Extreme variation in recombination rate and genetic diversity along the Sylvioidea neo-sex chromosome

Recombination strongly impacts sequence evolution by affecting the extent of linkage and the efficiency of selection. Here, we study recombination over the Z chromosome in great reed warblers (Acrocephalus arundinaceus) using pedigree-based linkage mapping. This species has extended Z and W chromosomes (neo-sex chromosomes) formed by a fusion between a part of chromosome 4A and the ancestral sex chromosomes, which provides a unique opportunity to assess recombination and sequence evolution in sex-linked regions of different ages. We assembled an 87.54 Mbp and 90.19 cM large Z with a small pseudoautosomal region (0.89 Mbp) at one end and the fused Chr4A-part at the other end of the chromosome. A prominent feature in our data was an extreme variation in male recombination rate along Z with high values at both chromosome ends, but an apparent lack of recombination over a substantial central section, covering 78% of the chromosome. The nonrecombining region showed a drastic loss of genetic diversity and accumulation of repeats compared to the recombining parts. Thus, our data emphasize a key role of recombination in affecting local levels of polymorphism. Nonetheless, the evolutionary rate of genes (dN/dS) did not differ between high and low recombining regions, suggesting that the efficiency of selection on protein-coding sequences can be maintained also at very low levels of recombination. Finally, the Chr4A-derived part showed a similar recombination rate as the part of the ancestral Z that did recombine, but its sequence characteristics reflected both its previous autosomal, and current Z-linked, recombination patterns.

Automated summary

Recombination plays a significant role in sequence evolution by affecting linkage and selection efficiency. This study investigates recombination in the Z chromosome of great reed warblers using pedigree-based linkage mapping. A notable finding is the extreme variation in male recombination rate along the Z chromosome, with high values at the chromosome ends but a lack of recombination in the central section. The nonrecombining region shows a significant loss of genetic diversity and an accumulation of repeats compared to the recombining parts. Despite this, the evolutionary rate of protein-coding genes does not differ between high and low recombining regions, suggesting that selection efficiency can be maintained even at low recombination levels. Additionally, the recombination rate in the Chr4A-derived part of the Z chromosome is similar to the recombining region, but its sequence characteristics reflect both its previous autosomal and current Z-linked recombination patterns.