The degenerate Y chromosome – can conversion save it?
Jennifer A. Marshall GravesResearch School of Biological Sciences, The Australian National University, Canberra, ACT, Australia. email: jenny.graves@anu.edu.au
Reproduction, Fertility and Development 16(5) 527-534 https://doi.org/10.1071/RD03096
Submitted: 8 October 2003 Accepted: 15 April 2004 Published: 22 July 2004
Abstract
The human Y chromosome is running out of time. In the last 300 million years, it has lost 1393 of its original 1438 genes, and at this rate it will lose the last 45 in a mere 10 million years. But there has been a proposal that perhaps rescue is at hand in the form of recently discovered gene conversion within palindromes. However, I argue here that although conversion will increase the frequency of variation of the Y (particularly amplification) between Y chromosomes in a population, it will not lead to a drive towards a more functional Y. The forces of evolution have made the Y a genetically isolated, non-recombining entity, vulnerable to genetic drift and selection for favourable new variants sharing the Y with damaging mutations. Perhaps it will even speed up the decline of the Y chromosome and the onset of a new round of sex-chromosome differentiation. The struggle to preserve males may perhaps lead to hominid speciation.
Aitken, R. J. , and Graves, J. A. M. (2002). The future of sex. Nature 415, 963.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Arakawa, Y. , Nishida-Umehara, C. , Matsuda, Y. , Sutou, S. , and Suzuki, H. (2002). X-chromosomal localization of mammalian Y-linked genes in two XO species of the Ryukyu spiny rat. Cytogenet. Genome Res. 99, 303–309.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Baumstark, A. , Makhverdyan, M. , Schulze, A. , Reisert, I. , Vogel, W. , and Just, W. (2001). Exclusion of SOX9 as the testis determining factor in Ellobius lutescens: evidence for another testis determining gene beside SRY and SOX9. Mol. Genet. Metab. 72, 61–66.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bishop, C. E. , Witworth, D. J. , Qin, Y. , Agoulnik, A. I. , Agoulnik, I. U. , Harrison, W. R. , Behringer, R. R. , and Overvbeek, P. A. (2000). A transgenic insertion upstream of Sox9 is associated with dominant XX sex reversal in the mouse. Nat. Genet. 26, 490–494.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Charlesworth, B. (1991). The evolution of sex chromosomes. Science 251, 1030–1033.
| PubMed |
Delbridge, M. L. , Harry, J. L. , Toder, R. , and Graves, J. A. M. (1997). Only one human candidate spermatogenesis gene is conserved on the marsupial Y chromosome. Nat. Genet. 15, 131–136.
| PubMed |
Delbridge, M. L. , Lingenfelter, P. A. , Disteche, C. M. , and Graves, J. A. M. (1999). The candidate spermatogenesis gene RBMY has a homologue on the human X chromosome. Nat. Genet. 22, 223–224.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Delbridge, M. L. , Longepied, G. , and Depeteis, D. (in press). TSPY, the candidate gonadoblastoma gene on the human Y chromosome, has a widely expressed homologue on the X – implications for Y chromosome evolution. Chromosome Res. ,
Ford, C. E. , Jones, K. W. , Polani, P. E. , de Almeida, J. C. , and Briggs, J. H. (1959). A sex chromosome anomaly in the case of gonadal dysgenesis. Lancet 273, 711–713.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Foster, J. W. , and Graves, J. A. M. (1994). An SRY-related sequence on the marsupial X chromosome: implications for the evolution of the mammalian testis-determining gene. Proc. Natl Acad. Sci. USA 91, 1927–1931.
| PubMed |
Fredga, K. (1988). Aberrant chromosomal sex-determining mechanisms in mammals, with special reference to species with XY females. Phil. Trans. R. Soc. Lond. Biol. 322, 83–95.
