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Fast Accumulation of Nonsynonymous Mutations on the Female-Specific W Chromosome in Birds

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Abstract

Following cessation of recombination during sex chromosome evolution, the nonrecombining sex chromosome is affected by a number of degenerative forces, possibly resulting in the fixation of deleterious mutations. This might take place because of weak selection against recessive or partly recessive deleterious mutations due to permanent heterozygosity of nonrecombining chromosomes. Furthermore, population genetic processes, such as selective sweeps, background selection, and Muller’s ratchet, result in a reduction in Ne, which increase the likelihood of fixation of deleterious mutations. Theory thus predicts that nonrecombining genes should show increased levels of nonsynonymous (dN) to synonymous substitutions (dS). We tested this in an avian system by estimating the ratio between dN and dS in six gametologous gene pairs located on the Z chromosome and the nonrecombining, female-specific W chromosome. In comparisons, we found a significantly higher dN/dS ratio for the W-linked than the Z-linked copy in three of the investigated genes. In a concatenated alignment of all six genes, the dN/dS ratio was six times higher for W-linked than Z-linked genes. By using human and mouse as outgroup in maximum likelihood analyses, W-linked genes were found to evolve differently compared with their Z-linked gametologues and outgroup sequences. This seems not to be a consequence of functional diversification because dN/dS ratios between gametologous gene copies were consistently low. We conclude that deleterious mutations are accumulating at a high rate on the avian W chromosome, probably as a result of the lack of recombination in this female-specific chromosome.

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Acknowledgments

We thank Dr. Lori-Jayne Lawson Handley for the turkey UBAP2W and chicken UBAP2Z and UBAP2W sequences, and two anonymous reviewers and Deborah Charlesworth for useful comments. Financial support was obtained from the Swedish Research Council. H.E. is a Royal Academy of Sciences Research Fellow supported by a grant from the Knut and Alice Wallenberg Foundation.

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  1. Sofia Berlin

    Present address: Department of Genetics and Genomics, Roslin Institute (Edinburgh), Roslin, Midlothian, EH25 9PS, UK

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  1. Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Norbyvagen 18 D, Uppsala, 752 36, Sweden

    Sofia Berlin & Hans Ellegren

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  1. Sofia Berlin
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  2. Hans Ellegren
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Correspondence to Sofia Berlin.

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[Reviewing Editor: Dr. Deborah Charlesworth]

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Berlin, S., Ellegren, H. Fast Accumulation of Nonsynonymous Mutations on the Female-Specific W Chromosome in Birds. J Mol Evol 62, 66–72 (2006). https://doi.org/10.1007/s00239-005-0067-6

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