The genetic mosaic suggests a new role for hitchhiking in ecological speciation

Early in ecological speciation, the genomically localized effects of divergent selection cause heterogeneity among loci in divergence between incipient species. We call this pattern of genomic variability in divergence the 'genetic mosaic of speciation'. Previous studies have used F(ST) outliers as a way to identify divergently selected genomic regions, but the nature of the relationship between outlier loci and quantitative trait loci (QTL) involved in reproductive isolation has not yet been quantified. Here, we show that F(ST) outliers between a pair of incipient species are significantly clustered around QTL for traits that cause ecologically based reproductive isolation. Around these key QTL, extensive 'divergence hitchhiking' occurs because reduced inter-race mating and negative selection decrease the opportunity for recombination between chromosomes bearing different locally adapted QTL alleles. Divergence hitchhiking is likely to greatly increase the opportunity for speciation in populations that are sympatric, regardless of whether initial divergence was sympatric or allopatric. Early in ecological speciation, analyses of population structure, gene flow or phylogeography based on different random or arbitrarily chosen neutral markers should be expected to conflict--only markers in divergently selected genomic regions will reveal the evolutionary history of adaptive divergence and ecologically based reproductive isolation. Species retain mosaic genomes for a very long time, and gene exchange in hybrid zones can vary dramatically among loci. However, in hybridizing species, the genomic regions that affect ecologically based reproductive isolation are difficult to distinguish from regions that have diverged for other reasons.     

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.     

Genomic regions repeatedly involved in divergence among plant‐specialized pea aphid biotypes

Understanding the genetic bases of biological diversification is a long‐standing goal in evolutionary biology. Here, we investigate whether replicated cases of adaptive divergence involve the same genomic regions in the pea aphid, Acyrthosiphon pisum, a large complex of genetically differentiated biotypes, each specialized on different species of legumes. A previous study identified genomic regions putatively involved in host‐plant adaptation and/or reproductive isolation by performing a hierarchical genome scan in three biotypes. This led to the identification of 11 F_ST outliers among 390 polymorphic microsatellite markers. In this study, the outlier status of these 11 loci was assessed in eight biotypes specialized on other host plants. Four of the 11 previously identified outliers showed greater genetic differentiation among these additional biotypes than expected under the null hypothesis of neutral evolution (α < 0.01). Whether these hotspots of genomic divergence result from adaptive events, intrinsic barriers or reduced recombination is discussed.     

HETEROGENEOUS GENOMIC DIFFERENTIATION IN MARINE THREESPINE STICKLEBACKS: ADAPTATION ALONG AN ENVIRONMENTAL GRADIENT

Evolutionary divergence among populations occupying ecologically distinct environments can occur even in the face of on‐going gene flow. However, the genetic underpinnings, as well as the scale and magnitude at which this differentiation occurs in marine habitats are not well understood. We investigated the patterns and degree of genomic heterogeneity in threespine sticklebacks (Gasterosteus aculeatus) by assessing genetic variability in 20 nongenic and 20 genic (associated with genes important for freshwater adaptation) microsatellite loci in samples collected from 38 locations spanning the entire Baltic Sea coast to the North Sea boundary. Population divergence (F_ST ≈ 0.026) and structuring (five genetic clusters) was significantly more pronounced in the genic as compared to nongenic markers (F_ST ≈ 0.008; no genetic clusters). Patterns of divergence in the genic markers—45% of which were identified as outliers—correlated with local differences in salinity. Yet, a strong positive correlation between divergence in genic and nongenic markers, and their association with environmental factors suggests that adaptive divergence is reducing gene flow across the genome. Apart from providing a clear demonstration of heterogeneous genomic patterns of differentiation in a marine species, the results are indicative of adaptive population structuring across the relatively young Baltic Sea in spite of ample opportunities for gene flow.     

GENETIC AND PHENOTYPIC DIVERGENCE BETWEEN LOW‐ AND HIGH‐ALTITUDE POPULATIONS OF TWO RECENTLY DIVERGED CINNAMON TEAL SUBSPECIES

Spatial variation in the environment can lead to divergent selection between populations occupying different parts of a species’ range, and ultimately lead to population divergence. The colonization of new areas can thus facilitate divergence in beneficial traits, yet with little differentiation at neutral genetic markers. We investigated genetic and phenotypic patterns of divergence between low‐ and high‐altitude populations of cinnamon teal inhabiting normoxic and hypoxic regions in the Andes and adjacent lowlands of South America. Cinnamon teal showed strong divergence in body size (PC1; P_ST= 0.56) and exhibited significant frequency differences in a single nonsynonymous α‐hemoglobin amino acid polymorphism (Asn/Ser‐α9; F_ST= 0.60) between environmental extremes, despite considerable admixture of mtDNA and intron loci (F_ST= 0.004–0.168). Inferences of strong population segregation were further supported by the observation of few mismatched individuals in either environmental extreme. Coalescent analyses indicated that the highlands were most likely colonized from lowland regions but following divergence, gene flow has been asymmetric from the highlands into the lowlands. Multiple selection pressures associated with high‐altitude habitats, including cold and hypoxia, have likely shaped morphological and genetic divergence within South American cinnamon teal populations.     

