Evolution of X-Degenerate Y Chromosome Genes in Greater Apes: Conservation of Gene Content in Human and Gorilla, But Not Chimpanzee
- 445 Downloads
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.
KeywordsY chromosome Genetic degeneration Sperm competition Sex chromosomes Ape evolution Gene content
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.
- Dixson AF (1998) Primate sexuality: comparative studies of the prosimians, monkeys, apes, and human beings. Oxford University Press, New YorkGoogle Scholar
- Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge, MAGoogle Scholar
- Hasegawa T, Hiraiwai-Hasegawa M (1990) Sperm competition and mating behavior. In: Nishida T (ed) The chimpanzees of the Mahale mountains: sexual and life history strategies. University of Tokyo Press, Tokyo, pp 115–132Google Scholar
- Hinrichs AS, Karolchik D, Baertsch R, Barber GP, Bejerano G, Clawson H, Diekhans M, Furey TS, Harte RA, Hsu F, Hillman-Jackson J, Kuhn RM, Pedersen JS, Pohl A, Raney BJ, Rosenbloom KR, Siepel A, Smith KE, Sugnet CW, Sultan-Qurraie A, Thomas DJ, Trumbower H, Weber RJ, Weirauch M, Zweig AS, Haussler D, Kent WJ (2006) The UCSC Genome Browser Database: update 2006. Nucleic Acids Res 34:D590–D598PubMedCrossRefGoogle Scholar
- Kuroki Y, Toyoda A, Noguchi H, Taylor TD, Itoh T, Kim DS, Kim DW, Choi SH, Kim IC, Choi HH, Kim YS, Satta Y, Saitou N, Yamada T, Morishita S, Hattori M, Sakaki Y, Park HS, Fujiyama A (2006) Comparative analysis of chimpanzee and human Y chromosomes unveils complex evolutionary pathway. Nat Genet 38:158–167PubMedCrossRefGoogle Scholar
- Ohno S (1967) Monographs on endocrinology. Sex chromosomes and sex-linked genes, 1st edn. Springer, HeidelbergGoogle Scholar
- Shi J, Xi H, Wang Y, Zhang C, Jiang Z, Zhang K, Shen Y, Jin L, Zhang K, Yuan W, Wang Y, Lin J, Hua Q, Wang F, Xu S, Ren S, Xu S, Zhao G, Chen Z, Jin L, Huang W (2003) Divergence of the genes on human chromosome 21 between human and other hominoids and variation of substitution rates among transcription units. Proc Natl Acad Sci USA 100:8331–8336PubMedCrossRefGoogle Scholar
- Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, Repping S, Pyntikova T, Ali J, Bieri T, Chinwalla A, Delehaunty A, Delehaunty K, Du H, Fewell G, Fulton L, Fulton R, Graves T, Hou SF, Latrielle P, Leonard S, Mardis E, Maupin R, McPherson J, Miner T, Nash W, Nguyen C, Ozersky P, Pepin K, Rock S, Rohlfing T, Scott K, Schultz B, Strong C, Tin-Wollam A, Yang SP, Waterston RH, Wilson RK, Rozen S, Page DC (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:825–837PubMedCrossRefGoogle Scholar
- Veyrunes F, Waters PD, Miethke P, Rens W, McMillan D, Alsop AE, Grützner F, Deakin JE, Whittington CM, Schatzkamer K, Kremitzki CL, Graves T, Ferguson-Smith MA, Warren W, Marshall Graves JA (2008) Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Res 18:965–973PubMedCrossRefGoogle Scholar