Correlated patterns of genetic diversity and differentiation across an avian family

Abstract

Comparative studies of genomic differentiation among independent lineages can provide insights into aspects of the speciation process, such as the relative importance of selection and drift in shaping genomic landscapes, the role of genomic regions of high differentiation, and the prevalence of convergent molecular evolution. We investigated patterns of genetic diversity and divergence in stonechats (genus Saxicola), a widely distributed avian species complex with phenotypic variation in plumage, morphology, and migratory behavior, to ask whether similar genomic regions are important in the evolution of independent, but closely related, taxa. We used whole-genome pooled sequencing of 262 individuals from 5 taxa and found that patterns of genetic diversity and divergence are highly similar among different stonechat taxa. We then asked if these patterns remain correlated at deeper evolutionary scales and found that homologous genomic regions have become differentiated in stonechats and the closely related Ficedula flycatchers. Such correlation across a range of evolutionary divergence and among phylogenetically independent comparisons suggests that similar processes may be driving the differentiation of these independently evolving lineages, which in turn may be the result of intrinsic properties of particular genomic regions (e.g., areas of low recombination). Consequently, studies employing genome scans to search for areas important in reproductive isolation should account for corresponding regions of differentiation, as these regions may not necessarily represent speciation islands or facilitate local adaptation.All rights reserved. No reuse allowed without permission.was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.

Comparative analysis examining patterns of genomic differentiation across multiple episodes of population divergence in birds

“…As speciation proceeds, drift and background selection will begin to affect differentiation as well and, combined with positive selection and genetic hitchhiking, these processes could result in the landscape of differentiation reflecting genomic features more directly. This scenario was described by Burri (2017) and is in line with recent work showing that linked selection (positive or purifying in nature) may generate repeated patterns of differentiation at longer time scales (Phung et al 2016;Dutoit et al 2017;Van Doren et al 2017;Vijay et al 2017). Note that the beginning stages of speciation may be less repeatable even without different selective pressures.…”

“…For example, if genomic variables are conserved across pairs, constraints imposed by processes like linked selection in these regions should generate correlated or repeated patterns of genomic differentiation. Comparative analyses are beginning to accumulate but are often limited to a closely related group of species or populations, precluding an evaluation of temporal effects and introducing statistical nonindependence if a limited number of pairs are included (e.g., sticklebacks, Jones et al 2012;sunflowers, Renaut et al 2014;guppies, Fraser et al 2015; songbirds, Irwin et al 2016;Van Doren et al 2017;copepods, Pereira et al 2016). In addition, working at broader taxonomic scales may eliminate the role shared selective regimes play in generating repeatable patterns of differentiation, isolating the effects of genomic constraints.…”

Interpreting differentiation landscapes in the light of long-term linked selection

“…In line with this, linked selection appears to reduce genetic diversity below neutral expectations across a wider range of recombination rates in taxa with high N e (Corbett-Detig et al 2015). In taxa with very low N e , effects of linked selection may be negligible altogether, and correlations between genomic landscapes be absent, or even inversed (Van Doren et al 2017;Burri 2017b) In conclusion, the alignment of multiple genomic features in space (along the genome) and over time in combination with population-level processes are expected to determine the conditions under which correlated differentiation landscapes may evolve and the timescales over which correlations persist (see section Outstanding Questions).…”

“…This cumulative impact of linked selection is reflected in a correlation of extant diversity (π) with ancestral diversity (reflected in sequence divergence, d XY , among closely related species, Box 1) (Nachman and Payseur 2012;Burri et al 2015). The reduction of ancestral diversity through long-term linked selection may be strong enough to even impact sequence divergence between distantly related species, such as human and mouse, and bird species as divergent as 50 my (Phung et al 2016;Dutoit et al 2017;Van Doren et al 2017;Vijay et al 2017). Second, linked selection within extant lineages maintains the relative levels of diversity among genomic regions.…”

“…See Bhatia et al (2013) for recommendations regarding F ST estimation. It is worth noting that the π/d XY ratio that has recently found application to interpret differentiation patterns (Irwin et al 2016;Van Doren et al 2017) is directly related to F ST , as π total is strongly related to d XY .…”