The evolutionary maintenance of ancient recombining sex chromosomes in the ostrich

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.