Genetic Barriers to Historical Gene Flow between Cryptic Species of Alpine Bumblebees Revealed by Comparative Population Genomics

Evidence is accumulating that gene flow commonly occurs between recently diverged species, despite the existence of barriers to gene flow in their genomes. However, we still know little about what regions of the genome become barriers to gene flow and how such barriers form. Here, we compare genetic differentiation across the genomes of bumblebee species living in sympatry and allopatry to reveal the potential impact of gene flow during species divergence and uncover genetic barrier loci. We first compared the genomes of the alpine bumblebee Bombus sylvicola and a previously unidentified sister species living in sympatry in the Rocky Mountains, revealing prominent islands of elevated genetic divergence in the genome that colocalize with centromeres and regions of low recombination. This same pattern is observed between the genomes of another pair of closely related species living in allopatry (B. bifarius and B. vancouverensis). Strikingly however, the genomic islands exhibit significantly elevated absolute divergence (d_XY) in the sympatric, but not the allopatric, comparison indicating that they contain loci that have acted as barriers to historical gene flow in sympatry. Our results suggest that intrinsic barriers to gene flow between species may often accumulate in regions of low recombination and near centromeres through processes such as genetic hitchhiking, and that divergence in these regions is accentuated in the presence of gene flow.     

Biases in Demographic Modeling Affect Our Understanding of Recent Divergence

Testing among competing demographic models of divergence has become an important component of evolutionary research in model and non-model organisms. However, the effect of unaccounted demographic events on model choice and parameter estimation remains largely unexplored. Using extensive simulations, we demonstrate that under realistic divergence scenarios, failure to account for population size (N_e) changes in daughter and ancestral populations leads to strong biases in divergence time estimates as well as model choice. We illustrate these issues reconstructing the recent demographic history of North Sea and Baltic Sea turbots (Scophthalmus maximus) by testing 16 isolation with migration (IM) and 16 secondary contact (SC) scenarios, modeling changes in N_e as well as the effects of linked selection and barrier loci. Failure to account for changes in N_e resulted in selecting SC models with long periods of strict isolation and divergence times preceding the formation of the Baltic Sea. In contrast, models accounting for N_e changes suggest recent (<6 kya) divergence with constant gene flow. We further show how interpreting genomic landscapes of differentiation can help discerning among competing models. For example, in the turbot data, islands of differentiation show signatures of recent selective sweeps, rather than old divergence resisting secondary introgression. The results have broad implications for the study of population divergence by highlighting the potential effects of unmodeled changes in N_e on demographic inference. Tested models should aim at representing realistic divergence scenarios for the target taxa, and extreme caution should always be exercised when interpreting results of demographic modeling.     

Genetic Divergence and Signatures of Natural Selection in Marginal Populations of a Keystone,Long-Lived Conifer,Eastern White Pine (Pinus strobus) from Northern Ontario

Marginal populations are expected to provide the frontiers for adaptation, evolution and range shifts of plant species under the anticipated climate change conditions. Marginal populations are predicted to show genetic divergence from central populations due to their isolation, and divergent natural selection and genetic drift operating therein. Marginal populations are also expected to have lower genetic diversity and effective population size (N _e) and higher genetic differentiation than central populations. We tested these hypotheses using eastern white pine (Pinus strobus) as a model for keystone, long-lived widely-distributed plants. All 614 eastern white pine trees, in a complete census of two populations each of marginal old-growth, central old-growth, and central second-growth, were genotyped at 11 microsatellite loci. The central populations had significantly higher allelic and genotypic diversity, latent genetic potential (LGP) and N _e than the marginal populations. However, heterozygosity and fixation index were similar between them. The marginal populations were genetically diverged from the central populations. Model testing suggested predominant north to south gene flow in the study area with curtailed gene flow to northern marginal populations. Signatures of natural selection were detected at three loci in the marginal populations; two showing divergent selection with directional change in allele frequencies, and one balancing selection. Contrary to the general belief, no significant differences were observed in genetic diversity, differentiation, LGP, and N _e between old-growth and second-growth populations. Our study provides information on the dynamics of migration, genetic drift and selection in central versus marginal populations of a keystone long-lived plant species and has broad evolutionary, conservation and adaptation significance.     

