Heterogeneous Genomic Differentiation Research Articles

Recurrent selection shapes the genomic landscape of differentiation between a pair of host-specialized haplodiploids that diverged with gene flow.

Understanding the genetics of adaptation and speciation is critical for a complete picture of how biodiversity is generated and maintained. Heterogeneous genomic differentiation between diverging taxa is commonly documented, with genomic regions of high differentiation interpreted as resulting from differential gene flow, linked selection and reduced recombination rates. Disentangling the roles of each of these non-exclusive processes in shaping genome-wide patterns of divergence is challenging but will enhance our knowledge of the repeatability of genomic landscapes across taxa. Here, we combine whole-genome resequencing and genome feature data to investigate the processes shaping the genomic landscape of differentiation for a sister-species pair of haplodiploid pine sawflies, Neodiprion lecontei and Neodiprion pinetum. We find genome-wide correlations between genome features and summary statistics are consistent with pervasive linked selection, with patterns of diversity and divergence more consistently predicted by exon density and recombination rate than the neutral mutation rate (approximated by dS). We also find that both global and local patterns of FST, dXY and π provide strong support for recurrent selection as the primary selective process shaping variation across pine sawfly genomes, with some contribution from balancing selection and lineage-specific linked selection. Because inheritance patterns for haplodiploid genomes are analogous to those of sex chromosomes, we hypothesize that haplodiploids may be especially prone to recurrent selection, even if gene flow occurred throughout divergence. Overall, our study helps fill an important taxonomic gap in the genomic landscape literature and contributes to our understanding of the processes that shape genome-wide patterns of genetic variation.

Genome architecture and diverged selection shaping pattern of genomic differentiation in wild barley.

Divergent selection of populations in contrasting environments leads to functional genomic divergence. However, the genomic architecture underlying heterogeneous genomic differentiation remains poorly understood. Here, we de novo assembled two high-quality wild barley (Hordeum spontaneum K. Koch) genomes and examined genomic differentiation and gene expression patterns under abiotic stress in two populations. These two populations had a shared ancestry and originated in close geographic proximity but experienced different selective pressures due to their contrasting micro-environments. We identified structural variants that may have played significant roles in affecting genes potentially associated with well-differentiated phenotypes such as flowering time and drought response between two wild barley genomes. Among them, a 29-bp insertion into the promoter region formed a cis-regulatory element in the HvWRKY45 gene, which may contribute to enhanced tolerance to drought. A single SNP mutation in the promoter region may influence HvCO5 expression and be putatively linked to local flowering time adaptation. We also revealed significant genomic differentiation between the two populations with ongoing gene flow. Our results indicate that SNPs and small SVs link to genetic differentiation at the gene level through local adaptation and are maintained through divergent selection. In contrast, large chromosome inversions may have shaped the heterogeneous pattern of genomic differentiation along the chromosomes by suppressing chromosome recombination and gene flow. Our research offers novel insights into the genomic basis underlying local adaptation and provides valuable resources for the genetic improvement of cultivated barley.

Faster-haplodiploid evolution under divergence-with-gene-flow: Simulations and empirical data from pine-feeding hymenopterans.

Although haplodiploidy is widespread in nature, the evolutionary consequences of this mode of reproduction are not well characterized. Here, we examine how genome-wide hemizygosity and a lack of recombination in haploid males affects genomic differentiation in populations that diverge via natural selection while experiencing gene flow. First, we simulated diploid and haplodiploid "genomes" (500-kb loci) evolving under an isolation-with-migration model with mutation, drift, selection, migration and recombination; and examined differentiation at neutral sites both tightly and loosely linked to a divergently selected site. As long as there is divergent selection and migration, sex-limited hemizygosity and recombination cause elevated differentiation (i.e., produce a "faster-haplodiploid effect") in haplodiploid populations relative to otherwise equivalent diploid populations, for both recessive and codominant mutations. Second, we used genome-wide single nucleotide polymorphism data to model divergence history and describe patterns of genomic differentiation between sympatric populations of Neodiprion lecontei and N. pinetum, a pair of pine sawfly species (order: Hymenoptera; family: Diprionidae) that are specialized on different pine hosts. These analyses support a history of continuous gene exchange throughout divergence and reveal a pattern of heterogeneous genomic differentiation that is consistent with divergent selection on many unlinked loci. Third, using simulations of haplodiploid and diploid populations evolving according to the estimated divergence history of N. lecontei and N. pinetum, we found that divergent selection would lead to higher differentiation in haplodiploids. Based on these results, we hypothesize that haplodiploids undergo divergence-with-gene-flow and sympatric speciation more readily than diploids.

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 >600,000years 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 FST =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 (1-3Mbp) 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.

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.

