dynamic process that is affected by various factors, including the genetic architecture of barriers to gene flow. Herein we quantitatively describe aspects of the genetic architecture of two sets of traits, male genitalic morphology and oviposition preference, that putatively function as barriers to gene flow between the butterfly species Lycaeides idas and L. melissa. Our analyses are based on unmapped DNA sequence data and a recently developed Bayesian regression approach that includes variable selection and explicit parameters for the genetic architecture of traits. A modest number of nucleotide polymorphisms explained a small to large proportion of the variation in each trait, and average genetic variant effects were nonnegligible. Several genetic regions were associated with variation in multiple traits or with trait variation within‐ and among‐populations. In some instances, genetic regions associated with trait variation also exhibited exceptional genetic differentiation between species or exceptional introgression in hybrids. These results are consistent with the hypothesis that divergent selection on male genitalia has contributed to heterogeneous genetic differentiation, and that both sets of traits affect fitness in hybrids. Although these results are encouraging, we highlight several difficulties related to understanding the genetics of speciation.     

After 60 years,an answer to the question: what is the Karner blue butterfly?

The Karner blue butterfly (KBB), Lycaeides melissa samuelis, is a federally protected taxon whose relationship to the Melissa blue, Lycaeides melissa, has been a point of contention during the 66 years since the KBB was first described. Using a large population-genomic dataset and a model of population divergence with migration, we investigated the relationship between the KBB and L. melissa, as well as the relationship between L. melissa and a third taxon, Lycaeides idas. We report that gene flow between the KBB and L. melissa is low, and comparable to gene flow between L. melissa and L. idas. Considering this population-genetic evidence, we conclude that the KBB is a unique evolutionary lineage that should be recognized as Lycaeides samuelis.     

GENETIC HITCHHIKING AND THE DYNAMIC BUILDUP OF GENOMIC DIVERGENCE DURING SPECIATION WITH GENE FLOW

A major issue in evolutionary biology is explaining patterns of differentiation observed in population genomic data, as divergence can be due to both direct selection on a locus and genetic hitchhiking. “Divergence hitchhiking” (DH) theory postulates that divergent selection on a locus reduces gene flow at physically linked sites, facilitating the formation of localized clusters of tightly linked, diverged loci. “Genome hitchhiking” (GH) theory emphasizes genome‐wide effects of divergent selection. Past theoretical investigations of DH and GH focused on static snapshots of divergence. Here, we used simulations assessing a variety of strengths of selection, migration rates, population sizes, and mutation rates to investigate the relative importance of direct selection, GH, and DH in facilitating the dynamic buildup of genomic divergence as speciation proceeds through time. When divergently selected mutations were limiting, GH promoted divergence, but DH had little measurable effect. When populations were small and divergently selected mutations were common, DH enhanced the accumulation of weakly selected mutations, but this contributed little to reproductive isolation. In general, GH promoted reproductive isolation by reducing effective migration rates below that due to direct selection alone, and was important for genome‐wide “congealing” or “coupling” of differentiation (F_ST) across loci as speciation progressed.     

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.     

Identifying units for conservation using molecular systematics: the cautionary tale of the Karner blue butterfly

The federally endangered North American Karner blue butterfly (Lycaeides melissa samuelis) and the closely related Melissa blue butterfly (L. m. melissa) can be distinguished based on life history and morphology. Western populations of L. m. samuelis share mitochondrial haplotypes with L. m. melissa populations, while eastern populations of L. m. samuelis have divergent haplotypes. Here we test two hypotheses concerning the presence of L. m. melissa mitochondrial haplotypes in western L. m. samuelis populations: (i) mitochondrial introgression has occurred from L. m. melissa populations into western L. m. samuelis populations, or (ii) western populations of the nominal L. m. samuelis are more closely related to L. m. melissa than to eastern L. m. samuelis populations, yet are phenotypically similar to the latter. A Bayesian algorithm was used to cluster 190 L. melissa individuals based on 143 informative amplified fragment length polymorphism (AFLP) loci. This method clearly differentiated L. m. samuelis and L. m. melissa. Thus, genomic divergence was greater between western L. m. samuelis populations and L. m. melissa populations than it was between western and eastern populations of L. m. samuelis. This supports the hypothesis that the presence of L. m. melissa mitochondrial haplotypes in western L. m. samuelis populations is the result of mitochondrial introgression. These data provide valuable information for conservation and management plans for the endangered L. m. samuelis, and illustrate the risks of using data from a single locus for diagnosing significant units of biodiversity for conservation.     

