Impacts of climate warming on hybrid zone movement: Geographically diffuse and biologically porous “species borders”

Abstract The ecology and evolutionary biology of insect–plant associations has realized extensive attention, especially during the past 60 years. The classifications (categorical designations) of continuous variation in biodiversity, ranging from global patterns (e.g., latitudinal gradients in species richness/diversity and degree of herbivore feeding specialization) to localized insect–plant associations that span the biospectrum from polyphenisms, polymorphisms, biotypes, demes, host races, to cryptic species, remain academically contentious. Semantic and biosystematic (taxonomical) disagreements sometimes detract from more important ecological and evolutionary processes that drive diversification, the dynamics of gene flow and local extinctions. This review addresses several aspects of insect specialization, host‐associated divergence and ecological (including “hybrid”) speciation, with special reference to the climate warming impacts on species borders of hybridizing swallowtail butterflies (Papilionidae). Interspecific hybrid introgression may result in collapse of multi‐species communities or increase species numbers via homoploid hybrid speciation. We may see diverging, merging, or emerging genotypes across hybrid zones, all part of the ongoing processes of evolution. Molecular analyses of genetic mosaics and genomic dynamics with “divergence hitchhiking”, combined with ecological, ethological and physiological studies of “species porosity”, have already begun to unveil some answers for some important ecological/evolutionary questions. (i) How rapidly can host‐associated divergence lead to new species (and why doesn't it always do so, e.g., resulting in “incomplete” speciation)? (ii) How might “speciation genes” function, and how/where would we find them? (iii) Can oscillations from specialists to generalists and back to specialists help explain global diversity in herbivorous insects? (iv) How could recombinant interspecific hybridization lead to divergence and speciation? From ancient phytochemically defined angiosperm affiliations to recent and very local geographical mosaics, the Papilionidae (swallowtail butterflies) have provided a model for enhanced understanding of ecological patterns and evolutionary processes, including host‐associated genetic divergence, genomic mosaics, genetic hitchhiking and sex‐linked speciation genes. Apparent homoploid hybrid speciation in Papilio appears to have been catalyzed by climate warming‐induced interspecific introgression of some, but not all, species diagnostic traits, reflecting strong divergent selection (discordant), especially on the Z (= X) chromosome. Reproductive isolation of these novel recombinant hybrid genotypes appears to be accomplished via a delayed post‐diapause emergence or temporal isolation, and is perhaps aided by the thermal landscape. Changing thermal landscapes appear to have created (and may destroy) novel recombinant hybrid genotypes and hybrid species.     

Widespread Genomic Signatures of Natural Selection in Hominid Evolution

Selection acting on genomic functional elements can be detected by its indirect effects on population diversity at linked neutral sites. To illuminate the selective forces that shaped hominid evolution, we analyzed the genomic distributions of human polymorphisms and sequence differences among five primate species relative to the locations of conserved sequence features. Neutral sequence diversity in human and ancestral hominid populations is substantially reduced near such features, resulting in a surprisingly large genome average diversity reduction due to selection of 19–26% on the autosomes and 12–40% on the X chromosome. The overall trends are broadly consistent with “background selection” or hitchhiking in ancestral populations acting to remove deleterious variants. Average selection is much stronger on exonic (both protein-coding and untranslated) conserved features than non-exonic features. Long term selection, rather than complex speciation scenarios, explains the large intragenomic variation in human/chimpanzee divergence. Our analyses reveal a dominant role for selection in shaping genomic diversity and divergence patterns, clarify hominid evolution, and provide a baseline for investigating specific selective events.     

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.     

Footprints of ancient‐balanced polymorphisms in genetic variation data from closely related species

When long‐lasting, balancing selection can lead to “trans‐species” polymorphisms that are shared by two or more species identical by descent. In such cases, the gene genealogy at the selected site clusters by allele instead of by species, and nearby neutral sites also have unusual genealogies because of linkage. While this scenario is expected to leave discernible footprints in genetic variation data, the specific patterns remain poorly characterized. Motivated by recent findings in primates, we focus on the case of a biallelic polymorphism under ancient balancing selection and derive approximations for summaries of the polymorphism data from two species. Specifically, we characterize the length of the segment that carries most of the footprints, the expected number of shared neutral single nucleotide polymorphisms (SNPs), and the patterns of allelic associations among them. We confirm the accuracy of our approximations by coalescent simulations. We further show that for humans and chimpanzees—more generally, for pairs of species with low genetic diversity levels—these patterns are highly unlikely to be generated by neutral recurrent mutations. We discuss the implications for the design and interpretation of genome scans for ancient balanced polymorphisms in primates and other taxa.     

