A neutral view of the evolving genomic architecture of speciation

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

RIVERSCAPE GENETICS IDENTIFIES REPLICATED ECOLOGICAL DIVERGENCE ACROSS AN AMAZONIAN ECOTONE

Ecological speciation involves the evolution of reproductive isolation and niche divergence in the absence of a physical barrier to gene flow. The process is one of the most controversial topics of the speciation debate, particularly in tropical regions. Here, we investigate ecologically based divergence across an Amazonian ecotone in the electric fish, Steatogenys elegans. We combine phylogenetics, genome scans, and population genetics with a recently developed individual‐based evolutionary landscape genetics approach that incorporates selection. This framework is used to assess the relative contributions of geography and divergent natural selection between environments as biodiversity drivers. We report on two closely related and sympatric lineages that exemplify how divergent selection across a major Amazonian aquatic ecotone (i.e., between rivers with markedly different hydrochemical properties) may result in replicated ecologically mediated speciation. The results link selection across an ecological gradient with reproductive isolation and we propose that assortative mating based on water color may be driving the divergence. Divergence resulting from ecologically driven selection highlights the importance of considering environmental heterogeneity in studies of speciation in tropical regions. Furthermore, we show that framing ecological speciation in a spatially explicit evolutionary landscape genetics framework provides an important first step in exploring a wide range of the potential effects of spatial dependence in natural selection.     

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.     

Ernst Mayr and the integration of geographic and ecological factors in speciation

Mayr's best recognized scientific contributions include the biological species concept and the theory of geographic speciation. In the latter, reproductive isolation evolves as an incidental by‐product of genetic divergence between allopatric populations. Mayr noted that divergent natural selection could accelerate speciation, but also argued that gene flow so strongly retards divergence that, even with selection, non‐allopatric speciation is unlikely. However, current theory and data demonstrate that substantial divergence, and even speciation, in the face of gene flow is possible. Here, I attempt to connect some opposing views about speciation by integrating Mayr's ideas about the roles of ecology and geography in speciation with current data and theory. My central premise is that the speciation process (i.e. divergence) is often continuous, and that the opposing processes of selection and gene flow interact to determine the degree of divergence (i.e. the degree of progress towards the completion of speciation). I first establish that, in the absence of gene flow, divergent selection often promotes speciation. I then discuss how population differentiation in the face of gene flow is common when divergent selection occurs. However, such population differentiation does not always lead to the evolution of discontinuities, strong reproductive isolation, and thus speciation per se. I therefore explore the genetic and ecological circumstances that facilitate speciation in the face of gene flow. For example, particular genetic architectures or ecological niches may tip the balance between selection and gene flow strongly in favour of selection. The circumstances allowing selection to overcome gene flow to the extent that a discontinuity develops, and how often these circumstances occur, are major remaining questions in speciation research. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 26–46.     

Spatially explicit models of divergence and genome hitchhiking

Strong barriers to genetic exchange can exist at divergently selected loci, whereas alleles at neutral loci flow more readily between populations, thus impeding divergence and speciation in the face of gene flow. However, ‘divergence hitchhiking’ theory posits that divergent selection can generate large regions of differentiation around selected loci. ‘Genome hitchhiking’ theory suggests that selection can also cause reductions in average genome‐wide rates of gene flow, resulting in widespread genomic divergence (rather than divergence only around specific selected loci). Spatial heterogeneity is ubiquitous in nature, yet previous models of genetic barriers to gene flow have explored limited combinations of spatial and selective scenarios. Using simulations of secondary contact of populations, we explore barriers to gene flow in various selective and spatial contexts in continuous, two‐dimensional, spatially explicit environments. In general, the effects of hitchhiking are strongest in environments with regular spatial patterning of starkly divergent habitat types. When divergent selection is very strong, the absence of intermediate habitat types increases the effects of hitchhiking. However, when selection is moderate or weak, regular (vs. random) spatial arrangement of habitat types becomes more important than the presence of intermediate habitats per se. We also document counterintuitive processes arising from the stochastic interplay between selection, gene flow and drift. Our results indicate that generalization of results from two‐deme models requires caution and increase understanding of the genomic and geographic basis of population divergence.     