Localizing FST outliers on a QTL map reveals evidence for large genomic regions of reduced gene exchange during speciation‐with‐gene‐flow

Populations that maintain phenotypic divergence in sympatry typically show a mosaic pattern of genomic divergence, requiring a corresponding mosaic of genomic isolation (reduced gene flow). However, mechanisms that could produce the genomic isolation required for divergence‐with‐gene‐flow have barely been explored, apart from the traditional localized effects of selection and reduced recombination near centromeres or inversions. By localizing F_ST outliers from a genome scan of wild pea aphid host races on a Quantitative Trait Locus (QTL) map of key traits, we test the hypothesis that between‐population recombination and gene exchange are reduced over large ‘divergence hitchhiking’ (DH) regions. As expected under divergence hitchhiking, our map confirms that QTL and divergent markers cluster together in multiple large genomic regions. Under divergence hitchhiking, the nonoutlier markers within these regions should show signs of reduced gene exchange relative to nonoutlier markers in genomic regions where ongoing gene flow is expected. We use this predicted difference among nonoutliers to perform a critical test of divergence hitchhiking. Results show that nonoutlier markers within clusters of F_ST outliers and QTL resolve the genetic population structure of the two host races nearly as well as the outliers themselves, while nonoutliers outside DH regions reveal no population structure, as expected if they experience more gene flow. These results provide clear evidence for divergence hitchhiking, a mechanism that may dramatically facilitate the process of speciation‐with‐gene‐flow. They also show the power of integrating genome scans with genetic analyses of the phenotypic traits involved in local adaptation and population divergence.     

Genetic Variability and Structuring of Arctic Charr (Salvelinus alpinus) Populations in Northern Fennoscandia

Variation in presumably neutral genetic markers can inform us about evolvability, historical effective population sizes and phylogeographic history of contemporary populations. We studied genetic variability in 15 microsatellite loci in six native landlocked Arctic charr (Salvelinus alpinus) populations in northern Fennoscandia, where this species is considered near threatened. We discovered that all populations were genetically highly (mean F _ST ≈ 0.26) differentiated and isolated from each other. Evidence was found for historical, but not for recent population size bottlenecks. Estimates of contemporary effective population size (N _e) ranged from seven to 228 and were significantly correlated with those of historical N _e but not with lake size. A census size (N _C) was estimated to be approximately 300 individuals in a pond (0.14 ha), which exhibited the smallest N _e (i.e. N _e/N _C = 0.02). Genetic variability in this pond and a connected lake is severely reduced, and both genetic and empirical estimates of migration rates indicate a lack of gene flow between them. Hence, albeit currently thriving, some northern Fennoscandian populations appear to be vulnerable to further loss of genetic variability and are likely to have limited capacity to adapt if selection pressures change.     

Interspecific hybridization contributes to high genetic diversity and apparent effective population size in an endemic population of mottled ducks (Anas fulvigula maculosa)

Under drift-mutation equilibrium, genetic diversity is expected to be correlated with effective population size (N _e ). Changes in population size and gene flow are two important processes that can cause populations to deviate from this expected relationship. In this study, we used DNA sequences from six independent loci to examine the influence of these processes on standing genetic diversity in endemic mottled ducks (Anas fulvigula) and geographically widespread mallards (A. platyrhynchos), two species known to hybridize. Mottled ducks have an estimated census size that is about two orders-of-magnitude smaller than that of mallards, yet these two species have similar levels of genetic diversity, especially at nuclear DNA. Coalescent analyses suggest that a population expansion in the mallard at least partly explains this discrepancy, but the mottled duck harbors higher genetic diversity and apparent N _e than expected for its census size even after accounting for a population decline. Incorporating gene flow into the model, however, reduced the estimated N _e of mottled ducks to 33 % of the equilibrium N _e and yielded an estimated N _e consistent with census size. We also examined the utility of these loci to distinguish among mallards, mottled ducks, and their hybrids. Most putatively pure individuals were correctly assigned to species, but the power for detecting hybrids was low. Although hybridization with mallards potentially poses a conservation threat to mottled ducks by creating a risk of extinction by hybridization, introgression of mallard alleles has helped maintain high genetic diversity in mottled ducks and might be important for the adaptability and survival of this species.     