Genomic Evidence of Rapid and Stable Adaptive Oscillations over Seasonal Time Scales in Drosophila

In many species, genomic data have revealed pervasive adaptive evolution indicated by the fixation of beneficial alleles. However, when selection pressures are highly variable along a species'' range or through time adaptive alleles may persist at intermediate frequencies for long periods. So called “balanced polymorphisms” have long been understood to be an important component of standing genetic variation, yet direct evidence of the strength of balancing selection and the stability and prevalence of balanced polymorphisms has remained elusive. We hypothesized that environmental fluctuations among seasons in a North American orchard would impose temporally variable selection on Drosophila melanogaster that would drive repeatable adaptive oscillations at balanced polymorphisms. We identified hundreds of polymorphisms whose frequency oscillates among seasons and argue that these loci are subject to strong, temporally variable selection. We show that these polymorphisms respond to acute and persistent changes in climate and are associated in predictable ways with seasonally variable phenotypes. In addition, our results suggest that adaptively oscillating polymorphisms are likely millions of years old, with some possibly predating the divergence between D. melanogaster and D. simulans. Taken together, our results are consistent with a model of balancing selection wherein rapid temporal fluctuations in climate over generational time promotes adaptive genetic diversity at loci underlying polygenic variation in fitness related phenotypes.     

Selection from parasites favours immunogenetic diversity but not divergence among locally adapted host populations

The unprecedented polymorphism in the major histocompatibility complex (MHC) genes is thought to be maintained by balancing selection from parasites. However, do parasites also drive divergence at MHC loci between host populations, or do the effects of balancing selection maintain similarities among populations? We examined MHC variation in populations of the livebearing fish Poecilia mexicana and characterized their parasite communities. Poecilia mexicana populations in the Cueva del Azufre system are locally adapted to darkness and the presence of toxic hydrogen sulphide, representing highly divergent ecotypes or incipient species. Parasite communities differed significantly across populations, and populations with higher parasite loads had higher levels of diversity at class II MHC genes. However, despite different parasite communities, marked divergence in adaptive traits and in neutral genetic markers, we found MHC alleles to be remarkably similar among host populations. Our findings indicate that balancing selection from parasites maintains immunogenetic diversity of hosts, but this process does not promote MHC divergence in this system. On the contrary, we suggest that balancing selection on immunogenetic loci may outweigh divergent selection causing divergence, thereby hindering host divergence and speciation. Our findings support the hypothesis that balancing selection maintains MHC similarities among lineages during and after speciation (trans‐species evolution).     

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.     

THE BIOLOGY OF SPECIATION

Since Darwin published the “Origin,” great progress has been made in our understanding of speciation mechanisms. The early investigations by Mayr and Dobzhansky linked Darwin's view of speciation by adaptive divergence to the evolution of reproductive isolation, and thus provided a framework for studying the origin of species. However, major controversies and questions remain, including: When is speciation nonecological? Under what conditions does geographic isolation constitute a reproductive isolating barrier? and How do we estimate the “importance” of different isolating barriers? Here, we address these questions, providing historical background and offering some new perspectives. A topic of great recent interest is the role of ecology in speciation. “Ecological speciation” is defined as the case in which divergent selection leads to reproductive isolation, with speciation under uniform selection, polyploid speciation, and speciation by genetic drift defined as “nonecological.” We review these proposed cases of nonecological speciation and conclude that speciation by uniform selection and polyploidy normally involve ecological processes. Furthermore, because selection can impart reproductive isolation both directly through traits under selection and indirectly through pleiotropy and linkage, it is much more effective in producing isolation than genetic drift. We thus argue that natural selection is a ubiquitous part of speciation, and given the many ways in which stochastic and deterministic factors may interact during divergence, we question whether the ecological speciation concept is useful. We also suggest that geographic isolation caused by adaptation to different habitats plays a major, and largely neglected, role in speciation. We thus provide a framework for incorporating geographic isolation into the biological species concept (BSC) by separating ecological from historical processes that govern species distributions, allowing for an estimate of geographic isolation based upon genetic differences between taxa. Finally, we suggest that the individual and relative contributions of all potential barriers be estimated for species pairs that have recently achieved species status under the criteria of the BSC. Only in this way will it be possible to distinguish those barriers that have actually contributed to speciation from those that have accumulated after speciation is complete. We conclude that ecological adaptation is the major driver of reproductive isolation, and that the term “biology of speciation,” as proposed by Mayr, remains an accurate and useful characterization of the diversity of speciation mechanisms.     