Consequences of divergence and introgression for speciation in Andean cloud forest birds

Divergence with gene flow is well documented and reveals the influence of ecological adaptation on speciation. Yet, it remains intuitive that gene exchange inhibits speciation in many scenarios, particularly among ecologically similar populations. The influence of gene flow on the divergence of populations facing similar selection pressures has received less empirical attention than scenarios where differentiation is coupled with local environmental adaptation. I used a paired study design to test the influence of genomic divergence and introgression on plumage differentiation between ecologically similar allopatric replacements of Andean cloud forest birds. Through analyses of short‐read genome‐wide sequences from over 160 individuals in 16 codistributed lineages, I found that plumage divergence is associated with deep genetic divergence, implicating a prominent role of geographic isolation in speciation. By contrast, lineages that lack plumage divergence across the same geographic barrier are more recently isolated or exhibit a signature of secondary genetic introgression, indicating a negative relationship between gene flow and divergence in phenotypic traits important to speciation. My results suggest that the evolutionary outcomes of cycles of isolation and divergence in this important theatre of biotic diversification are sensitive to time spent in the absence of gene flow.     

THE GENETIC ARCHITECTURE OF REPRODUCTIVE ISOLATION DURING SPECIATION‐WITH‐GENE‐FLOW IN LAKE WHITEFISH SPECIES PAIRS ASSESSED BY RAD SEQUENCING

During speciation‐with‐gene‐flow, effective migration varies across the genome as a function of several factors, including proximity of selected loci, recombination rate, strength of selection, and number of selected loci. Genome scans may provide better empirical understanding of the genome‐wide patterns of genetic differentiation, especially if the variance due to the previously mentioned factors is partitioned. In North American lake whitefish (Coregonus clupeaformis), glacial lineages that diverged in allopatry about 60,000 years ago and came into contact 12,000 years ago have independently evolved in several lakes into two sympatric species pairs (a normal benthic and a dwarf limnetic). Variable degrees of reproductive isolation between species pairs across lakes offer a continuum of genetic and phenotypic divergence associated with adaptation to distinct ecological niches. To disentangle the complex array of genetically based barriers that locally reduce the effective migration rate between whitefish species pairs, we compared genome‐wide patterns of divergence across five lakes distributed along this divergence continuum. Using restriction site associated DNA (RAD) sequencing, we combined genetic mapping and population genetics approaches to identify genomic regions resistant to introgression and derive empirical measures of the barrier strength as a function of recombination distance. We found that the size of the genomic islands of differentiation was influenced by the joint effects of linkage disequilibrium maintained by selection on many loci, the strength of ecological niche divergence, as well as demographic characteristics unique to each lake. Partial parallelism in divergent genomic regions likely reflected the combined effects of polygenic adaptation from standing variation and independent changes in the genetic architecture of postzygotic isolation. This study illustrates how integrating genetic mapping and population genomics of multiple sympatric species pairs provide a window on the speciation‐with‐gene‐flow mechanism.     

Insight into the roles of selection in speciation from genomic patterns of divergence and introgression in secondary contact in venomous rattlesnakes

Investigating secondary contact of historically isolated lineages can provide insight into how selection and drift influence genomic divergence and admixture. Here, we studied the genomic landscape of divergence and introgression following secondary contact between lineages of the Western Diamondback Rattlesnake (Crotalus atrox) to determine whether genomic regions under selection in allopatry also contribute to reproductive isolation during introgression. We used thousands of nuclear loci to study genomic differentiation between two lineages that have experienced recent secondary contact following isolation, and incorporated sampling from a zone of secondary contact to identify loci that are resistant to gene flow in hybrids. Comparisons of patterns of divergence and introgression revealed a positive relationship between allelic differentiation and resistance to introgression across the genome, and greater‐than‐expected overlap between genes linked to lineage‐specific divergence and loci that resist introgression. Genes linked to putatively selected markers were related to prominent aspects of rattlesnake biology that differ between populations of Western Diamondback rattlesnakes (i.e., venom and reproductive phenotypes). We also found evidence for selection against introgression of genes that may contribute to cytonuclear incompatibility, consistent with previously observed biased patterns of nuclear and mitochondrial alleles suggestive of partial reproductive isolation due to cytonuclear incompatibilities. Our results provide a genome‐scale perspective on the relationships between divergence and introgression in secondary contact that is relevant for understanding the roles of selection in maintaining partial isolation of lineages, causing admixing lineages to not completely homogenize.     

