Genomics of expanded avian sex chromosomes shows that certain chromosomes are predisposed towards sex-linkage in vertebrates

Abstract

Sex chromosomes have evolved from the same autosomes multiple times across vertebrates, suggesting that certain genomic regions are predisposed towards sex-linkage. However, to test this hypothesis detailed studies of independently originated sex-linked regions and their gene content are needed. Here we address this problem through comparative genomics of birds where multiple chromosomes appear to have formed neo-sex chromosomes: larks (Alaudidae; Sylvioidea). We detected the largest known avian sex chromosome (195.3 Mbp) and show that it originates from fusions between (parts of) four avian chromosomes (Z, 3, 4A and 5). We found evidence of five evolutionary strata where recombination has been suppressed at different time points, and that these time points correlate with the level of Z–W gametolog differentiation. We show that there is extensive homology to sex chromosomes in other vertebrate lineages: three of the fused chromosomes (Z, 4A, 5) have independently evolved into sex chromosomes in fish (Z), turtles (Z, 5), lizards (Z, 4A) and mammals (Z, 4A). Moreover, we found that the fourth chromosome, chromosome 3, was significantly enriched for genes with predicted sex-specific functions. These results support a key role of chromosome content in the evolution of sex chromosomes in vertebrates.

Neo-sex chromosomes, genetic diversity and demographic history in the Critically Endangered Raso lark

“…Our results indicate that two other large chromosomes, 3 and 5, have also become sex-linked in the genera Alauda and Galerida. Another recent study [38] supports these observations and further indicates that at least chromosome 3 is also sex-linked in two additional outgroup species (horned lark, bearded reedling).…”

“…Female Oriental skylark and crested lark also show elevated densities of heterozygous sites, but over smaller portions of chromosomes 3 and 5 (Figure 2A). Using our results in combination with those from a recent study of two additional outgroup species, the bearded reedling Panurus biarmicus and the horned lark Eremophila alpestris [38], we are able to partially reconstruct the stepwise progression of recombination suppression ( Figure 2B). We infer that the initial suppression occurred in two narrow 'strata' on chromosomes 3 and 4a-1 [38].…”

“…Despite the deep age of the neo-sex chromosomes, our results indicate fairly strong homology between the neo-W and neo-Z in the regions of recombination suppression, with around 99% similarity. This value may be somewhat underestimated, as the most divergent parts would be excluded due to poor read mapping [38]. Nevertheless, even a divergence of 2% would translate to ~2.2 million generations to coalescence -much less than the age of the neo-sex chromosomes.…”

“…The evolutionary causes and consequences of the enlarged neo-sex chromsoomes requires further study. It is hypothesised that sexually antagonistic selection might favour recombination suppression between sex chromosomes [38,46]. Whether this is true in the Alauda larks is currently unclear.…”

“…One scaffold appears to bridge chromosomes 3 and 5, but this too may be a misassembly, as it maps to the centre of the two regions of suppressed recombination ( Figure S1). Figure S2) as well as reference [38] (the latter are shown in grey and indicated with an asterisk). Note that chromosomes are not shown as fused as we do not have evidence for or against physical linkage in this study.…”