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Letter

Fast-X on the Z: Rapid evolution of sex-linked genes in birds

Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18 D, SE 752 36 Uppsala, Sweden

Theoretical work predicts natural selection to be more efficient in the fixation of beneficial mutations in X-linked genes than in autosomal genes. This "fast-X effect" should be evident by an increased ratio of nonsynonymous to synonymous substitutions (d_N/d_S) for sex-linked genes; however, recent studies have produced mixed support for this expectation. To make an independent test of the idea of fast-X evolution, we focused on birds, which have female heterogamety (males ZZ, females ZW), where analogous arguments would predict a fast-Z effect. We aligned 2.8 Mb of orthologous protein-coding sequence of zebra finch and chicken from 172 Z-linked and 4848 autosomal genes. Zebra finch data were in the form of EST sequences from brain cDNA libraries, while chicken genes were from the draft genome sequence. The d_N/d_S ratio was significantly higher for Z-linked (0.110) than for all autosomal genes (0.085; P = 0.002), as well as for genes linked to similarly sized autosomes 1–10 (0.0948; P = 0.04). This pattern of fast-Z was evident even after we accounted for the nonrandom distribution of male-biased genes. We also examined the nature of standing variation in the chicken protein-coding regions. The ratio of nonsynonymous to synonymous polymorphism (p_N/p_S) did not differ significantly between genes on the Z chromosome (0.104) and on the autosomes (0.0908). In conjunction, these results suggest that evolution proceeds more quickly on the Z chromosome, where hemizygous exposure of beneficial nondominant mutations increases the rate of fixation.

E-mail Hans.Ellegren{at}ebc.uu.se; fax 46-18-4716310.

[Supplemental material is available online at www.genome.org and http://www.egs.uu.se/evbiol/Research/Data/fast-Z/.]

Article published online before print. Article and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.6031907

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