Integrating QTL mapping and genome scans towards the characterization of candidate loci under parallel selection in the lake whitefish (Coregonus clupeaformis)

As natural selection must act on underlying genetic variation, discovering the number and location of loci under the influence of selection is imperative towards understanding adaptive divergence in evolving populations. Studies employing genome scans have hypothesized that the action of divergent selection should reduce gene flow at the genomic locations implicated in adaptation and speciation among natural populations, yet once 'outlier' patterns of variation have been identified the function and role of such loci needs to be confirmed. We integrated adaptive QTL mapping and genomic scans among diverging sympatric pairs of the lake whitefish (Coregonus clupeaformis) species complex in order to test the hypothesis that differentiation between dwarf and normal ecotypes at growth-associated QTL was maintained by directional selection. We found evidence of significantly high levels of molecular divergence among eight growth QTL where two of the strongest candidate loci under the influence of directional selection exhibited parallel reductions of gene flow over multiple populations.     

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.     

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.     

Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis)

The evolutionary mechanisms generating the tremendous biodiversity of islands have long fascinated evolutionary biologists. Genetic drift and divergent selection are predicted to be strong on islands and both could drive population divergence and speciation. Alternatively, strong genetic drift may preclude adaptation. We conducted a genomic analysis to test the roles of genetic drift and divergent selection in causing genetic differentiation among populations of the island fox (Urocyon littoralis). This species consists of six subspecies, each of which occupies a different California Channel Island. Analysis of 5293 SNP loci generated using Restriction‐site Associated DNA (RAD) sequencing found support for genetic drift as the dominant evolutionary mechanism driving population divergence among island fox populations. In particular, populations had exceptionally low genetic variation, small N_e (range = 2.1–89.7; median = 19.4), and significant genetic signatures of bottlenecks. Moreover, islands with the lowest genetic variation (and, by inference, the strongest historical genetic drift) were most genetically differentiated from mainland grey foxes, and vice versa, indicating genetic drift drives genome‐wide divergence. Nonetheless, outlier tests identified 3.6–6.6% of loci as high F_ST outliers, suggesting that despite strong genetic drift, divergent selection contributes to population divergence. Patterns of similarity among populations based on high F_ST outliers mirrored patterns based on morphology, providing additional evidence that outliers reflect adaptive divergence. Extremely low genetic variation and small N_e in some island fox populations, particularly on San Nicolas Island, suggest that they may be vulnerable to fixation of deleterious alleles, decreased fitness and reduced adaptive potential.     

What can patterns of differentiation across plant genomes tell us about adaptation and speciation?

Genome scans have become a common approach to identify genomic signatures of natural selection and reproductive isolation, as well as the genomic bases of ecologically relevant phenotypes, based on patterns of polymorphism and differentiation among populations or species. Here, we review the results of studies taking genome scan approaches in plants, consider the patterns of genomic differentiation documented and their possible causes, discuss the results in light of recent models of genomic differentiation during divergent adaptation and speciation, and consider assumptions and caveats in their interpretation. We find that genomic regions of high divergence generally appear quite small in comparisons of both closely and more distantly related populations, and for the most part, these differentiated regions are spread throughout the genome rather than strongly clustered. Thus, the genome scan approach appears well-suited for identifying genomic regions or even candidate genes that underlie adaptive divergence and/or reproductive barriers. We consider other methodologies that may be used in conjunction with genome scan approaches, and suggest further developments that would be valuable. These include broader use of sequence-based markers of known genomic location, greater attention to sampling strategies to make use of parallel environmental or phenotypic transitions, more integration with approaches such as quantitative trait loci mapping and measures of gene flow across the genome, and additional theoretical and simulation work on processes related to divergent adaptation and speciation.