Abstract
Closely related species may show similar levels of genetic diversity in homologous regions of the genome owing to shared ancestral variation still segregating in the extant species. However, after completion of lineage sorting, such covariation is not necessarily expected. On the other hand, if the processes that govern genetic diversity are conserved, diversity may potentially covary even among distantly related species. We mapped regions of conserved synteny between the genomes of two divergent bird species—collared flycatcher and hooded crow—and identified more than 600 Mb of homologous regions (66% of the genome). From analyses of whole-genome resequencing data in large population samples of both species we found nucleotide diversity in 200 kb windows to be well correlated (Spearman's ρ = 0.407). The correlation remained highly similar after excluding coding sequences. To explain this covariation, we suggest that a stable avian karyotype and a conserved landscape of recombination rate variation render the diversity-reducing effects of linked selection similar in divergent bird lineages. Principal component regression analysis of several potential explanatory variables driving heterogeneity in flycatcher diversity levels revealed the strongest effects from recombination rate variation and density of coding sequence targets for selection, consistent with linked selection. It is also possible that a stable karyotype is associated with a conserved genomic mutation environment contributing to covariation in diversity levels between lineages. Our observations imply that genetic diversity is to some extent predictable.
Highlights
We suggest that a stable avian karyotype and a conserved landscape of recombination rate variation render the diversity-reducing effects of linked selection similar in divergent bird lineages
Understanding the evolutionary mechanisms governing the extent of genetic diversity within and between species is important to evolutionary biology in several respects [1]
The influence of linked selection has been shown to be affected by several factors, including recombination rate [7,50] and density of targets of selection [6,51]
Summary
Understanding the evolutionary mechanisms governing the extent of genetic diversity (e.g. degree of polymorphism, heterozygosity or nucleotide diversity) within and between species is important to evolutionary biology in several respects [1]. If karyotypic stability is associated with conservation of evolutionary processes governing genetic diversity (see further below), we hypothesized that covariation in regional levels of genetic diversity might be detectable in diverging lineages of birds We test this hypothesis using whole-genome resequencing data from population samples of two distantly related passerine species, the collared flycatcher (Ficedula albicollis) and the hooded crow (Corvus (corone) cornix), both species with a karyotype of 2n 1⁄4 80 [19]; for flycatcher karyotype information is from F. parva and F. mugimaki [20]. To investigate the effect of coding sequence density 3 on the extent of linked selection in the flycatcher genome, we regressed nucleotide diversity against recombination rate within gene-rich and gene-poor regions using respectively the highest and the lowest 10% of windows from the distribution of coding sequence density. Because coding sequence density is correlated with GC content, we further regressed nucleotide diversity against recombination rate within GC-rich and GC-poor regions using respectively the highest and the lowest 10% of windows from the distribution of GC content
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