Genome‐wide association analyses reveal polygenic genomic architecture underlying divergent shell morphology in Spanish Littorina saxatilis ecotypes

Gene flow between diverging populations experiencing dissimilar ecological conditions can theoretically constrain adaptive evolution. To minimize the effect of gene flow, alleles underlying traits essential for local adaptation are predicted to be located in linked genome regions with reduced recombination. Local reduction in gene flow caused by selection is expected to produce elevated divergence in these regions. The highly divergent crab‐adapted and wave‐adapted ecotypes of the marine snail Littorina saxatilis present a model system to test these predictions. We used genome‐wide association (GWA) analysis of geometric morphometric shell traits associated with microgeographic divergence between the two L. saxatilis ecotypes within three separate sampling sites. A total of 477 snails that had individual geometric morphometric data and individual genotypes at 4,066 single nucleotide polymorphisms (SNPs) were analyzed using GWA methods that corrected for population structure among the three sites. This approach allowed dissection of the genomic architecture of shell shape divergence between ecotypes across a wide geographic range, spanning two glacial lineages. GWA revealed 216 quantitative trait loci (QTL) with shell size or shape differences between ecotypes, with most loci explaining a small proportion of phenotypic variation. We found that QTL were evenly distributed across 17 linkage groups, and exhibited elevated interchromosomal linkage, suggesting a genome‐wide response to divergent selection on shell shape between the two ecotypes. Shell shape trait‐associated loci showed partial overlap with previously identified outlier loci under divergent selection between the two ecotypes, supporting the hypothesis of diversifying selection on these genomic regions. These results suggest that divergence in shell shape between the crab‐adapted and wave‐adapted ecotypes is produced predominantly by a polygenic genomic architecture with positive linkage disequilibrium among loci of small effect.     

Hitching a lift on the road to speciation

Understanding how speciation can take place in the presence of homogenizing gene flow remains a major challenge in evolutionary biology. In the early stages of ecological speciation, reproductive isolation between populations occupying different habitats is expected to be concentrated around genes for local adaptation. These genomic regions will show high divergence while gene exchange in other regions of the genome should continue relatively unimpaired, resulting in low levels of differentiation. The problem is to explain how speciation progresses from this point towards complete reproductive isolation, allowing genome‐wide divergence. A new study by Via and West (2008) on speciation between host races of the pea aphid, Acyrthosiphon pisum, introduces the mechanism of ‘divergence hitchhiking’ which can generate large ‘islands of differentiation’ and facilitate the build‐up of linkage disequilibrium, favouring increased reproductive isolation. This idea potentially removes a major stumbling block to speciation under continuous gene flow.     

High degree of genetic differentiation in marine three‐spined sticklebacks (Gasterosteus aculeatus)

Populations of widespread marine organisms are typically characterized by a low degree of genetic differentiation in neutral genetic markers, but much less is known about differentiation in genes whose functional roles are associated with specific selection regimes. To uncover possible adaptive population divergence and heterogeneous genomic differentiation in marine three‐spined sticklebacks (Gasterosteus aculeatus), we used a candidate gene‐based genome‐scan approach to analyse variability in 138 microsatellite loci located within/close to (<6 kb) functionally important genes in samples collected from ten geographic locations. The degree of genetic differentiation in markers classified as neutral or under balancing selection—as determined with several outlier detection methods—was low (F_ST = 0.033 or 0.011, respectively), whereas average F_ST for directionally selected markers was significantly higher (F_ST = 0.097). Clustering analyses provided support for genomic and geographic heterogeneity in selection: six genetic clusters were identified based on allele frequency differences in the directionally selected loci, whereas four were identified with the neutral loci. Allelic variation in several loci exhibited significant associations with environmental variables, supporting the conjecture that temperature and salinity, but not optic conditions, are important drivers of adaptive divergence among populations. In general, these results suggest that in spite of the high degree of physical connectivity and gene flow as inferred from neutral marker genes, marine stickleback populations are strongly genetically structured in loci associated with functionally relevant genes.     

