The Y Chromosomes of the Great Apes

Overview

Journal Hum Genet

Specialty Genetics

Date 2017 Mar 8

PMID 28265767

Citations 14

Authors

Pille Hallast

Mark A Jobling

Affiliations

Soon will be listed here.

Abstract

The great apes (orangutans, gorillas, chimpanzees, bonobos and humans) descended from a common ancestor around 13 million years ago, and since then their sex chromosomes have followed very different evolutionary paths. While great-ape X chromosomes are highly conserved, their Y chromosomes, reflecting the general lability and degeneration of this male-specific part of the genome since its early mammalian origin, have evolved rapidly both between and within species. Understanding great-ape Y chromosome structure, gene content and diversity would provide a valuable evolutionary context for the human Y, and would also illuminate sex-biased behaviours, and the effects of the evolutionary pressures exerted by different mating strategies on this male-specific part of the genome. High-quality Y-chromosome sequences are available for human and chimpanzee (and low-quality for gorilla). The chromosomes differ in size, sequence organisation and content, and while retaining a relatively stable set of ancestral single-copy genes, show considerable variation in content and copy number of ampliconic multi-copy genes. Studies of Y-chromosome diversity in other great apes are relatively undeveloped compared to those in humans, but have nevertheless provided insights into speciation, dispersal, and mating patterns. Future studies, including data from larger sample sizes of wild-born and geographically well-defined individuals, and full Y-chromosome sequences from bonobos, gorillas and orangutans, promise to further our understanding of population histories, male-biased behaviours, mutation processes, and the functions of Y-chromosomal genes.

Citing Articles

Assessing the recovery of Y chromosome microsatellites with population genomic data using Papio and Theropithecus genomes.

Mutti G, Oteo-Garcia G, Caldon M, Ferreira da Silva M, Minhos T, Cowlishaw G Sci Rep. 2023; 13(1):13839.

PMID: 37620368 PMC: 10449864. DOI: 10.1038/s41598-023-40931-x.

Eighty million years of rapid evolution of the primate Y chromosome.

Zhou Y, Zhan X, Jin J, Zhou L, Bergman J, Li X Nat Ecol Evol. 2023; 7(7):1114-1130.

PMID: 37268856 DOI: 10.1038/s41559-022-01974-x.

Editorial: Role of Y Chromosome in Molecular Anthropology, Forensics, and Genetic Genealogy.

Hadi S, Yao J, Adnan A Front Genet. 2022; 13:863455.

PMID: 35754810 PMC: 9218708. DOI: 10.3389/fgene.2022.863455.

Improved Models of Coalescence Ages of Y-DNA Haplogroups.

McDonald I Genes (Basel). 2021; 12(6).

PMID: 34200049 PMC: 8228294. DOI: 10.3390/genes12060862.

Molecular characterization of the Yp11.2 region deletion in the Chinese Han population.

Pang Q, Lin Q, Wang D, Sun Z, Wang J Int J Legal Med. 2021; 135(4):1351-1358.

PMID: 33903958 PMC: 8205872. DOI: 10.1007/s00414-021-02596-x.

References

Soh Y, Alfoldi J, Pyntikova T, Brown L, Graves T, Minx P . Sequencing the mouse Y chromosome reveals convergent gene acquisition and amplification on both sex chromosomes. Cell. 2014; 159(4):800-13. PMC: 4260969. DOI: 10.1016/j.cell.2014.09.052. View

Skaletsky H, Kuroda-Kawaguchi T, Minx P, Cordum H, Hillier L, Brown L . The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature. 2003; 423(6942):825-37. DOI: 10.1038/nature01722. View

Arora N, Nater A, van Schaik C, Willems E, van Noordwijk M, Goossens B . Effects of Pleistocene glaciations and rivers on the population structure of Bornean orangutans (Pongo pygmaeus). Proc Natl Acad Sci U S A. 2010; 107(50):21376-81. PMC: 3003094. DOI: 10.1073/pnas.1010169107. View

Toder R, Zeitler S, Goodfellow P, Schempp W . Comparative mapping of SRY in the great apes. Chromosome Res. 1993; 1(2):117-20. DOI: 10.1007/BF00710034. View

Bosch E, Hurles M, Navarro A, Jobling M . Dynamics of a human interparalog gene conversion hotspot. Genome Res. 2004; 14(5):835-44. PMC: 479110. DOI: 10.1101/gr.2177404. View