The genomic landscape at a late stage of stickleback speciation: High genomic divergence interspersed by small localized regions of introgression.

Speciation is a continuous process and analysis of species pairs at different stages of divergence provides insight into how it unfolds. Previous genomic studies on young species pairs have revealed peaks of divergence and heterogeneous genomic differentiation. Yet less known is how localised peaks of differentiation progress to genome-wide divergence during the later stages of speciation in the presence of persistent gene flow. Spanning the speciation continuum, stickleback species pairs are ideal for investigating how genomic divergence builds up during speciation. However, attention has largely focused on young postglacial species pairs, with little knowledge of the genomic signatures of divergence and introgression in older stickleback systems. The Japanese stickleback species pair, composed of the Pacific Ocean three-spined stickleback (Gasterosteus aculeatus) and the Japan Sea stickleback (G. nipponicus), which co-occur in the Japanese islands, is at a late stage of speciation. Divergence likely started well before the end of the last glacial period and crosses between Japan Sea females and Pacific Ocean males result in hybrid male sterility. Here we use coalescent analyses and Approximate Bayesian Computation to show that the two species split approximately 0.68–1 million years ago but that they have continued to exchange genes at a low rate throughout divergence. Population genomic data revealed that, despite gene flow, a high level of genomic differentiation is maintained across the majority of the genome. However, we identified multiple, small regions of introgression, occurring mainly in areas of low recombination rate. Our results demonstrate that a high level of genome-wide divergence can establish in the face of persistent introgression and that gene flow can be localized to small genomic regions at the later stages of speciation with gene flow.

Genomic differentiation and patterns of gene flow between two long-tailed tit species (Aegithalos).

Patterns of heterogeneous genomic differentiation have been well documented between closely related species, with some highly differentiated genomic regions ("genomic differentiation islands") spread throughout the genome. Differential levels of gene flow are proposed to account for this pattern, as genomic differentiation islands are suggested to be resistant to gene flow. Recent studies have also suggested that genomic differentiation islands could be explained by linked selection acting on genomic regions with low recombination rates. Here, we investigate genomic differentiation and gene-flow patterns for autosomes using RAD-seq data between two closely related species of long-tailed tits (Aegithalos bonvaloti and A.fuliginosus) in both allopatric and contact zone populations. The results confirm recent or ongoing gene flow between these two species. However, there is little evidence that the genomic regions that were found to be highly differentiated between the contact zone populations are resistant to gene flow, suggesting that differential levels of gene flow is not the cause of the heterogeneous genomic differentiation. Linked selection may be the cause of genomic differentiation islands between the allopatric populations with no or very limited gene flow, but this could not account for the heterogeneous genomic differentiation between the contact zone populations, which show evidence of recent or ongoing gene flow.

Modeling the Multiple Facets of Speciation-with-Gene-Flow toward Inferring the Divergence History of Lake Whitefish Species Pairs (Coregonus clupeaformis).

Parallel divergence across replicated species pairs occurring in similar environmental contrasts may arise through distinct evolutionary scenarios. Deciphering whether such parallelism actually reflects repeated parallel divergence driven by divergent selection or a single divergence event with subsequent gene flow needs to be ascertained. Reconstructing historical gene flow is therefore of fundamental interest to understand how demography and selection jointly shaped genomic divergence during speciation. Here, we use an extended modeling framework to explore the multiple facets of speciation-with-gene-flow with demo-genetic divergence models that capture both temporal and genomic variation in effective population size and migration rate. We investigate the divergence history of replicate sympatric species pairs of Lake Whitefish (normal benthic and dwarf limnetic) characterized by variable degrees of ecological divergence and reproductive isolation. Genome-wide SNPs were used to document the extent of genetic differentiation in each species pair, and 26 divergence models were fitted and compared with the unfolded joint allele frequency spectrum of each pair. We found evidence that a recent (circa 3,000–4,000 generations) asymmetrical secondary contact between expanding postglacial populations has accompanied Whitefish diversification. Our results suggest that heterogeneous genomic differentiation has emerged through the combined effects of linked selection generating variable rates of lineage sorting across the genome during geographical isolation, and heterogeneous introgression eroding divergence at different rates across the genome upon secondary contact. This study thus provides a new retrospective insight into the historical demographic and selective processes that shaped a continuum of divergence associated with ecological speciation.

Genetic structure and signatures of selection in grey reef sharks (Carcharhinus amblyrhynchos).

