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Evolution of X-Degenerate Y Chromosome Genes in Greater Apes: Conservation of Gene Content in Human and Gorilla, But Not Chimpanzee

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Abstract

Compared with the X chromosome, the mammalian Y chromosome is considerably diminished in size and has lost most of its ancestral genes during evolution. Interestingly, for the X-degenerate region on the Y chromosome, human has retained all 16 genes, while chimpanzee has lost 4 of the 16 genes since the divergence of the two species. To uncover the evolutionary forces governing ape Y chromosome degeneration, we determined the complete sequences of the coding exons and splice sites for 16 gorilla Y chromosome genes of the X-degenerate region. We discovered that all studied reading frames and splice sites were intact, and thus, this genomic region experienced no gene loss in the gorilla lineage. Higher nucleotide divergence was observed in the chimpanzee than the human lineage, particularly for genes with disruptive mutations, suggesting a lack of functional constraints for these genes in chimpanzee. Surprisingly, our results indicate that the human and gorilla orthologues of the genes disrupted in chimpanzee evolve under relaxed functional constraints and might not be essential. Taking mating patterns and effective population sizes of ape species into account, we conclude that genetic hitchhiking associated with positive selection due to sperm competition might explain the rapid decline in the Y chromosome gene number in chimpanzee. As we found no evidence of positive selection acting on the X-degenerate genes, such selection likely targets other genes on the chimpanzee Y chromosome.

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Acknowledgments

We are grateful to Chungoo Park, Saby Das, Allison N. Lau, Masafumi Nozawa, and Melissa Wilson for valuable suggestions. We also thank M. Paula Goetting-Minesky for experimental support at the early stages of this project. Meg Bakewell kindly provided the control files for PAML. One of the male gorilla DNA samples was provided by Robert Baker from the Natural Sciences Research Laboratory at Texas Tech University. This research was supported by startup funds from the Eberly College of Sciences at Pennsylvania State University to K.D.M.

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  1. Department of Biology and Center for Comparative Genomics and Bioinformatics, 305 Wartik Laboratory, The Pennsylvania State University, University Park, PA, 16802, USA

    Hiroki Goto, Lei Peng & Kateryna D. Makova

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  1. Hiroki Goto
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  2. Lei Peng
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  3. Kateryna D. Makova
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Correspondence to Kateryna D. Makova.

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Goto, H., Peng, L. & Makova, K.D. Evolution of X-Degenerate Y Chromosome Genes in Greater Apes: Conservation of Gene Content in Human and Gorilla, But Not Chimpanzee. J Mol Evol 68, 134–144 (2009). https://doi.org/10.1007/s00239-008-9189-y

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  • DOI: https://doi.org/10.1007/s00239-008-9189-y

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