Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition

Abstract

In birds, as in mammals, one pair of chromosomes differs between the sexes. In birds, males are ZZ and females ZW. In mammals, males are XY and females XX. Like the mammalian XY pair, the avian ZW pair is believed to have evolved from autosomes, with most change occurring in the chromosomes found in only one sex – the W and Y chromosomes1–5. By contrast, the sex chromosomes found in both sexes – the Z and X chromosomes – are assumed to have diverged little from their autosomal progenitors2. Here we report findings that overturn this assumption for both the chicken Z and human X chromosomes. The chicken Z chromosome, which we sequenced essentially to completion, is less gene-dense than chicken autosomes but contains a massive tandem array containing hundreds of duplicated genes expressed in testes. A comprehensive comparison of the chicken Z chromosome to the finished sequence of the human X chromosome demonstrates that each evolved independently from different portions of the ancestral genome. Despite this independence, the chicken Z and human X chromosomes share features that distinguish them from autosomes: the acquisition and amplification of testis-expressed genes, as well as a low gene density resulting from an expansion of intergenic regions. These features were not present on the autosomes from which the Z and X chromosomes originated but were instead acquired during the evolution of the Z and X as sex chromosomes. We conclude that the avian Z and mammalian X chromosomes followed convergent evolutionary trajectories, despite their evolving with opposite (female vs. male) systems of heterogamety. More broadly, in birds and mammals, sex chromosome evolution involved not only gene loss in sex-specific chromosomes, but also marked expansion and gene acquisition in sex chromosomes common to males and females.

Rapid divergence and expansion of the X chromosome in papaya

“…The transposable element accumulation in the X-specific region is consistent with the greater quantity of such insertions in other sex chromosomes (X of mammals and Z of chickens) (14), and can be explained by its lower recombination frequency than that of autosomes; this difference arises because recombination occurs in only females, because of lack of recombination between the X-and Y-specific region in males (or HSY in hermaphrodites), in which the X spends one-third of its time. In Silene latifolia, whose sex chromosomes are extremely large and heteromorphic (the Y chromosome is 570 Mb and the X is 420 Mb), these changes have evolved over ∼10 million y (21).…”

“…In mammals, the gene order in the X chromosomes has been conserved across such distantly related species as human, cat, horse, cattle, and elephant, with the exception of mouse (22)(23)(24)(25)(26). In the human X and chicken Z, gene trafficking and sequence expansion have been detected, using comparisons with orthologous autosomal segments of other species (12)(13)(14). Given its recent origin, the differences in gene content between papaya and V. monoica are surprising.…”

“…Although other studies have compared the ancient human X and chicken Z chromosomes with their orthologous autosomal regions in distantly related species (12)(13)(14), our study is unique in being a detailed direct comparison between a newly evolved X-specific chromosomal region and its nonsex chromosomal homolog in a close relative. This comparison This article is a PNAS Direct Submission.…”

Rowley Review

“…For example, Nanda and colleagues recently reported that the Z is highly conserved across at least 14 species representing 11 families (Nanda et al 2008). The Z sex chromosome carries~1000 genes (Bellott et al 2010), most of which are ostensibly unrelated to sex. However, most recently, it has been show that the Chicken Z chromosome, like the mammalian X chromosome, is enriched for testis-expressed genes (Bellott et al 2010).…”

“…The Z sex chromosome carries~1000 genes (Bellott et al 2010), most of which are ostensibly unrelated to sex. However, most recently, it has been show that the Chicken Z chromosome, like the mammalian X chromosome, is enriched for testis-expressed genes (Bellott et al 2010). One of these is DMRT1 (Doublesex and Mab-3 Related Transcription factor, #1), which has a key role in testis development and may represent the master avian testis determinant (Smith et al 2009a) (described below).…”