With overfishing reducing the abundance of marine predators in multiple marine ecosystems, knowledge of genetic structure and local adaptation may provide valuable information to assist sustainable management. Despite recent technological advances, most studies on sharks have used small sets of neutral markers to describe their genetic structure. We used 5517 nuclear single-nucleotide polymorphisms (SNPs) and a mitochondrial DNA (mtDNA) gene to characterize patterns of genetic structure and detect signatures of selection in grey reef sharks (Carcharhinus amblyrhynchos). Using samples from Australia, Indonesia and oceanic reefs in the Indian Ocean, we established that large oceanic distances represent barriers to gene flow, whereas genetic differentiation on continental shelves follows an isolation by distance model. In Australia and Indonesia differentiation at nuclear SNPs was weak, with coral reefs acting as stepping stones maintaining connectivity across large distances. Differentiation of mtDNA was stronger, and more pronounced in females, suggesting sex-biased dispersal. Four independent tests identified a set of loci putatively under selection, indicating that grey reef sharks in eastern Australia are likely under different selective pressures to those in western Australia and Indonesia. Genetic distances averaged across all loci were uncorrelated with genetic distances calculated from outlier loci, supporting the conclusion that different processes underpin genetic divergence in these two data sets. This pattern of heterogeneous genomic differentiation, suggestive of local adaptation, has implications for the conservation of grey reef sharks; furthermore, it highlights that marine species showing little genetic differentiation at neutral loci may exhibit patterns of cryptic genetic structure driven by local selection.

Inferring the demographic history underlying parallel genomic divergence among pairs of parasitic and nonparasitic lamprey ecotypes.

Understanding the evolutionary mechanisms generating parallel genomic divergence patterns among replicate ecotype pairs remains an important challenge in speciation research. We investigated the genomic divergence between the anadromous parasitic river lamprey (Lampetra fluviatilis) and the freshwater-resident nonparasitic brook lamprey (Lampetra planeri) in nine population pairs displaying variable levels of geographic connectivity. We genotyped 338 individuals with RAD sequencing and inferred the demographic divergence history of each population pair using a diffusion approximation method. Divergence patterns in geographically connected population pairs were better explained by introgression after secondary contact, whereas disconnected population pairs have retained a signal of ancient migration. In all ecotype pairs, models accounting for differential introgression among loci outperformed homogeneous migration models. Generating neutral predictions from the inferred divergence scenarios to detect highly differentiated markers identified greater proportions of outliers in disconnected population pairs than in connected pairs. However, increased similarity in the most divergent genomic regions was found among connected ecotype pairs, indicating that gene flow was instrumental in generating parallelism at the molecular level. These results suggest that heterogeneous genomic differentiation and parallelism among replicate ecotype pairs have partly emerged through restricted introgression in genomic islands.

Variation in Linked Selection and Recombination Drive Genomic Divergence during Allopatric Speciation of European and American Aspens.

Despite the global economic and ecological importance of forest trees, the genomic basis of differential adaptation and speciation in tree species is still poorly understood. Populus tremula and Populus tremuloides are two of the most widespread tree species in the Northern Hemisphere. Using whole-genome re-sequencing data of 24 P. tremula and 22 P. tremuloides individuals, we find that the two species diverged ∼2.2–3.1 million years ago, coinciding with the severing of the Bering land bridge and the onset of dramatic climatic oscillations during the Pleistocene. Both species have experienced substantial population expansions following long-term declines after species divergence. We detect widespread and heterogeneous genomic differentiation between species, and in accordance with the expectation of allopatric speciation, coalescent simulations suggest that neutral evolutionary processes can account for most of the observed patterns of genetic differentiation. However, there is an excess of regions exhibiting extreme differentiation relative to those expected under demographic simulations, which is indicative of the action of natural selection. Overall genetic differentiation is negatively associated with recombination rate in both species, providing strong support for a role of linked selection in generating the heterogeneous genomic landscape of differentiation between species. Finally, we identify a number of candidate regions and genes that may have been subject to positive and/or balancing selection during the speciation process.

Population genomic evidence for adaptive differentiation in Baltic Sea three-spined sticklebacks.

BackgroundThe degree of genetic differentiation among populations experiencing high levels of gene flow is expected to be low for neutral genomic sites, but substantial divergence can occur in sites subject to directional selection. Studies of highly mobile marine fish populations provide an opportunity to investigate this kind of heterogeneous genomic differentiation, but most studies to this effect have focused on a relatively low number of genetic markers and/or few populations. Hence, the patterns and extent of genomic divergence in high-gene-flow marine fish populations remain poorly understood.ResultsWe here investigated genome-wide patterns of genetic variability and differentiation in ten marine populations of three-spined stickleback (Gasterosteus aculeatus) distributed across a steep salinity and temperature gradient in the Baltic Sea, by utilizing >30,000 single nucleotide polymorphisms obtained with a pooled RAD-seq approach. We found that genetic diversity and differentiation varied widely across the genome, and identified numerous fairly narrow genomic regions exhibiting signatures of both divergent and balancing selection. Evidence was uncovered for substantial genetic differentiation associated with both salinity and temperature gradients, and many candidate genes associated with local adaptation in the Baltic Sea were identified.ConclusionsThe patterns of genetic diversity and differentiation, as well as candidate genes associated with adaptation, in Baltic Sea sticklebacks were similar to those observed in earlier comparisons between marine and freshwater populations, suggesting that similar processes may be driving adaptation to brackish and freshwater environments. Taken together, our results provide strong evidence for heterogenic genomic divergence driven by local adaptation in the face of gene flow along an environmental gradient in the post-glacially formed Baltic Sea.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0130-8) contains supplementary material, which is available to authorized users.

