The evolutionary maintenance of ancient recombining sex chromosomes in the ostrich

PLoS Genet. 2023 Jun 30;19(6):e1010801. doi: 10.1371/journal.pgen.1010801. eCollection 2023 Jun.

Abstract

Sex chromosomes have evolved repeatedly across the tree of life and often exhibit extreme size dimorphism due to genetic degeneration of the sex-limited chromosome (e.g. the W chromosome of some birds and Y chromosome of mammals). However, in some lineages, ancient sex-limited chromosomes have escaped degeneration. Here, we study the evolutionary maintenance of sex chromosomes in the ostrich (Struthio camelus), where the W remains 65% the size of the Z chromosome, despite being more than 100 million years old. Using genome-wide resequencing data, we show that the population scaled recombination rate of the pseudoautosomal region (PAR) is higher than similar sized autosomes and is correlated with pedigree-based recombination rate in the heterogametic females, but not homogametic males. Genetic variation within the sex-linked region (SLR) (π = 0.001) was significantly lower than in the PAR, consistent with recombination cessation. Conversely, genetic variation across the PAR (π = 0.0016) was similar to that of autosomes and dependent on local recombination rates, GC content and to a lesser extent, gene density. In particular, the region close to the SLR was as genetically diverse as autosomes, likely due to high recombination rates around the PAR boundary restricting genetic linkage with the SLR to only ~50Kb. The potential for alleles with antagonistic fitness effects in males and females to drive chromosome degeneration is therefore limited. While some regions of the PAR had divergent male-female allele frequencies, suggestive of sexually antagonistic alleles, coalescent simulations showed this was broadly consistent with neutral genetic processes. Our results indicate that the degeneration of the large and ancient sex chromosomes of the ostrich may have been slowed by high recombination in the female PAR, reducing the scope for the accumulation of sexually antagonistic variation to generate selection for recombination cessation.

MeSH terms

  • Animals
  • Biological Evolution
  • Evolution, Molecular
  • Female
  • Male
  • Mammals / genetics
  • Recombination, Genetic
  • Sex Chromosomes / genetics
  • Struthioniformes* / genetics

Grants and funding

The authors would like to acknowledge support from Science for Life Laboratory (Wallenberg Advanced Bioinformatic Infrastructure project 1502). The computations were enabled by resources in project SNIC2020-16-269 provided by the Swedish National Infrastructure for Computing (SNIC) at UPPMAX, partially funded by the Swedish Research Council through grant agreement no. 2018-05973. The resource population sampled was managed under the auspices of the Western Cape Department of Agriculture and partially funded by the Western Cape Agricultural Research Trust (Reference No: 0070/000 Volstruise). This research was funded by the Swedish Research Council (grant number 2017-03880 to CKC; 2016-00689 to BH), The Wenner-Gren and Olle Engkvist Foundations (postdoctoral fellowships to CO) and Knut and Alice Wallenberg Foundation (Wallenberg Academy fellowship numbers 2013.0129 & 2018.0138 to CKC) and Carl Tryggers Foundation (grant numbers 12:92 & 19:71 to CKC). PU is financially supported by the Knut and Alice Wallenberg Foundation as part of the National Bioinformatics Infrastructure Sweden at Science for Life Laboratory. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.