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

Daniel W. Bellott, Helen Skaletsky, Tatyana Pyntikova, Elaine R. Mardis, Tina Graves, Colin Kremitzki, Laura G. Brown, Steve Rozen, Wesley C. Warren, Richard K. Wilson, David C. Page

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123 Scopus citations

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 sexĝ€"the W and Y chromosomes. By contrast, the sex chromosomes found in both sexesĝ€"the Z and X chromosomesĝ€" are assumed to have diverged little from their autosomal progenitors. Here we report findings that challenge this assumption for both the chicken Z chromosome and the human X chromosome. 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 with 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, and 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 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 versus 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.

Original languageEnglish
Pages (from-to)612-616
Number of pages5
JournalNature
Volume466
Issue number7306
DOIs
StatePublished - Jul 29 2010

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    Bellott, D. W., Skaletsky, H., Pyntikova, T., Mardis, E. R., Graves, T., Kremitzki, C., Brown, L. G., Rozen, S., Warren, W. C., Wilson, R. K., & Page, D. C. (2010). Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition. Nature, 466(7306), 612-616. https://doi.org/10.1038/nature09172