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 FST 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.

SNP signatures of selection on standing genetic variation and their association with adaptive phenotypes along gradients of ecological speciation in lake whitefish species pairs (Coregonus spp.)

As populations adapt to novel environments, divergent selection will promote heterogeneous genomic differentiation via reductions in gene flow for loci underlying adaptive traits. Using a data set of over 100 SNP markers, genome scans were performed to investigate the effect of natural selection maintaining differentiation in five lakes harbouring sympatric pairs of normal and dwarf lake whitefish (Coregonus clupeaformis). A variable proportion of SNPs (between 0% and 12%) was identified as outliers, which corroborated the predicted intensity of competitive interactions unique to each lake. Moreover, strong reduction in heterozygosity was typically observed for outlier loci in dwarf but not in normal whitefish, indicating that directional selection has been acting on standing genetic variation more intensively in dwarf whitefish. SNP associations in backcross hybrid progeny identified 16 genes exhibiting genotype-phenotype associations for four adaptive traits (growth, swimming activity, gill rakers and condition factor). However, neither simple relationship between elevated levels of genetic differentiation with adaptive phenotype nor conspicuous genetic signatures for parallelism at outlier loci were detected, which underscores the importance of independent evolution among lakes. The integration of phenotypic, transcriptomic and functional genomic information identified two candidate genes (sodium potassium ATPase and triosephosphate isomerase) involved in the recent ecological divergence of lake whitefish. Finally, the identification of several markers under divergent selection suggests that many genes, in an environment-specific manner, are recruited by selection and ultimately contributed to the repeated ecological speciation of a dwarf phenotype.

HETEROGENEOUS GENOMIC DIFFERENTIATION BETWEEN WALKING-STICK ECOTYPES: "ISOLATION BY ADAPTATION" AND MULTIPLE ROLES FOR DIVERGENT SELECTION

Genetic differentiation can be highly variable across the genome. For example, loci under divergent selection and those tightly linked to them may exhibit elevated differentiation compared to neutral regions. These represent "outlier loci" whose differentiation exceeds neutral expectations. Adaptive divergence can also increase genome-wide differentiation by promoting general barriers to neutral gene flow, thereby facilitating genomic divergence via genetic drift. This latter process can yield a positive correlation between adaptive phenotypic divergence and neutral genetic differentiation (described here as "isolation-by-adaptation"). Here, we examine both these processes by combining an AFLP genome scan of two host plant ecotypes of Timema cristinae walking-sticks with existing data on adaptive phenotypic divergence and ecological speciation in these insects. We found that about 8% of loci are outliers in multiple population comparisons. Replicated comparisons between population-pairs using the same versus different host species revealed that 1-2% of loci are subject to host-related selection specifically. Locus-specific analyses revealed that up to 10% of putatively neutral (nonoutlier) AFLP loci exhibit significant isolation-by-adaptation. Our results suggest that selection may affect differentiation directly, via linkage, or by facilitating genetic drift. They thus illustrate the varied and sometimes nonintuitive contributions of selection to heterogeneous genomic differentiation.

Sex-biased dispersal in a salmonid fish.

We tested the hypothesis that dispersal is sex biased in an unexploited population of brook trout, Salvelinus fontinalis, on Cape Race, Newfoundland, Canada. Based on the assumptions that trout are promiscuous and that reproductive success is limited primarily by either number of mates (males) or fecundity (females), we predicted that males would disperse greater distances than females. We also tested the hypothesis that trout populations comprise stationary and mobile individuals, predicting that males have greater mobility than females. Based on a mark-recapture study of 943 individually tagged fishes, 191 of which were recaptured over 5 years, we find strong support for our hypothesis of male-biased dispersal in brook trout. Averaged among all 11 resampling periods, males dispersed 2.5 times as far as females; during the spawning period only, male dispersal exceeded that by females almost fourfold. Both sexes were heterogeneous with respect to movement, with a lower incidence of mobility among females (29.6%) than males (41.1%); mobile males dispersed six times further than mobile females. We conclude that this sex bias reduces mate competition among male kin and decreases the probability that males will reproduce with related females.