Did Genetic Drift Drive Increases in Genome Complexity?

Mechanisms underlying the dramatic patterns of genome size variation across the tree of life remain mysterious. Effective population size (N_e) has been proposed as a major driver of genome size: selection is expected to efficiently weed out deleterious mutations increasing genome size in lineages with large (but not small) N_e. Strong support for this model was claimed from a comparative analysis of N_eu and genome size for ≈30 phylogenetically diverse species ranging from bacteria to vertebrates, but analyses at that scale have so far failed to account for phylogenetic nonindependence of species. In our reanalysis, accounting for phylogenetic history substantially altered the perceived strength of the relationship between N_eu and genomic attributes: there were no statistically significant associations between N_eu and gene number, intron size, intron number, the half-life of gene duplicates, transposon number, transposons as a fraction of the genome, or overall genome size. We conclude that current datasets do not support the hypothesis of a mechanistic connection between N_e and these genomic attributes, and we suggest that further progress requires larger datasets, phylogenetic comparative methods, more robust estimators of genetic drift, and a multivariate approach that accounts for correlations between putative explanatory variables.     

Phylogenetic relationships among the European and American bison and seven cattle breeds reconstructed using the BovineSNP50 Illumina Genotyping BeadChip

Here we present the first attempt to use the BovineSNP50 Illumina Genotyping BeadChip for genome-wide screening of European bison Bison bonasus bonasus (EB), two subspecies of American bison: the plains bison Bison bison bison (PB), the wood bison Bison bison athabascae (WB) and seven cattle Bos taurus breeds. Our aims were to (1) reconstruct their evolutionary relationships, (2) detect any genetic signature of past bottlenecks and to quantify the consequences of bottlenecks on the genetic distances amongst bison subspecies and cattle, and (3) detect loci under positive or stabilizing selection. A Bayesian clustering procedure (STRUCTURE) detected ten genetically distinct clusters, with separation among all seven cattle breeds and European and American bison, but no separation between plain and wood bison. A linkage disequilibrium based program (LDNE) was used to estimate the effective population size (N _e) for the cattle breeds; N _e was generally low, relative to the census size of the breeds (cattle breeds: mean N _e = 299.5, min N _e = 18.1, max N _e = 755.0). BOTTLENECK 1.2 detected signs of population bottlenecks in EB, PB and WB populations (sign test and standardized sign test: p = 0.0001). Evidence for loci under selection was found in cattle but not in bison. All extant wild populations of bison have shown to have survived severe bottlenecks, which has likely had large effects on genetic diversity within and differentiation among groups.     

Contrasting patterns of introgression at X-linked loci across the hybrid zone between subspecies of the European rabbit (Oryctolagus cuniculus)

Hybrid zones provide an excellent opportunity for studying the consequences of genetic changes between closely related taxa. Here we investigate patterns of genetic variability and gene flow at four X-linked loci within and between the two subspecies of European rabbit (Oryctolagus cuniculus cuniculus and O. c. algirus). Two of these genes are located near the centromere and two are located near the telomeres. We observed a deep split in the genealogy of each gene with the root located along the deepest branch in each case, consistent with the evolution of these subspecies in allopatry. The two centromeric loci showed low levels of variability, high levels of linkage disequilibrium, and little introgression between subspecies. In contrast, the two telomeric loci showed high levels of variability, low levels of linkage disequilibrium, and considerable introgression between subspecies. These data are consistent with suppression of recombination near the centromere of the rabbit X chromosome. These observations support a view of speciation where genomic incompatibilities at different loci in the genome create localized differences in levels of gene flow between nascent species.     