Genomic footprints of speciation in Atlantic eels (Anguilla anguilla and A. rostrata)

The importance of speciation‐with‐geneflow scenarios is increasingly appreciated. However, the specific processes and the resulting genomic footprints of selection are subject to much discussion. We studied the genomics of speciation between the two panmictic, sympatrically spawning sister species; European (Anguilla anguilla) and American eel (A. rostrata). Divergence is assumed to have initiated more than 3 Ma, and although low gene flow still occurs, strong postzygotic barriers are present. Restriction‐site‐associated DNA (RAD) sequencing identified 328 300 SNPs for subsequent analysis. However, despite the presence of 3757 strongly differentiated SNPs (F_ST > 0.8), sliding window analyses of F_ST showed no larger genomic regions (i.e. hundreds of thousands to millions of bases) of elevated differentiation. Overall F_ST was 0.041, and linkage disequilibrium was virtually absent for SNPs separated by more than 1000 bp. We suggest this to reflect a case of genomic hitchhiking, where multiple regions are under directional selection between the species. However, low but biologically significant gene flow and high effective population sizes leading to very low genetic drift preclude accumulation of strong background differentiation. Genes containing candidate SNPs for positive selection showed significant enrichment for gene ontology (GO) terms relating to developmental processes and phosphorylation, which seems consistent with assumptions that differences in larval phase duration and migratory distances underlie speciation. Most SNPs under putative selection were found outside coding regions, lending support to emerging views that noncoding regions may be more functionally important than previously assumed. In total, the results demonstrate the necessity of interpreting genomic footprints of selection in the context of demographic parameters and life‐history features of the studied species.     

Genomic divergence across ecological gradients in the Central African rainforest songbird (Andropadus virens)

The little greenbul, a common rainforest passerine from sub‐Saharan Africa, has been the subject of long‐term evolutionary studies to understand the mechanisms leading to rainforest speciation. Previous research found morphological and behavioural divergence across rainforest–savannah transition zones (ecotones), and a pattern of divergence with gene flow suggesting divergent natural selection has contributed to adaptive divergence and ecotones could be important areas for rainforests speciation. Recent advances in genomics and environmental modelling make it possible to examine patterns of genetic divergence in a more comprehensive fashion. To assess the extent to which natural selection may drive patterns of differentiation, here we investigate patterns of genomic differentiation among populations across environmental gradients and regions. We find compelling evidence that individuals form discrete genetic clusters corresponding to distinctive environmental characteristics and habitat types. Pairwise F_ST between populations in different habitats is significantly higher than within habitats, and this differentiation is greater than what is expected from geographic distance alone. Moreover, we identified 140 SNPs that showed extreme differentiation among populations through a genomewide selection scan. These outliers were significantly enriched in exonic and coding regions, suggesting their functional importance. Environmental association analysis of SNP variation indicates that several environmental variables, including temperature and elevation, play important roles in driving the pattern of genomic diversification. Results lend important new genomic evidence for environmental gradients being important in population differentiation.     

Investigating the genomic basis of discrete phenotypes using a Pool‐Seq‐only approach: New insights into the genetics underlying colour variation in diverse taxa

While large‐scale genomic approaches are increasingly revealing the genetic basis of polymorphic phenotypes such as colour morphs, such approaches are almost exclusively conducted in species with high‐quality genomes and annotations. Here, we use Pool‐Seq data for both genome assembly and SNP frequency estimation, followed by scanning for F_ST outliers to identify divergent genomic regions. Using paired‐end, short‐read sequencing data from two groups of individuals expressing divergent phenotypes, we generate a de novo rough‐draft genome, identify SNPs and calculate genomewide F_ST differences between phenotypic groups. As genomes generated by Pool‐Seq data are highly fragmented, we also present an approach for super‐scaffolding contigs using existing protein‐coding data sets. Using this approach, we reanalysed genomic data from two recent studies of birds and butterflies investigating colour pattern variation and replicated their core findings, demonstrating the accuracy and power of a Pool‐Seq‐only approach. Additionally, we discovered new regions of high divergence and new annotations that together suggest novel parallels between birds and butterflies in the origins of their colour pattern variation.     