Foresta C, Moro E, Rossi A, Rossato M, Garolla A, Ferlin A . Role of the AZFa candidate genes in male infertility. J Endocrinol Invest. 2000; 23(10):646-51. DOI: 10.1007/BF03343788. View

Mendez F, Poznik G, Castellano S, Bustamante C . The Divergence of Neandertal and Modern Human Y Chromosomes. Am J Hum Genet. 2016; 98(4):728-34. PMC: 4833433. DOI: 10.1016/j.ajhg.2016.02.023. View

Eriksson J, Siedel H, Lukas D, Kayser M, Erler A, Hashimoto C . Y-chromosome analysis confirms highly sex-biased dispersal and suggests a low male effective population size in bonobos (Pan paniscus). Mol Ecol. 2006; 15(4):939-49. DOI: 10.1111/j.1365-294X.2006.02845.x. View

Hughes J, Skaletsky H, Brown L, Pyntikova T, Graves T, Fulton R . Strict evolutionary conservation followed rapid gene loss on human and rhesus Y chromosomes. Nature. 2012; 483(7387):82-6. PMC: 3292678. DOI: 10.1038/nature10843. View

10.

Churchill J, Schmedes S, King J, Budowle B . Evaluation of the Illumina(®) Beta Version ForenSeq™ DNA Signature Prep Kit for use in genetic profiling. Forensic Sci Int Genet. 2015; 20:20-29. DOI: 10.1016/j.fsigen.2015.09.009. View

11.

Knebel S, Pasantes J, Thi D, SCHALLER F, Schempp W . Heterogeneity of pericentric inversions of the human y chromosome. Cytogenet Genome Res. 2011; 132(4):219-26. DOI: 10.1159/000322080. View

12.

Rozen S, Marszalek J, Alagappan R, Skaletsky H, Page D . Remarkably little variation in proteins encoded by the Y chromosome's single-copy genes, implying effective purifying selection. Am J Hum Genet. 2009; 85(6):923-8. PMC: 2790577. DOI: 10.1016/j.ajhg.2009.11.011. View

13.

Perry G, Tito R, Verrelli B . The evolutionary history of human and chimpanzee Y-chromosome gene loss. Mol Biol Evol. 2007; 24(3):853-9. DOI: 10.1093/molbev/msm002. View

14.

Li G, Davis B, Raudsepp T, Pearks Wilkerson A, Mason V, Ferguson-Smith M . Comparative analysis of mammalian Y chromosomes illuminates ancestral structure and lineage-specific evolution. Genome Res. 2013; 23(9):1486-95. PMC: 3759724. DOI: 10.1101/gr.154286.112. View

15.

Paria N, Raudsepp T, Pearks Wilkerson A, OBrien P, Ferguson-Smith M, Love C . A gene catalogue of the euchromatic male-specific region of the horse Y chromosome: comparison with human and other mammals. PLoS One. 2011; 6(7):e21374. PMC: 3143126. DOI: 10.1371/journal.pone.0021374. View

16.

Willems T, Gymrek M, Poznik G, Tyler-Smith C, Erlich Y . Population-Scale Sequencing Data Enable Precise Estimates of Y-STR Mutation Rates. Am J Hum Genet. 2016; 98(5):919-933. PMC: 4863667. DOI: 10.1016/j.ajhg.2016.04.001. View

17.

Repping S, van Daalen S, Brown L, Korver C, Lange J, Marszalek J . High mutation rates have driven extensive structural polymorphism among human Y chromosomes. Nat Genet. 2006; 38(4):463-7. DOI: 10.1038/ng1754. View

18.

Brown G, Furlong R, Sargent C, Erickson R, Longepied G, Mitchell M . Characterisation of the coding sequence and fine mapping of the human DFFRY gene and comparative expression analysis and mapping to the Sxrb interval of the mouse Y chromosome of the Dffry gene. Hum Mol Genet. 1998; 7(1):97-107. DOI: 10.1093/hmg/7.1.97. View

19.

Balaresque P, King T, Parkin E, Heyer E, Carvalho-Silva D, Kraaijenbrink T . Gene conversion violates the stepwise mutation model for microsatellites in y-chromosomal palindromic repeats. Hum Mutat. 2014; 35(5):609-17. PMC: 4233959. DOI: 10.1002/humu.22542. View

20.

Cooke H, Brown W, Rappold G . Hypervariable telomeric sequences from the human sex chromosomes are pseudoautosomal. Nature. 1985; 317(6039):687-92. DOI: 10.1038/317687a0. View