Genomics of speciation and introgression in Princess cichlid fishes from Lake Tanganyika

How variation in the genome translates into biological diversity and new species originate has endured as the mystery of mysteries in evolutionary biology. African cichlid fishes are prime model systems to address speciation‐related questions for their remarkable taxonomic and phenotypic diversity, and the possible role of gene flow in this process. Here, we capitalize on genome sequencing and phylogenomic analyses to address the relative impacts of incomplete lineage sorting, introgression and hybrid speciation in the Neolamprologus savoryi‐complex (the ‘Princess cichlids’) from Lake Tanganyika. We present a time‐calibrated species tree based on whole‐genome sequences and provide strong evidence for incomplete lineage sorting in the early phases of diversification and multiple introgression events affecting different stages. Importantly, we find that the Neolamprologus chromosomes show centre‐to‐periphery biases in nucleotide diversity, sequence divergence, GC content, incomplete lineage sorting and rates of introgression, which are likely modulated by recombination density and linked selection. The detection of heterogeneous genomic landscapes has strong implications on the genomic mechanisms involved in speciation. Collinear chromosomal regions can be protected from gene flow and harbour incompatibility genes if they reside in lowly recombining regions, and coupling can evolve between nonphysically linked genomic regions (chromosome centres in particular). Simultaneously, higher recombination towards chromosome peripheries makes these more dynamic, evolvable regions where adaptation polymorphisms have a fertile ground. Hence, differences in genome architecture could explain the levels of taxonomic and phenotypic diversity seen in taxa with collinear genomes and might have contributed to the spectacular cichlid diversity observed today.     

Tracking the progression of speciation: variable patterns of introgression across the genome provide insights on the species delimitation between progenitor–derivative spruces (Picea mariana × P. rubens)

The genic species concept implies that while most of the genome can be exchanged somewhat freely between species through introgression, some genomic regions remain impermeable to interspecific gene flow. Hence, interspecific differences can be maintained despite ongoing gene exchange within contact zones. This study assessed the heterogeneous patterns of introgression at gene loci across the hybrid zone of an incipient progenitor–derivative species pair, Picea mariana (black spruce) and Picea rubens (red spruce). The spruce taxa likely diverged in geographic isolation during the Pleistocene and came into secondary contact during late Holocene. A total of 300 SNPs distributed across the 12 linkage groups (LG) of black spruce were genotyped for 385 individual trees from 33 populations distributed across the allopatric zone of each species and within the zone of sympatry. An integrative framework combining three population genomic approaches was used to scan the genomes, revealing heterogeneous patterns of introgression. A total of 23 SNPs scattered over 10 LG were considered impermeable to introgression and putatively under diverging selection. These loci revealed the existence of impermeable genomic regions forming the species boundary and are thus indicative of ongoing speciation between these two genetic lineages. Another 238 SNPs reflected selectively neutral diffusion across the porous species barrier. Finally, 39 highly permeable SNPs suggested ancestral polymorphism along with balancing selection. The heterogeneous patterns of introgression across the genome indicated that the speciation process between black spruce and red spruce is young and incomplete, albeit some interspecific differences are maintained, allowing ongoing species divergence even in sympatry. The approach developed in this study can be used to track the progression of ongoing speciation processes.     

Genetic variability,local selection and demographic history: genomic evidence of evolving towards allopatric speciation in Asian seabass

Genomewide analysis of genetic divergence is critically important in understanding the genetic processes of allopatric speciation. We sequenced RAD tags of 131 Asian seabass individuals of six populations from South‐East Asia and Australia/Papua New Guinea. Using 32 433 SNPs, we examined the genetic diversity and patterns of population differentiation across all the populations. We found significant evidence of genetic heterogeneity between South‐East Asian and Australian/Papua New Guinean populations. The Australian/Papua New Guinean populations showed a rather lower level of genetic diversity. F_ST and principal components analysis revealed striking divergence between South‐East Asian and Australian/Papua New Guinean populations. Interestingly, no evidence of contemporary gene flow was observed. The demographic history was further tested based on the folded joint site frequency spectrum. The scenario of ancient migration with historical population size changes was suggested to be the best fit model to explain the genetic divergence of Asian seabass between South‐East Asia and Australia/Papua New Guinea. This scenario also revealed that Australian/Papua New Guinean populations were founded by ancestors from South‐East Asia during mid‐Pleistocene and were completely isolated from the ancestral population after the last glacial retreat. We also detected footprints of local selection, which might be related to differential ecological adaptation. The ancient gene flow was examined and deemed likely insufficient to counteract the genetic differentiation caused by genetic drift. The observed genomic pattern of divergence conflicted with the ‘genomic islands’ scenario. Altogether, Asian seabass have likely been evolving towards allopatric speciation since the split from the ancestral population during mid‐Pleistocene.     