GENE FLOW AND MITOCHONDRIAL DNA VARIATION IN THE KILLIFISH,FUNDULUS HETEROCLITUS

Two subspecies of killifish, Fundulus heteroclitus, inhabit the Atlantic coast of the United States. The contact zones between them are typified by morphological, physiological, nuclear gene, and mitochondrial DNA clines. Considerable debate exists about the importance of restricted gene flow and natural selection in maintaining these clines. To evaluate the relative importance of these two evolutionary forces we employed analysis of mtDNA as an independent measure of gene flow. Solutions of equilibrium diffusion equations suggested that killifish dispersal must be less than 2 km to maintain previously observed allozyme frequency clines in the absence of strong selection. To determine whether populations separated by distances greater than 2 km accumulate significant genetic differences we examined a total of N = 480 individuals from five killifish populations spanning a continuous shoreline distance of 8.4 km. Distribution of the 25 detected haplotypes indicated that most of the variation was within rather than between sampling locations. No evidence of geographic structure was detected, nor were there any significant genetic differences between killifish populations. With these data, gene flow was evaluated by estimating effective migration rate (N_em) between the populations. N_em was estimated from G_st(N_em = 49.4), from F_st (N_em = 24.1), by the private alleles approach (N_em = 18.5) and via four phylogenetic analyses (N_em ranged from 11.4 to 16.9). Regardless of the analysis, N_em was greater than one; the threshold level at which gene flow is strong enough to prevent differentiation due to genetic drift. This suggests that while the characteristics that distinguish Fundulus subspecies may have arisen in isolation, the current clinal distributions exhibited along the Atlantic coast are most likely maintained by selection.     

Higher differentiation among subspecies of the house mouse (Mus musculus) in genomic regions with low recombination

In the early stages of reproductive isolation, genomic regions of reduced recombination are expected to show greater levels of differentiation, either because gene flow between species is reduced in these regions or because the effects of selection at linked sites within species are enhanced in these regions. Here, we study the patterns of DNA sequence variation at 27 autosomal loci among populations of Mus musculus musculus, M. m. domesticus, and M. m. castaneus, three subspecies of house mice with collinear genomes. We found that some loci exhibit considerable shared variation among subspecies, while others exhibit fixed differences. We used an isolation-with-gene-flow model to estimate divergence times and effective population sizes (N(e) ) and to disentangle ancestral variation from gene flow. Estimates of divergence time indicate that all three subspecies diverged from one another within a very short period of time approximately 350,000 years ago. Overall, N(e) for each subspecies was associated with the degree of genetic differentiation: M. m. musculus had the smallest N(e) and the greatest proportion of monophyletic gene genealogies, while M. m. castaneus had the largest N(e) and the smallest proportion of monophyletic gene genealogies. M. m. domesticus and M. m. musculus were more differentiated from each other than either were from M. m. castaneus, consistent with greater reproductive isolation between M. m. domesticus and M. m. musculus. F(ST) was significantly greater at loci experiencing low recombination rates compared to loci experiencing high recombination rates in comparisons between M. m. castaneus and M. m. musculus or M. m. domesticus. These results provide evidence that genomic regions with less recombination show greater differentiation, even in the absence of chromosomal rearrangements.     

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.     

Taking multiple infections of cells and recombination into account leads to small within-host effective-population-size estimates of HIV-1