Experimental evidence of genome‐wide impact of ecological selection during early stages of speciation‐with‐gene‐flow

Theory predicts that speciation‐with‐gene‐flow is more likely when the consequences of selection for population divergence transitions from mainly direct effects of selection acting on individual genes to a collective property of all selected genes in the genome. Thus, understanding the direct impacts of ecologically based selection, as well as the indirect effects due to correlations among loci, is critical to understanding speciation. Here, we measure the genome‐wide impacts of host‐associated selection between hawthorn and apple host races of Rhagoletis pomonella (Diptera: Tephritidae), a model for contemporary speciation‐with‐gene‐flow. Allele frequency shifts of 32 455 SNPs induced in a selection experiment based on host phenology were genome wide and highly concordant with genetic divergence between co‐occurring apple and hawthorn flies in nature. This striking genome‐wide similarity between experimental and natural populations of R. pomonella underscores the importance of ecological selection at early stages of divergence and calls for further integration of studies of eco‐evolutionary dynamics and genome divergence.     

Thermal adaptation and ecological speciation

Ecological speciation is defined as the emergence of reproductive isolation as a direct or indirect consequence of divergent ecological adaptation. Several empirical examples of ecological speciation have been reported in the literature which very often involve adaptation to biotic resources. In this review, we investigate whether adaptation to different thermal habitats could also promote speciation and try to assess the importance of such processes in nature. Our survey of the literature identified 16 animal and plant systems where divergent thermal adaptation may underlie (partial) reproductive isolation between populations or may allow the stable coexistence of sibling taxa. In many of the systems, the differentially adapted populations have a parapatric distribution along an environmental gradient. Isolation often involves extrinsic selection against locally maladapted parental or hybrid genotypes, and additional pre- or postzygotic barriers may be important. Together, the identified examples strongly suggest that divergent selection between thermal environments is often strong enough to maintain a bimodal genotype distribution upon secondary contact. What is less clear from the available data is whether it can also be strong enough to allow ecological speciation in the face of gene flow through reinforcement-like processes. It is possible that intrinsic features of thermal gradients or the genetic basis of thermal adaptation make such reinforcement-like processes unlikely but it is equally possible that pertinent systems are understudied. Overall, our literature survey highlights (once again) the dearth of studies that investigate similar incipient species along the continuum from initial divergence to full reproductive isolation and studies that investigate all possible reproductive barriers in a given system.     

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.     

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

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

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.     

Ecological speciation

Ecological processes are central to the formation of new species when barriers to gene flow (reproductive isolation) evolve between populations as a result of ecologically‐based divergent selection. Although laboratory and field studies provide evidence that ‘ecological speciation’ can occur, our understanding of the details of the process is incomplete. Here we review ecological speciation by considering its constituent components: an ecological source of divergent selection, a form of reproductive isolation, and a genetic mechanism linking the two. Sources of divergent selection include differences in environment or niche, certain forms of sexual selection, and the ecological interaction of populations. We explore the evidence for the contribution of each to ecological speciation. Forms of reproductive isolation are diverse and we discuss the likelihood that each may be involved in ecological speciation. Divergent selection on genes affecting ecological traits can be transmitted directly (via pleiotropy) or indirectly (via linkage disequilibrium) to genes causing reproductive isolation and we explore the consequences of both. Along with these components, we also discuss the geography and the genetic basis of ecological speciation. Throughout, we provide examples from nature, critically evaluate their quality, and highlight areas where more work is required.     

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.     

Strong divergent selection at multiple loci in two closely related species of ragworts adapted to high and low elevations on Mount Etna