Evidence of gene orthology and trans‐species polymorphism,but not of parallel evolution,despite high levels of concerted evolution in the major histocompatibility complex of flamingo species

The major histocompatibility complex (MHC) is a cornerstone in the study of adaptive genetic diversity. Intriguingly, highly polymorphic MHC sequences are often not more similar within species than between closely related species. Divergent selection of gene duplicates, balancing selection maintaining trans‐species polymorphism (TSP) that predate speciation and parallel evolution of species sharing similar selection pressures can all lead to higher sequence similarity between species. In contrast, high rates of concerted evolution increase sequence similarity of duplicated loci within species. Assessing these evolutionary models remains difficult as relatedness and ecological similarities are often confounded. As sympatric species of flamingos are more distantly related than allopatric species, flamingos represent an ideal model to disentangle these evolutionary models. We characterized MHC Class I exon 3, Class IIB exon 2 and exon 3 of the six extant flamingo species. We found up to six MHC Class I loci and two MHC Class IIB loci. As all six species shared the same number of MHC Class IIB loci, duplication appears to predate flamingo speciation. However, the high rate of concerted evolution has prevented the divergence of duplicated loci. We found high sequence similarity between all species regardless of codon position. The latter is consistent with balancing selection maintaining TSP, as under this mechanism amino acid sites under pathogen‐mediated selection should be characterized by fewer synonymous codons (due to their common ancestry) than under parallel evolution. Overall, balancing selection maintaining TSP appears to result in high MHC similarity between species regardless of species relatedness and geographical distribution.     

Estimating divergence time and ancestral effective population size of Bornean and Sumatran orangutan subspecies using a coalescent hidden Markov model

Due to genetic variation in the ancestor of two populations or two species, the divergence time for DNA sequences from two populations is variable along the genome. Within genomic segments all bases will share the same divergence-because they share a most recent common ancestor-when no recombination event has occurred to split them apart. The size of these segments of constant divergence depends on the recombination rate, but also on the speciation time, the effective population size of the ancestral population, as well as demographic effects and selection. Thus, inference of these parameters may be possible if we can decode the divergence times along a genomic alignment. Here, we present a new hidden Markov model that infers the changing divergence (coalescence) times along the genome alignment using a coalescent framework, in order to estimate the speciation time, the recombination rate, and the ancestral effective population size. The model is efficient enough to allow inference on whole-genome data sets. We first investigate the power and consistency of the model with coalescent simulations and then apply it to the whole-genome sequences of the two orangutan sub-species, Bornean (P. p. pygmaeus) and Sumatran (P. p. abelii) orangutans from the Orangutan Genome Project. We estimate the speciation time between the two sub-species to be thousand years ago and the effective population size of the ancestral orangutan species to be , consistent with recent results based on smaller data sets. We also report a negative correlation between chromosome size and ancestral effective population size, which we interpret as a signature of recombination increasing the efficacy of selection.     

Genomewide patterns of variation in genetic diversity are shared among populations,species and higher‐order taxa

Genomewide screens of genetic variation within and between populations can reveal signatures of selection implicated in adaptation and speciation. Genomic regions with low genetic diversity and elevated differentiation reflective of locally reduced effective population sizes (N_e) are candidates for barrier loci contributing to population divergence. Yet, such candidate genomic regions need not arise as a result of selection promoting adaptation or advancing reproductive isolation. Linked selection unrelated to lineage‐specific adaptation or population divergence can generate comparable signatures. It is challenging to distinguish between these processes, particularly when diverging populations share ancestral genetic variation. In this study, we took a comparative approach using population assemblages from distant clades assessing genomic parallelism of variation in N_e. Utilizing population‐level polymorphism data from 444 resequenced genomes of three avian clades spanning 50 million years of evolution, we tested whether population genetic summary statistics reflecting genomewide variation in N_e would covary among populations within clades, and importantly, also among clades where lineage sorting has been completed. All statistics including population‐scaled recombination rate (ρ), nucleotide diversity (π) and measures of genetic differentiation between populations (F_ST, PBS, d_xy) were significantly correlated across all phylogenetic distances. Moreover, genomic regions with elevated levels of genetic differentiation were associated with inferred pericentromeric and subtelomeric regions. The phylogenetic stability of diversity landscapes and stable association with genomic features support a role of linked selection not necessarily associated with adaptation and speciation in shaping patterns of genomewide heterogeneity in genetic diversity.     