Whether HIV-1 evolution in infected individuals is dominated by deterministic or stochastic effects remains unclear because current estimates of the effective population size of HIV-1 in vivo, N_e, are widely varying. Models assuming HIV-1 evolution to be neutral estimate N_e∼10²–10⁴, smaller than the inverse mutation rate of HIV-1 (∼10⁵), implying the predominance of stochastic forces. In contrast, a model that includes selection estimates N_e>10⁵, suggesting that deterministic forces would hold sway. The consequent uncertainty in the nature of HIV-1 evolution compromises our ability to describe disease progression and outcomes of therapy. We perform detailed bit-string simulations of viral evolution that consider large genome lengths and incorporate the key evolutionary processes underlying the genomic diversification of HIV-1 in infected individuals, namely, mutation, multiple infections of cells, recombination, selection, and epistatic interactions between multiple loci. Our simulations describe quantitatively the evolution of HIV-1 diversity and divergence in patients. From comparisons of our simulations with patient data, we estimate N_e∼10³–10⁴, implying predominantly stochastic evolution. Interestingly, we find that N_e and the viral generation time are correlated with the disease progression time, presenting a route to a priori prediction of disease progression in patients. Further, we show that the previous estimate of N_e>10⁵ reduces as the frequencies of multiple infections of cells and recombination assumed increase. Our simulations with N_e∼10³–10⁴ may be employed to estimate markers of disease progression and outcomes of therapy that depend on the evolution of viral diversity and divergence.     

The estimates of effective population size based on linkage disequilibrium are virtually unaffected by natural selection

The effective population size (N_e) is a key parameter to quantify the magnitude of genetic drift and inbreeding, with important implications in human evolution. The increasing availability of high-density genetic markers allows the estimation of historical changes in N_e across time using measures of genome diversity or linkage disequilibrium between markers. Directional selection is expected to reduce diversity and N_e, and this reduction is modulated by the heterogeneity of the genome in terms of recombination rate. Here we investigate by computer simulations the consequences of selection (both positive and negative) and recombination rate heterogeneity in the estimation of historical N_e. We also investigate the relationship between diversity parameters and N_e across the different regions of the genome using human marker data. We show that the estimates of historical N_e obtained from linkage disequilibrium between markers (N_eLD) are virtually unaffected by selection. In contrast, those estimates obtained by coalescence mutation-recombination-based methods can be strongly affected by it, which could have important consequences for the estimation of human demography. The simulation results are supported by the analysis of human data. The estimates of N_eLD obtained for particular genomic regions do not correlate, or they do it very weakly, with recombination rate, nucleotide diversity, proportion of polymorphic sites, background selection statistic, minor allele frequency of SNPs, loss of function and missense variants and gene density. This suggests that N_eLD measures mainly reflect demographic changes in population size across generations.     

Multi-locus inference of population structure: a comparison between single nucleotide polymorphisms and microsatellites

Although growing numbers of single nucleotide polymorphisms (SNPs) and microsatellites (short tandem repeat polymorphisms or STRPs) are used to infer population structure, their relative properties in this context remain poorly understood. SNPs and STRPs mutate differently, suggesting multi-locus genotypes at these loci might differ in ability to detect population structure. Here, we use coalescent simulations to measure the power of sets of SNPs and STRPs to identify population structure. To maximize the applicability of our results to empirical studies, we focus on the popular STRUCTURE analysis and evaluate the role of several biological and practical factors in the detection of population structure. We find that: (1) fewer unlinked STRPs than SNPs are needed to detect structure at recent divergence times <0.3 N_e generations; (2) accurate estimation of the number of populations requires many fewer STRPs than SNPs; (3) for both marker types, declines in power due to modest gene flow (N_em=1.0) are largely negated by increasing marker number; (4) variation in the STRP mutational model affects power modestly; (5) SNP haplotypes (θ=1, no recombination) provide power comparable with STRP loci (θ=10); (6) ascertainment schemes that select highly variable STRP or SNP loci increase power to detect structure, though ascertained data may not be suitable to other inference; and (7) when samples are drawn from an admixed population and one of its parent populations, the reduction in power to detect two populations is greater for STRPs than SNPs. These results should assist the design of multi-locus studies to detect population structure in nature.     