Graves, J. A. M. (1995). The origin and function of the mammalian Y chromosome and Y-borne genes – an evolving understanding. Bioessays 17, 311–320.
| PubMed |
Graves, J. A. M. , Disteche, C. M. , and Toder, R. (1998). Gene dosage in the evolution and function of mammalian sex chromosomes. Cytogenet. Cell Geneto. 80, 94–103.
| Crossref | GoogleScholarGoogle Scholar |
Graves, J. A. M. (2000). The human Y chromosome, sex determination and spermatogenesis – a feminist view. Biol. Reprod. 63, 667–676.
| Crossref | GoogleScholarGoogle Scholar |
Graves, J. A. M. (2002). The rise and fall of SRY. Trends Genet. 18, 259–264.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Graves, J. A. M. , and Shetty, S. (2001). Sex from W to Z – evolution of vertebrate sex chromosomes and sex determining genes. J. Exp. Zool. 281, 472–481.
| Crossref | GoogleScholarGoogle Scholar |
Hoekstra, H. E. , and Edwards, S. V. (2000). Multiple origins of XY female mice (genus Akodon): phylogenetic and chromosomal evidence. Proc. R. Soc. Lond. B. Biol. Sci. 267, 1825–1831.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Huang, B. , Wang, S. , Lamb, A. N. , and Bartley, J. (1999). Autosomal XX sex reversal caused by duplication of SOX9. J. Med. Genet. 87, 349–353.
| Crossref | GoogleScholarGoogle Scholar |
Hurst, L. D. (1994). Embryonic growth and the evolution of the mammalilan Y chromosome. I. The Y as an attractor for selfish growth factors. Heredity 73, 223–232.
| PubMed |
Jacobs, P. A. , and Strong, J. A. (1959). A case of human intersexuality having a possible XXY sex-determining mechanism. Nature 183, 302.
| PubMed |
Just, W. , Rau, W. , Vogel, W. , Akhverdian, M. , Fredga, K. , Graves, J. A. M. , and Lyapunova, E. (1995). Absence of SRY in species of the vole Ellobius. Nat. Genet. 11, 117–118.
| PubMed |
Kent-First, M. G. , Kol, S. , Muallem, A. , Ofir, R. , Manor, D. , Blazer, S. , and First, N. (1996). The incidence and possible relevance of Y-linked microdeletions in babies born after intracytoplasmic sperm injection and their infertile fathers. Mol. Hum. Reprod. 2, 943–950.
| PubMed |
Lahn, B. , and Page, D. C. (1997). Functional coherence of the human Y chromosome. Science 278, 675–680.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lahn, B. T. , and Page, D. C. (1999a). Retroposition of autosomal mRNA yielded testis-specific gene family on human Y chromosome. Nat. Genet. 21, 429–433.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lahn, B. T. , and Page, D. C. (1999b). Four evolutionary strata on the human X chromosome. Science 286, 964–967.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lander, E. S. , Linton, L. M. , Birren, B. , Nusbaum, C. , Zody, M. C. , and International Human Genome Sequencing Consortium, , et al. (2001). Initial sequencing and analysis of the human genome. Nature 409, 861–921.
| Crossref | GoogleScholarGoogle Scholar |
Makova, K. D. , and Li, W. H. (2002). Strong male-driven evolution of DNA sequences in humans and apes. Nature 416, 624–626.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mazeyrat, S. , Saut, N. , Mattei, M.-G. , and Mitchell, M. J. (1999). RBMY evolved on the Y chromosome from a ubiquitously transcribed X-Y identical gene. Nat. Genet. 22, 224–226.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Meyers-Walling, V. M. , Palmer, V. L. , Acland, G. M. , and Hershfield, B. (1995). Sry-negative XX sex reversal in the American cocker spaniel dog. Mol. Reprod. Dev. 41, 300–305.
| PubMed |
Mitchell, M. J. , Wilcox, S. A. , Watson, J. M. , Lerner, J. L. , Woods, D. R. , Scheffler, J. , Hearn, J. P. , Bishop, C. E. , and Graves, J. A. M. (1998). The origin and loss of the ubiquitin activating enzyme gene on the mammalian Y chromosome. Hum. Mol. Genet. 7, 429–434.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Miyata, T. , Hayashida, H. , Kuma, K. , Mitsuyasu, K. , and Yasunaga, T. (1987). Male-driven molecular evolution: a model and nucleotide sequence analysis. Cold Spring Harb. Symp. Quant. Biol. 52, 863–867.
| PubMed |
Nagamine, C. M. (1994). The testis-determining gene, SRY, exists in multiple copies in Old World rodents. Genet. Res. 64, 151–159.
| PubMed |
Nanda, I. , Shan, Z. , Schartl, M. , Burt, D. W. , and Koehler, M. , et al. (1999). 300 million years of conserved synteny between chicken Z and human chromosome 9. Nat. Genet. 21, 258–259.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ohno, S. (1967). (Springer Verlag: Berlin, Germany.)
