Correlated patterns of genetic diversity and differentiation across an avian family

Abstract

Comparative studies of closely related taxa can provide insights into the evolutionary forces that shape genome evolution and the prevalence of convergent molecular evolution. We investigated patterns of genetic diversity and differentiation in stonechats (genus Saxicola), a widely distributed avian species complex with phenotypic variation in plumage, morphology and migratory behaviour, to ask whether similar genomic regions have become differentiated in independent, but closely related, taxa. We used whole-genome pooled sequencing of 262 individuals from five taxa and found that levels of genetic diversity and divergence are strongly correlated among different stonechat taxa. We then asked whether 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 for reproductive isolation or adaptation should account for corresponding regions of differentiation, as these regions may not necessarily represent speciation islands or evidence of local adaptation.

Evolutionary dynamics of hybridization and introgression following the recent colonization of Glossy Ibis (Aves: Plegadis falcinellus) into the New World

“…However, d XY in all comparisons was positively correlated with genetic diversity (based on observed heterozygosity) at a given locus, similar to results from recent studies in Muscicapid flycatchers (Burri et al, ; van Doren et al, ; Vijay et al, ). Recent analyses of whole genome data sets from birds suggest the concordance between divergence and diversity may be driven by linked selection combined with a conserved recombination landscape across the avian genome, rather than parallel selection on the same loci across lineages (Burri et al, ; van Doren et al, ; Dutoit et al, ; Singhal et al, ). Given the association between divergence and genetic diversity we observed, a similar situation is likely the cause of shared regions of divergence in pairwise comparisons across the three Plegadis species.…”

Lack of gene flow: Narrow and dispersed differentiation islands in a triplet of Leptidea butterfly species

“…Third, the genetic differentiation outliers were often specific to each respective species and population comparison and not shared across all comparisons. This is different from the situation in many other systems, where genome scan approaches have identified more or less the same set of outlier regions even when independent species comparisons have been made across very divergent families (Van Doren et al, ; Vijay et al, ). Taken together, the divergence landscapes in Leptidea seem to be shaped by lineage‐specific selection and genetic drift, generating narrow and dispersed differentiation peaks.…”

“…This is consistent with the hypothesis that incompatibility genes should be sheltered from interspecific gene flow and therefore stand out as more differentiated than surrounding regions (e.g., Berner & Roesti, ; Feder, Flaxman, Egan, & Nosil, ; Nosil, Funk, & Ortiz‐Barrientos, ; Turner et al, ). However, a heterogeneous landscape of genomic differentiation is expected even without gene flow, predominantly as an effect of regional variation in recombination rate (Buerkle, ; Burri, ; Cruickshank & Hahn, ; Ellegren & Wolf, ; Jiggins & Martin, ; Lohse, ; Nachman & Payseur, ; Ravinet et al, ; Van Doren et al, ). Although the exact pinpointing of genes involved in reproductive isolation likely is out of reach in most natural study systems, a genome scan approach in recently diverged species can inform on the main molecular mechanisms and evolutionary forces underlying global patterns of genomic divergence during initial stages of the speciation process (Jiggins & Martin, ; Seehausen et al, ; Wolf & Ellegren, ; Zimmer et al, ).…”

Candidate genes for migration do not distinguish migratory and non-migratory birds

“…We further included genome sequences of five additional migratory species here: Siberian stonechat Saxicola maurus (Van Doren et al 2017), Swainson’s thrush Catharus ustulatus (Delmore et al 2015a), European blackcap Sylvia atricapilla (Delmore et al, in preparation), Willow warbler Phylloscopus trochilus (Lundberg et al 2017, accepted), and Greenish warbler Phylloscopus trochiloides (Irwin et al 2016). …”