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

Takeshi Kawakami,Reto Burri,Linnéa Smeds,Alexander Suh,Hans Ellegren,Alexander Nater,Carina F Mugal

doi:10.1111/mec.14197

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 200kb, 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.

Highlights

Using whole-genome polymorphism data of four populations of collared flycatchers and four populations of pied flycatchers, we found highly heterogeneous recombination landscapes in both species
The LD recombination map covered genomic regions that were not represented in the pedigree recombination map due to lack of genetic markers, regions towards the ends of chromosomes
The LD recombination map allowed for identification of recombination hotspots and direct analyses of the association between recombination events and genomic features

Summary

| INTRODUCTION

Meiotic recombination plays multiple important roles in DNA sequence evolution, genome integrity and the process of speciation. Studies in rodents and primates have shown that recombination is genetically regulated by localizing recombination-initiating DNA double-strand breaks (DSBs) to small regions of the genome, known as “recombination hotspots,” where recombination rate is 100- to 1,000fold higher than the genomic average (Baudat, Imai, & de Massy, 2013; Paigen & Petkov, 2010). It has been suggested that colocalization of recombination hotspots with transcription initiation contributes to an evolutionary stable recombination landscape (Axelsson et al, 2012; Lam & Keeney, 2015; Singhal et al, 2015) It is not clear whether transcriptional activity per se or underlying genomic features that are associated with promoter regions, such as CpG islands (CGIs), are responsible for this colocalization. As the heterogeneous landscape of differentiation in Ficedula flycatchers seems mainly to be the result of the extent of linked selection (Burri et al, 2015), species-specific estimates of recombination rate further make it possible to study the impact of changes in the recombination landscape on differentiation

| MATERIALS AND METHODS

| RESULTS

| DISCUSSION

Findings

DATA ACCESSIBILITY