O’Neill, R. J. W. , Brennan, F. E. , Delbridge, M. L. , and Graves, J. A. M. (1998). De novo insertion of an intron into the mammalian sex determining gene SRY. Proc. Natl Acad. Sci. USA 95, 1653–1657.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pailhoux, E. , Vigier, B. , Chaffaux, S. , Servel, N. , and Taourit, S. , et al. (2001). A 11.7-kb deletion triggers intersexuality and polledness in goats. Nat. Genet. 29, 453–458.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pask, A. , Renfree, M. B. , and Graves, J. A. M. (2000). The human sex-reversing gene ATRX has a homologue on the marsupial Y chromosome. Proc. Natl Acad. Sci. USA 97, 13198–13202.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Raymond, C. S. , Shamu, C. E. , Shen, M. M. , Seifert, K. J. , Hirsch, B. , Hodgkin, J. , and Zarkower, D. (1998). Evidence for evolutionary conservation of sex-determining genes. Nature 391, 691–695.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Reijo, R. , Lee, T.-Y. , Salo, P. , Alagappan, R. , and Brown, L. G. , et al. (1995). Diverse spermatogenic defects in humans caused by Y chromosome deletions encompassing a novel RNA-binding protein gene. Nat. Genet. 10, 383–393.
| PubMed |
Repping, S. , Skaletsky, H. , Brown, L. , van Dalen, S. K. M. , and Korver, C. M. , et al. (2003a). Polymorphism for a 1.6-Mb deletion of the human Y chromosome persisits through balance between recurrent mutation and haploid selection. Nat. Genet. 35, 247–251.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Repping, S. , de Vries, J. W. A. , van Daalen, S. K. M. , Korver, C. M. , Leschot, N. J. , and van der Veen, F. (2003b). The use of sperm HALO-FISH to determine DAZ gene copy number. Mol. Hum. Reprod. 9, 183–188.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rice, W. R. (1987). The accumulation of sexually antagonistic genes as selective agent promoting the evolution of reduced recombination between primitive sex chromosomes. Evolution 41, 911–914.
Rozen, S. , Skaletsky, H. , Marzalek, J. D. , Minx, P. J. , Cordum, H. S. , Waterston, R. H. , Wilson, R. K. , and Page, D. C. (2003). Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature 423, 873–876.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sandstedt, S. A. , and Tucker, P. K. (2004). Evolutionary strata on the mouse X chromosome correspond to strata on the human X chromosome. Genome Res. 14( ), 267–272.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sinclair, A. H. , Berta, P. , Palmer, M. S. , Hawkins, J. R. , Griffiths, B. L. , Smith, M. J. , Foster, J. W. , Frischauf, A. M. , Lovell-Badge, R. , and Goodfellow, P. N. (1990). A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346, 240–244.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Skaletsky, H. , Kuroda-Kawaguchi, T. , Minx, P. J. , Cordum, H. S. , and Hillier, L. , et al. (2003). The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423, 825–837.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sun, C. , Skaletsky, H. , Birren, B. , Devon, K. , Tang, Z. , Silber, S. , Oates, R. , and Page, D. C. (1999). An azoospermic man with a de novo point mutation in the Y-chromosomal gene USP9Y. Nat. Genet. 23, 429–432.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Surani, M. A. , Kothary, R. , Allen, N. D. , Singh, P. B. , Fundele, R. , Ferguson-Smith, A. C. , and Barton, S. C. (1990). Genomic imprinting and development on the mouse. Development , 89–98.
Sutou, S. , Mitsui, Y. , and Tsuchiya, K. (2001). Sex determination without the Y chromosome in two Japanese rodents Tokudaia osimensis osimensis and Tokudaia osimensis spp. Mamm. Genome 12, 17–21.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sykes, B. (2003). (Transworld Publishers: London, UK.)
Tyler-Smith, C. , and McVean, G. (2003). The comings and goings of a Y polymorphism. Nat. Genet. 35, 201–202.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Waters, P. , Duffy, B. , Frost, C. J. , Delbridge, M. L. , and Graves, J. A. M. (2001). The human Y chromosome derives largely from a single autosomal region added 80–130 million years ago. Cytogenet. Cell Genet. 92, 74–79.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Weaver, R. (1999). (McGraw Hill: Boston, MA, USA.)
Wyckoff, G. J. , Li, J. , and Wu, C.-I. (2002). Molecular evolution of functional genes on the mammalian Y chromosome. Mol. Biol. Evol. 19, 1633–1636.
| PubMed |