An extensive candidate gene approach to speciation: diversity,divergence and linkage disequilibrium in candidate pigmentation genes across the European crow hybrid zone

Colouration patterns have an important role in adaptation and speciation. The European crow system, in which all-black carrion crows and grey-coated hooded crows meet in a narrow hybrid zone, is a prominent example. The marked phenotypic difference is maintained by assortative mating in the absence of neutral genetic divergence, suggesting the presence of few pigmentation genes of major effect. We made use of the rich phenotypic and genetic resources in mammals and identified a comprehensive panel of 95 candidate pigmentation genes for birds. Based on functional annotation, we chose a subset of the most promising 37 candidates, for which we developed a marker system that demonstrably works across the avian phylogeny. In total, we sequenced 107 amplicons (∼3 loci per gene, totalling 60 kb) in population samples of crows (n=23 for each taxon). Tajima''s D, Fu''s F_S, DHEW and HKA (Hudson–Kreitman–Aguade) statistics revealed several amplicons that deviated from neutrality; however, none of these showed significantly elevated differentiation between the two taxa. Hence, colour divergence in this system may be mediated by uncharacterized pigmentation genes or regulatory regions outside genes. Alternatively, the observed high population recombination rate (4N_er∼0.03), with overall linkage disequilibrium dropping rapidly within the order of few 100 bp, may compromise the power to detect causal loci with nearby markers. Our results add to the debate as to the utility of candidate gene approaches in relation to genomic features and the genetic architecture of the phenotypic trait in question.     

Phenotypic Variation across Chromosomal Hybrid Zones of the Common Shrew (Sorex araneus) Indicates Reduced Gene Flow

Sorex araneus, the Common shrew, is a species with more than 70 karyotypic races, many of which form parapatric hybrid zones, making it a model for studying chromosomal speciation. Hybrids between races have reduced fitness, but microsatellite markers have demonstrated considerable gene flow between them, calling into question whether the chromosomal barriers actually do contribute to genetic divergence. We studied phenotypic clines across two hybrid zones with especially complex heterozygotes. Hybrids between the Novosibirsk and Tomsk races produce chains of nine and three chromosomes at meiosis, and hybrids between the Moscow and Seliger races produce chains of eleven. Our goal was to determine whether phenotypes show evidence of reduced gene flow at hybrid zones. We used maximum likelihood to fit tanh cline models to geometric shape data and found that phenotypic clines in skulls and mandibles across these zones had similar centers and widths as chromosomal clines. The amount of phenotypic differentiation across the zones is greater than expected if it were dissipating due to unrestricted gene flow given the amount of time since contact, but it is less than expected to have accumulated from drift during allopatric separation in glacial refugia. Only if heritability is very low, N_e very high, and the time spent in allopatry very short, will the differences we observe be large enough to match the expectation of drift. Our results therefore suggest that phenotypic differentiation has been lost through gene flow since post-glacial secondary contact, but not as quickly as would be expected if there was free gene flow across the hybrid zones. The chromosomal tension zones are confirmed to be partial barriers that prevent differentiated races from becoming phenotypically homogenous.     

Low genetic differentiation among reed warbler Acrocephalus scirpaceus populations across Europe

Migratory birds generally have higher dispersal propensity than resident species and are thus expected to show less genetic differentiation. On the other hand, specific migration patterns may promote genetic structure, such as in situations where migratory divides impede random mixing of individuals. Here we investigated population genetic structure and gene flow patterns in a polytypic passerine, the reed warbler Acrocephalus scirpaceus which shows a migratory divide in central Europe. Using ten polymorphic microsatellite loci and extensive sampling we found low but significant overall genetic differentiation (F_ST=0.013, G’_ST=0.078, D=0.063). Hierarchical F‐statistics and barrier analyses showed low but significant genetic differentiation of Iberian populations, and also slight genetic differences across the migratory divide and between subspecies (A. s. scirpaceus and A. s. fuscus). Three individual‐based Bayesian methods, however, inferred a single genetic unit. Our study thus found low levels of genetic differentiation among reed warbler populations but this genetic differentiation was not pronounced enough to detect a clear population structure using the microsatellite data and no prior information on geographic location of the sampled individuals. This result indicates high levels of gene flow and suggests a possibly recent divergence of European populations after a rapid range expansion. Further studies are necessary to assess divergence times and to reveal the evolutionary history of the reed warbler populations.     

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.