Recently diverged species present particularly informative systems for studying speciation and maintenance of genetic divergence in the face of gene flow. We investigated speciation in two closely related Senecio species, S. aethnensis and S. chrysanthemifolius, which grow at high and low elevations, respectively, on Mount Etna, Sicily and form a hybrid zone at intermediate elevations. We used a newly generated genome‐wide single nucleotide polymorphism (SNP) dataset from 192 individuals collected over 18 localities along an elevational gradient to reconstruct the likely history of speciation, identify highly differentiated SNPs, and estimate the strength of divergent selection. We found that speciation in this system involved heterogeneous and bidirectional gene flow along the genome, and species experienced marked population size changes in the past. Furthermore, we identified highly‐differentiated SNPs between the species, some of which are located in genes potentially involved in ecological differences between species (such as photosynthesis and UV response). We analysed the shape of these SNPs’ allele frequency clines along the elevational gradient. These clines show significantly variable coincidence and concordance, indicative of the presence of multifarious selective forces. Selection against hybrids is estimated to be very strong (0.16–0.78) and one of the highest reported in literature. The combination of strong cumulative selection across the genome and previously identified intrinsic incompatibilities probably work together to maintain the genetic and phenotypic differentiation between these species – pointing to the importance of considering both intrinsic and extrinsic factors when studying divergence and speciation.     

Divergent selection and drift shape the genomes of two avian sister species spanning a saline–freshwater ecotone

The role of species divergence due to ecologically based divergent selection—or ecological speciation—in generating and maintaining biodiversity is a central question in evolutionary biology. Comparison of the genomes of phylogenetically related taxa spanning a selective habitat gradient enables discovery of divergent signatures of selection and thereby provides valuable insight into the role of divergent ecological selection in speciation. Tidal marsh ecosystems provide tractable opportunities for studying organisms' adaptations to selective pressures that underlie ecological divergence. Sharp environmental gradients across the saline–freshwater ecotone within tidal marshes present extreme adaptive challenges to terrestrial vertebrates. Here, we sequence 20 whole genomes of two avian sister species endemic to tidal marshes—the saltmarsh sparrow (Ammospiza caudacutus) and Nelson's sparrow (A. nelsoni)—to evaluate the influence of selective and demographic processes in shaping genome‐wide patterns of divergence. Genome‐wide divergence between these two recently diverged sister species was notably high (genome‐wide F_ST = 0.32). Against a background of high genome‐wide divergence, regions of elevated divergence were widespread throughout the genome, as opposed to focused within islands of differentiation. These patterns may be the result of genetic drift resulting from past tidal march colonization events in conjunction with divergent selection to different environments. We identified several candidate genes that exhibited elevated divergence between saltmarsh and Nelson's sparrows, including genes linked to osmotic regulation, circadian rhythm, and plumage melanism—all putative candidates linked to adaptation to tidal marsh environments. These findings provide new insights into the roles of divergent selection and genetic drift in generating and maintaining biodiversity.     

LARGE-SCALE CANDIDATE GENE SCAN REVEALS THE ROLE OF CHEMORECEPTOR GENES IN HOST PLANT SPECIALIZATION AND SPECIATION IN THE PEA APHID

Understanding the drivers of speciation is critical to interpreting patterns of biodiversity. The identification of the genetic changes underlying adaptation and reproductive isolation is necessary to link barriers to gene flow to the causal origins of divergence. Here, we present a novel approach to the genetics of speciation, which should complement the commonly used approaches of quantitative trait locus mapping and genome-wide scans for selection. We present a large-scale candidate gene approach by means of sequence capture, applied to identifying the genetic changes underlying reproductive isolation in the pea aphid, a model system for the study of ecological speciation. Targeted resequencing enabled us to scale up the candidate gene approach, specifically testing for the role of chemosensory gene families in host plant specialization. Screening for the signature of divergence under selection at 172 candidate and noncandidate loci, we revealed a handful of loci that show high levels of differentiation among host races, which almost all correspond to odorant and gustatory receptor genes. This study offers the first indication that some chemoreceptor genes, often tightly linked together in the genome, could play a key role in local adaptation and reproductive isolation in the pea aphid and potentially other phytophagous insects. Our approach opens a new route toward the functional genomics of ecological speciation.     

