Whole‐genome patterns of linkage disequilibrium across flycatcher populations clarify the causes and consequences of fine‐scale recombination rate variation in birds

Abstract

Recombination rate is heterogeneous across the genome of various species and so are genetic diversity and differentiation as a consequence of linked selection. However, we still lack a clear picture of the underlying mechanisms for regulating recombination.Here we estimated fine-scale population recombination rate based on the patterns of linkage disequilibrium across the genomes of multiple populations of two closely related flycatcher species (Ficedula albicollis and F. hypoleuca). This revealed an overall conservation of the recombination landscape between these species at the scale of 200 kb, but we also identified differences in the local rate of recombination despite their recent divergence (<1 million years). Genetic diversity and differentiation were associated with recombination rate in a lineage-specific manner, indicating differences in the extent of linked selection between species. We detected 400-3,085 recombination hotspots per population. Location of hotspots was conserved between species, but the intensity of hotspot activity varied between species. Recombination hotspots were primarily associated with CpG islands (CGIs), regardless of whether CGIs were at promoter regions or away from genes. Recombination hotspots were also associated with specific transposable elements (TEs), but this association appears indirect due to shared preferences of the transposition machinery and the recombination machinery for accessible open chromatin regions. Our results suggest that CGIs are a major determinant of the localization of recombination hotspots, and we propose that both the distribution of TEs and fine-scale variation in recombination rate may be associated with the evolution of the epigenetic landscape.

Genomewide patterns of variation in genetic diversity are shared among populations, species and higher‐order taxa

“…In addition to putative centromeric regions, we found evidence for an association of subtelomeric regions with variation in genetic diversity. Yet, subtelomeric regions are not necessarily characterized by low recombination in birds (Backström et al., ; Kawakami et al., ) which is consistent with an explanation invoking recurrent positive selection rather than background selection reducing local N e . However, in other systems, it has been shown that subtelomeric regions experience low recombination rates, similar to centromeres (Roesti et al., ).…”

“…Unlike mammals, a relatively stable karyotype in birds (Ellegren, ) argues for global conservation of recombination landscape; however, the extent of such conservation is not clear, in particular at the level of individual chromosomes. Comparative analysis among chicken, zebra finch and collared flycatcher suggests that intrachromosomal rearrangements occurred at non‐negligible rates and that lack of recombination around (macro‐)chromosome centres appears to be specific to zebra finch (Kawakami et al., ). It is thus not straightforward to predict the degree of covariation in recombination rates at kb‐resolution considered here.…”

“…However, centromeric positions in crow, flycatcher and Darwin's finch were approximated relative to centromeres in zebra finch. Zebra finch is known for its many lineage‐specific inversions (Kawakami et al., ; Weissensteiner et al., ) which may have reduced the association of genetic differentiation with the predicted centromere locations in the target species. Recent work in crows, however, corroborates an impact of independently predicted, putative (peri)centromeric regions on population recombination, genetic diversity and differentiation (Weissensteiner et al., ).…”

“…species complex (Vijay et al., ). Functionally annotated genome assemblies with high sequence contiguity are available for one representative each of Ficedula flycatchers ( F. albicollis, genome size: 1.13, scaffold/contig N50 = 6.5 Mb/410 kb, National Center for Biotechnology Information (NCBI) Accession No: ; (Ellegren et al., ); new chromosome build (Kawakami et al., )) and for one hooded crow specimen ( Corvus (corone) cornix , genome size: 1.04 Gb, scaffold/contig N50 = 16.4 Mb/94 kb, NCBI Accession no: ; (Poelstra et al., ; Poelstra, Vijay, Hoeppner, & Wolf, )). The assembly of the medium ground finch G. fortis is of comparable size (1.07 Gb) and the least contiguous among the three both at the scaffold and contig level (scaffold/contig N50 = 5.3 Mb/30 kb, NCBI Accession no: ; (Rands et al., )).…”

“…It is conservative in that overlap is only expected if centromere position is conserved between zebra finch and the taxon under consideration. Evolutionary lability of these features, partly expected due to known lineage‐specific inversions in zebra finch (Hooper & Price, ; Kawakami et al., ; Romanov et al., ), would reduce any real correlation (type II error), but is unlikely to introduce spurious correlations (type I error). Twenty‐two centromere and 20 subtelomere positions were obtained for zebra finch from Knief and Forstmeier ().…”