Gene flow-dependent genomic divergence between Anopheles gambiae M and S forms

Anopheles gambiae sensu stricto exists as two often-sympatric races termed the M and S molecular forms, characterized by fixed differences at an X-linked marker. Extreme divergence between M and S forms at pericentromeric "genomic islands" suggested that selection on variants therein could be driving interform divergence in the presence of ongoing gene flow, but recent work has detected much more widespread genomic differentiation. Whether such genomic islands are important in reproductive isolation or represent ancestral differentiation preserved by low recombination is currently unclear. A critical test of these competing hypotheses could be provided by comparing genomic divergence when rates of recent introgression vary. We genotyped 871 single nucleotide polymorphisms (SNPs) in A. gambiae sensu stricto from locations of M and S sympatry and allopatry, encompassing the full range of observed hybridization rates (0-25%). M and S forms were readily partitioned based on genomewide SNP variation in spite of evidence for ongoing introgression that qualitatively reflects hybridization rates. Yet both the level and the heterogeneity of genomic divergence varied markedly in line with levels of introgression. A few genomic regions of differentiation between M and S were common to each sampling location, the most pronounced being two centromere-proximal speciation islands identified previously but with at least one additional region outside of areas expected to exhibit reduced recombination. Our results demonstrate that extreme divergence at genomic islands does not simply represent segregating ancestral polymorphism in regions of low recombination and can be resilient to substantial gene flow. This highlights the potential for islands comprising a relatively small fraction of the genome to play an important role in early-stage speciation when reproductive isolation is limited.     

Shared evolutionary origin of major histocompatibility complex polymorphism in sympatric lemurs

Genes of the major histocompatibility complex (MHC) play a central role in adaptive immune responses of vertebrates. They exhibit remarkable polymorphism, often crossing species boundaries with similar alleles or allelic motifs shared across species. This pattern may reflect parallel parasite‐mediated selective pressures, either favouring the long maintenance of ancestral MHC allelic lineages across successive speciation events by balancing selection (“trans‐species polymorphism”), or alternatively favouring the independent emergence of functionally similar alleles post‐speciation via convergent evolution. Here, we investigate the origins of MHC similarity across several species of dwarf and mouse lemurs (Cheirogaleidae). We examined MHC class II variation in two highly polymorphic loci (DRB, DQB) and evaluated the overlap of gut–parasite communities in four sympatric lemurs. We tested for parasite‐MHC associations across species to determine whether similar parasite pressures may select for similar MHC alleles in different species. Next, we integrated our MHC data with those previously obtained from other Cheirogaleidae to investigate the relative contribution of convergent evolution and co‐ancestry to shared MHC polymorphism by contrasting patterns of codon usage at functional vs. neutral sites. Our results indicate that parasites shared across species may select for functionally similar MHC alleles, implying that the dynamics of MHC‐parasite co‐evolution should be envisaged at the community level. We further show that balancing selection maintaining trans‐species polymorphism, rather than convergent evolution, is the primary mechanism explaining shared MHC sequence motifs between species that diverged up to 30 million years ago.     

Continental-Scale Footprint of Balancing and Positive Selection in a Small Rodent (Microtus arvalis)

Genetic adaptation to different environmental conditions is expected to lead to large differences between populations at selected loci, thus providing a signature of positive selection. Whereas balancing selection can maintain polymorphisms over long evolutionary periods and even geographic scale, thus leads to low levels of divergence between populations at selected loci. However, little is known about the relative importance of these two selective forces in shaping genomic diversity, partly due to difficulties in recognizing balancing selection in species showing low levels of differentiation. Here we address this problem by studying genomic diversity in the European common vole (Microtus arvalis) presenting high levels of differentiation between populations (average F _ST = 0.31). We studied 3,839 Amplified Fragment Length Polymorphism (AFLP) markers genotyped in 444 individuals from 21 populations distributed across the European continent and hence over different environmental conditions. Our statistical approach to detect markers under selection is based on a Bayesian method specifically developed for AFLP markers, which treats AFLPs as a nearly codominant marker system, and therefore has increased power to detect selection. The high number of screened populations allowed us to detect the signature of balancing selection across a large geographic area. We detected 33 markers potentially under balancing selection, hence strong evidence of stabilizing selection in 21 populations across Europe. However, our analyses identified four-times more markers (138) being under positive selection, and geographical patterns suggest that some of these markers are probably associated with alpine regions, which seem to have environmental conditions that favour adaptation. We conclude that despite favourable conditions in this study for the detection of balancing selection, this evolutionary force seems to play a relatively minor role in shaping the genomic diversity of the common vole, which is more influenced by positive selection and neutral processes like drift and demographic history.     