生态物种形成及其研究进展

物种形成是基本的进化过程, 也是生物多样性形成的基础。自然选择可以导致新物种的产生。生态物种形成是指以生态为基础的歧化选择使不同群体分化产生生殖隔离的物种形成过程。本文首先回顾了生态物种形成的研究历史, 并详细介绍了生态物种形成的3个要素, 即歧化选择的来源、生殖隔离的形式以及关联歧化选择与生殖隔离的遗传机制。歧化选择的来源主要包括不同的环境或生态位、不同形式的性选择, 以及群体间的相互作用。生殖隔离的形式多种多样, 我们总结了合子前和合子后隔离的遗传学机制以及在生态物种形成中起到的作用。控制适应性性状的基因与导致生殖隔离的基因可以通过基因多效性或连锁不平衡相互关联起来。借助于第二代测序技术, 研究者可以对生态物种形成的遗传学与基因组学基础进行研究。此外, 本文还总结了生态物种形成领域最新的研究进展, 包括平行进化的全基因组基础, 以及基因流影响群体分化的理论基础。通过归纳比较由下至上和由上至下这两种不同的研究思路, 作者认为这两种思路的结合可以为生态物种形成基因的筛选提供更有力也更精确的方法。同时, 作者还提出生态物种形成的研究应该基于更好的表型描述以及更完整的基因组信息, 研究的物种也应该具有更广泛的代表性。     

The relative influence of natural selection and geography on gene flow in guppies

Two general processes may influence gene flow among populations. One involves divergent selection, wherein the maladaptation of immigrants and hybrids impedes gene flow between ecological environments (i.e. ecological speciation). The other involves geographic features that limit dispersal. We determined the relative influence of these two processes in natural populations of Trinidadian guppies (Poecilia reticulata). If selection is important, gene flow should be reduced between different selective environments. If geography is important, gene flow should be impeded by geographic distance and physical barriers. We examined how genetic divergence, long-term gene flow, and contemporary dispersal within a watershed were influenced by waterfalls, geographic distance, predation, and habitat features. We found that waterfalls and geographic distance increased genetic divergence and reduced dispersal and long-term gene flow. Differences in predation or habitat features did not influence genetic divergence or gene flow. In contrast, differences in predation did appear to reduce contemporary dispersal. We suggest that the standard predictions of ecological speciation may be heavily nuanced by the mating behaviour and life history strategies of guppies.     

Patterns of divergence across the geographic and genomic landscape of a butterfly hybrid zone associated with a climatic gradient

Hybrid zones are a valuable tool for studying the process of speciation and for identifying the genomic regions undergoing divergence and the ecological (extrinsic) and nonecological (intrinsic) factors involved. Here, we explored the genomic and geographic landscape of divergence in a hybrid zone between Papilio glaucus and Papilio canadensis. Using a genome scan of 28,417 ddRAD SNPs, we identified genomic regions under possible selection and examined their distribution in the context of previously identified candidate genes for ecological adaptations. We showed that differentiation was genomewide, including multiple candidate genes for ecological adaptations, particularly those involved in seasonal adaptation and host plant detoxification. The Z chromosome and four autosomes showed a disproportionate amount of differentiation, suggesting genes on these chromosomes play a potential role in reproductive isolation. Cline analyses of significantly differentiated genomic SNPs, and of species‐diagnostic genetic markers, showed a high degree of geographic coincidence (81%) and concordance (80%) and were associated with the geographic distribution of a climate‐mediated developmental threshold (length of the growing season). A relatively large proportion (1.3%) of the outliers for divergent selection were not associated with candidate genes for ecological adaptations and may reflect the presence of previously unrecognized intrinsic barriers between these species. These results suggest that exogenous (climate‐mediated) and endogenous (unknown) clines may have become coupled and act together to reinforce reproductive isolation. This approach of assessing divergence across both the genomic and geographic landscape can provide insight about the interplay between the genetic architecture of reproductive isolation and endogenous and exogenous selection.     

When can ecological speciation be detected with neutral loci?

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

Genome scans and elusive candidate genes: detecting the variation that matters for speciation

Next‐generation sequencing is providing us with vast amounts of genetic data, yet we are currently struggling in our attempts to make sense of them. In particular, it has proven difficult to link phenotypic divergence and speciation to genome level divergence. In the current issue of Molecular Ecology, Ruegg et al. ( 2014 ) present new empirical results from two closely related bird taxa. They use a promising approach combining genome scan and candidate gene analysis. Their results suggest that we may have been looking in vain for candidate speciation genes by focusing only on genes found within genomic islands of divergence. This is because genes important in divergence and speciation may not be detected by genome scans and because features of the genomic architecture per se may have a large effect on the pattern of genome divergence.