Present and past genetic connectivity of the Indo‐Pacific tropical eel Anguilla bicolor

Aim The objective of this study was to reveal the present population structure and infer the gene‐flow history of the Indo‐Pacific tropical eel Anguilla bicolor. Location The Indo‐Pacific region. Methods The entire mitochondrial control region sequence and the genotypes at six microsatellite loci were analysed for 234 specimens collected from eight representative localities where two subspecies have been historically designated. In order to infer the population structure, genetic differentiation estimates, analysis of molecular variance and gene‐tree reconstruction were performed. The history of migration events and population growth was assessed using neutrality tests based on allelic frequency spectrum, coalescent‐based estimation of gene flow and Bayesian demographic analysis using control region sequences. Results Population structure analysis showed genetic divergence between eels from the Indian and Pacific oceans (F_ST = 0.0174–0.0251, P < 0.05 for microsatellites; Φ_ST = 0.706, P < 0.001 for control region), while no significant variation was observed within each ocean. Two mitochondrial sublineages that do not coincide with geographical regions were found in the Indian Ocean clade of a gene tree. However, these two sublineages were not differentiated at the microsatellite markers. The estimation of mitochondrial gene‐flow history suggested allopatric isolation between the Indian and Pacific oceans, and a possible secondary contact within the Indian Ocean after an initial population splitting. Bayesian demographic history reconstruction and neutrality tests indicated population growth in each ocean after the Indo‐Pacific divergence. Main conclusions Anguilla bicolor has diverged between the Indian and Pacific oceans, which is consistent with the classical subspecies designation, but is apparently genetically homogeneous in the Indian Ocean. The analysis of gene‐flow and demographic history indicated that the two mitochondrial sublineages observed in the Indian Ocean probably represent the haplotype groups of relict ancestral populations. A comparison with a sympatric congener suggested that absolute physical barriers to gene flow may not be necessary for population divergence in eels.     

Outlier loci highlight the direction of introgression in oaks

Loci considered to be under selection are generally avoided in attempts to infer past demographic processes as they do not fit neutral model assumptions. However, opportunities to better reconstruct some aspects of past demography might thus be missed. Here we examined genetic differentiation between two sympatric European oak species with contrasting ecological dynamics (Quercus robur and Quercus petraea) with both outlier (i.e. loci possibly affected by divergent selection between species or by hitchhiking effects with genomic regions under selection) and nonoutlier loci. We sampled 855 individuals in six mixed forests in France and genotyped them with a set of 262 SNPs enriched with markers showing high interspecific differentiation, resulting in accurate species delimitation. We identified between 13 and 74 interspecific outlier loci, depending on the coalescent simulation models and parameters used. Greater genetic diversity was predicted in Q. petraea (a late‐successional species) than in Q. robur (an early successional species) as introgression should theoretically occur predominantly from the resident species to the invading species. Remarkably, this prediction was verified with outlier loci but not with nonoutlier loci. We suggest that the lower effective interspecific gene flow at loci showing high interspecific divergence has better preserved the signal of past asymmetric introgression towards Q. petraea caused by the species' contrasting dynamics. Using markers under selection to reconstruct past demographic processes could therefore have broader potential than generally recognized.     

Population genomic analyses from low‐coverage RAD‐Seq data: a case study on the non‐model cucurbit bottle gourd

Restriction site‐associated DNA sequencing (RAD‐Seq), a next‐generation sequencing‐based genome ‘complexity reduction’ protocol, has been useful in population genomics in species with a reference genome. However, the application of this protocol to natural populations of genomically underinvestigated species, particularly under low‐to‐medium sequencing depth, has not been well justified. In this study, a Bayesian method was developed for calling genotypes from an F₂ population of bottle gourd [Lagenaria siceraria (Mol.) Standl.] to construct a high‐density genetic map. Low‐depth genome shotgun sequencing allowed the assembly of scaffolds/contigs comprising approximately 50% of the estimated genome, of which 922 were anchored for identifying syntenic regions between species. RAD‐Seq genotyping of a natural population comprising 80 accessions identified 3226 single nuclear polymorphisms (SNPs), based on which two sub‐gene pools were suggested for association with fruit shape. The two sub‐gene pools were moderately differentiated, as reflected by the Hudson's F_ST value of 0.14, and they represent regions on LG7 with strikingly elevated F_ST values. Seven‐fold reduction in heterozygosity and two times increase in LD (r²) were observed in the same region for the round‐fruited sub‐gene pool. Outlier test suggested the locus LX3405 on LG7 to be a candidate site under selection. Comparative genomic analysis revealed that the cucumber genome region syntenic to the high F_ST island on LG7 harbors an ortholog of the tomato fruit shape gene OVATE. Our results point to a bright future of applying RAD‐Seq to population genomic studies for non‐model species even under low‐to‐medium sequencing efforts. The genomic resources provide valuable information for cucurbit genome research.     