Model‐based demographic inference of introgression history in European whitefish species pairs'

Parallel phenotypic differentiation is generally attributed to parallel adaptive divergence as an evolutionary response to similar environmental contrasts. Such parallelism may actually originate from several evolutionary scenarios ranging from repeated parallel divergence caused by divergent selection to a unique divergence event followed by gene flow. Reconstructing the evolutionary history underlying parallel phenotypic differentiation is thus fundamental to understand the relative contribution of demography and selection on genomic divergence during speciation. In this study, we investigate the divergence history of replicate European whitefish (Coregonus lavaretus), limnetic and benthic species pairs from two lakes in Norway and two lakes in Switzerland. Demographic models accounting for semi‐permeability and linked selection were fitted to the unfolded joint allele frequency spectrum built from genome‐wide SNPs and compared to each other in each species pair. We found strong support for a model of asymmetrical post‐glacial secondary contact between glacial lineages in all four lakes. Moreover, our results suggest that heterogeneous genomic differentiation has been shaped by the joint action of linked selection accelerating lineage sorting during allopatry, and heterogeneous migration eroding divergence at different rates along the genome following secondary contact. Our analyses reveal how the interplay between demography, selection and historical contingency has influenced the levels of diversity observed in previous whitefish phylogeographic studies. This study thus provides new insights into the historical demographic and selective processes that shaped the divergence associated with ecological speciation in European whitefish.     

Evidence for widespread selection in shaping the genomic landscape during speciation of Populus

Increasing our understanding of how evolutionary processes drive the genomic landscape of variation is fundamental to a better understanding of the genomic consequences of speciation. However, genome‐wide patterns of within‐ and between‐ species variation have not been fully investigated in most forest tree species despite their global ecological and economic importance. Here, we use whole‐genome resequencing data from four Populus species spanning the speciation continuum to reconstruct their demographic histories and investigate patterns of diversity and divergence within and between species. Using Populus trichocarpa as an outgroup species, we further infer the genealogical relationships and estimate the extent of ancient introgression among the three aspen species (Populus tremula, Populus davidiana and Populus tremuloides) throughout the genome. Our results show substantial variation in these patterns along the genomes with this variation being strongly predicted by local recombination rates and the density of functional elements. This implies that the interaction between recurrent selection and intrinsic genomic features has dramatically sculpted the genomic landscape over long periods of time. In addition, our findings provide evidence that, apart from background selection, recent positive selection and long‐term balancing selection have also been crucial components in shaping patterns of genome‐wide variation during the speciation process.     

Signatures of balancing selection are maintained at disease resistance loci following mating system evolution and a population bottleneck in the genus Capsella

ABSTRACT: BACKGROUND: Population bottlenecks can lead to a loss of variation at disease resistance loci, which could have important consequences for the ability of populations to adapt to pathogen pressure. Alternatively, current or past balancing selection could maintain high diversity, creating a strong heterogeneity in the retention of polymorphism across the genome of bottlenecked populations. We sequenced part of the LRR region of 9 NBS-LRR disease resistance genes in the outcrossing Capsella grandiflora and the recently derived, bottlenecked selfing species Capsella rubella, and compared levels and patterns of nucleotide diversity and divergence with genome-wide reference loci. RESULTS: In strong contrast with reference loci, average diversity at resistance loci was comparable between C. rubella and C. grandiflora, primarily due to two loci with highly elevated diversity indicative of past or present balancing selection. Average between-species differentiation was also reduced at the set of R-genes compared with reference loci, which is consistent with the maintenance of ancestral polymorphism. CONCLUSIONS: Historical or ongoing balancing selection on plant disease resistance genes is a likely contributor to the retention of ancestral polymorphism in some regions of the bottlenecked Capella rubella genome.