Divergent selection and heterogeneous genomic divergence

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

Divergent and linked selection shape patterns of genomic differentiation between European and North American Atlantic salmon (Salmo salar)

As populations diverge many processes can shape genomic patterns of differentiation. Regions of high differentiation can arise due to divergent selection acting on selected loci, genetic hitchhiking of nearby loci, or through repeated selection against deleterious alleles (linked background selection); this divergence may then be further elevated in regions of reduced recombination. Atlantic salmon (Salmo salar) from Europe and North America diverged >600,000 years ago and despite some evidence of secondary contact, the majority of genetic data indicate substantial divergence between lineages. This deep divergence with potential gene flow provides an opportunity to investigate the role of different mechanisms that shape the genomic landscape during early speciation. Here, using 184,295 single nucleotide polymorphisms (SNPs) and 80 populations, we investigate the genomic landscape of differentiation across the Atlantic Ocean with a focus on highly differentiated regions and the processes shaping them. We found evidence of high (mean F_ST = 0.26) and heterogeneous genomic differentiation between continents. Genomic regions associated with high trans‐Atlantic differentiation ranged in size from single loci (SNPs) within important genes to large regions (1–3 Mbp ) on four chromosomes (Ssa06, Ssa13, Ssa16 and Ssa19). These regions showed signatures consistent with selection, including high linkage disequilibrium, despite no significant reduction in recombination. Genes and functional enrichment of processes associated with differentiated regions may highlight continental differences in ocean navigation and parasite resistance. Our results provide insight into potential mechanisms underlying differences between continents, and evidence of near‐fixed and potentially adaptive trans‐Atlantic differences concurrent with a background of high genome‐wide differentiation supports subspecies designation in Atlantic salmon.     

The genomic bases of morphological divergence and reproductive isolation driven by ecological speciation in Senecio (Asteraceae)

Ecological speciation, driven by adaptation to contrasting environments, provides an attractive opportunity to study the formation of distinct species, and the role of selection and genomic divergence in this process. Here, we focus on a particularly clear‐cut case of ecological speciation to reveal the genomic bases of reproductive isolation and morphological differences between closely related Senecio species, whose recent divergence within the last ~200 000 years was likely driven by the uplift of Mt. Etna (Sicily). These species form a hybrid zone, yet remain morphologically and ecologically distinct, despite active gene exchange. Here, we report a high‐density genetic map of the Senecio genome and map hybrid breakdown to one large and several small quantitative trait loci (QTL). Loci under diversifying selection cluster in three 5 cM regions which are characterized by a significant increase in relative (F_ST), but not absolute (d_XY), interspecific differentiation. They also correspond to some of the regions of greatest marker density, possibly corresponding to ‘cold‐spots’ of recombination, such as centromeres or chromosomal inversions. Morphological QTL for leaf and floral traits overlap these clusters. We also detected three genomic regions with significant transmission ratio distortion (TRD), possibly indicating accumulation of intrinsic genetic incompatibilities between these recently diverged species. One of the TRD regions overlapped with a cluster of high species differentiation, and another overlaps the large QTL for hybrid breakdown, indicating that divergence of these species may have occurred due to a complex interplay of ecological divergence and accumulation of intrinsic genetic incompatibilities.     

Genomic islands of divergence linked to ecotypic variation in sockeye salmon

Regions of the genome displaying elevated differentiation (genomic islands of divergence) are thought to play an important role in local adaptation, especially in populations experiencing high gene flow. However, the characteristics of these islands as well as the functional significance of genes located within them remain largely unknown. Here, we used data from thousands of SNPs aligned to a linkage map to investigate genomic islands of divergence in three ecotypes of sockeye salmon (Oncorhynchus nerka) from a single drainage in southwestern Alaska. We found ten islands displaying high differentiation among ecotypes. Conversely, neutral structure observed throughout the rest of the genome was low and not partitioned by ecotype. One island on linkage group So13 was particularly large and contained six SNPs with F_ST > 0.14 (average F_ST of neutral SNPs = 0.01). Functional annotation revealed that the peak of this island contained a nonsynonymous mutation in a gene involved in growth in other species (TULP4). The islands that we discovered were relatively small (80–402 Kb), loci found in islands did not show reduced levels of diversity, and loci in islands displayed slightly elevated linkage disequilibrium. These attributes suggest that the islands discovered here were likely generated by divergence hitchhiking; however, we cannot rule out the possibility that other mechanisms may have produced them. Our results suggest that islands of divergence serve an important role in local adaptation with gene flow and represent a significant advance towards understanding the genetic basis of ecotypic differentiation.     

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.