Homologous sex chromosomes in three deeply divergent anuran species

Evolution

Volumn 67, Issue 8, 2013, Pages 2434-2440

  Brelsford, Alan ^a   Stöck, Matthias ^a,b   Betto Colliard, Caroline ^a   Dubey, Sylvain ^a   Dufresnes, Christophe ^a   Jourdan Pineau, Hélène ^a   Rodrigues, Nicolas ^a   Savary, Romain ^a   Sermier, Roberto ^a   Perrin, Nicolas ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

Author keywords

Amphibian; Bufo siculus; Conserved synteny; Convergent evolution; DMRT1; Hyla arborea; Rana temporaria; Sex chromosome turnover

Indexed keywords

DMRT1 PROTEIN; TRANSCRIPTION FACTOR;

BIOMARKER; CHROMOSOME; COMPARATIVE STUDY; DATA ACQUISITION; GENE EXPRESSION; GENOME; SPECIES DIVERSITY; VERTEBRATE;

AMPHIBIA; ANIMAL; ANURA; ARTICLE; BUFO SICULUS; CLASSIFICATION; CONSERVED SYNTENY; CONVERGENT EVOLUTION; DMRT1; GENETICS; HYLA ARBOREA; RANA TEMPORARIA; SEX CHROMOSOME; SEX CHROMOSOME TURNOVER; SEX DETERMINATION PROCESS;

AMPHIBIAN; BUFO SICULUS; CONSERVED SYNTENY; CONVERGENT EVOLUTION; DMRT1; HYLA ARBOREA; RANA TEMPORARIA; SEX CHROMOSOME TURNOVER;

ANIMALS; ANURA; SEX CHROMOSOMES; SEX DETERMINATION PROCESSES; TRANSCRIPTION FACTORS;

EID: 84880822401     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12151     Document Type: Article

References (49)

1. Bachtrog, D., M. Kirkpatrick, J. E. Mank, S. F. McDaniel, J. C. Pires, W. R. Rice, and N. Valenzuela 2011. Are all sex chromosomes created equal? Trends Genet. 27:350-357.
2. Bellott, D. W., H. Skaletsky, T. Pyntikova, E. R. Mardis, T. Graves, C. Kremitzki, L. G. Brown, S. Rozen, W. C. Warren, R. K. Wilson, et al. 2010. Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition. Nature 466:612-616.
3. Berset-Brändli, L., J. Jaquiéry, S. Dubey, and N. Perrin 2006. A sex-specific marker reveals male heterogamety in European tree frogs. Mol. Biol. Evol. 23:1104-1106.
4. Berset-Brändli, L., J. Jaquiéry, T. Broquet, Y. Ulrich, and N. Perrin 2008. Extreme heterochiasmy and nascent sex chromosomes in European tree frogs. Proc. R. Soc. Lond. B 275:1577-1585.
5. Bewick, A. J., D. W. Anderson, and B. J. Evans 2011. Evolution of the closely related, sex-related genes DM-W and DMRT1 in African clawed frogs (Xenopus). Evolution 65:698-712.
6. Blaser, O., C. Grossen, S. Neuenschwander, and N. Perrin 2013. Sex-chromosome turnovers induced by deleterious mutation load. Evolution 67:635-645.
7. Bradley, K. M., J. P. Breyer, D. B. Melville, K. W. Broman, E. W. Knapik, and J. R. Smith 2011. An SNP-based linkage map for zebrafish reveals sex determination loci. G3 1:3-9.
8. Brunner, B., U. Hornung, Z. Shan, I. Nanda, M. Kondo, E. Zend-Ajusch, T. Haaf, H. H. Ropers, A. Shima, M. Schmid, et al. 2001. Genomic organization and expression of the doublesex-related gene cluster in vertebrates and detection of putative regulatory regions for DMRT1. Genomics 77:8-17.
9. Cano, J. M., M. H. Li, A. Laurila, J. Vilkki, and J. Merilä 2011. First-generation linkage map for the common frog Rana temporaria reveals sex-linkage group. Heredity 107:530-536.
10. Charlesworth, D., and J. E. Mank 2010. The birds and the bees and the flowers and the trees: lessons from genetic mapping of sex determination in plants and animals. Genetics 186:9-31.
11. Colliard, C., A. Sicilia, G. F. Turrisi, M. Arculeo, N. Perrin, and M. Stöck 2010. Strong reproductive barriers in a narrow hybrid zone of West-Mediterranean green toads (Bufo viridis subgroup) with Plio-Pleistocene divergence. BMC Evol. Biol. 10:232.
12. Evans, B. J., R. A. Pyron, and J. J. Wiens 2012. Polyploidization and sex chromosome evolution in amphibians. Pp. 385-410 in P. S. Soltis and D. E. Soltis, eds. Polyploidy and genome evolution. Springer Verlag, Heidelberg.
13. Gamble, T., and D. Zarkower 2012. Sex determination. Curr. Biol. 22:R257-R252.
14. Graves, J. A. M., and C. L. Peichel 2010. Are homologies in vertebrate sex determination due to shared ancestry or to limited options? Genome Biol. 11:205-217.
15. Graves, J. A. M. 2013. How to evolve new vertebrate sex determining genes. Dev. Dynam. 242:354-359.
16. Hellsten, U., R. M. Harland, M. J. Gilchrist, D. Hendrix, J. Jurka, V. Kaptonov, I. Ovcharenko, N. H. Putnam, S. Shu, L. Taher, et al. 2010. The genome of the western clawed frog Xenopus tropicalis. Science 328:633-636.
17. Mácha, J., R. Teichmanová, A. K. Sater, D. E. Wells, T. Tlapáková, L. B. Zimmerman, and V. Krylov 2012. Deep ancestry of mammalian X chromosome revealed by comparison with the basal tetrapod Xenopus tropicalis. BMC Genom. 13:315.
18. Mank, J. E. 2009. Sex chromosomes and the evolution of sexual dimorphism: lessons from the genome. Am. Nat. 171:141-150.
19. Matson, C. K., and D. Zarkower 2012. Sex and the singular DM domain: insights into sexual regulation, evolution, and plasticity. Nat. Rev. Genet. 13:163-174.
20. Matson, C. K., M. W. Murphy, A. L. Sarver, M. D. Griswold, V. J. Bardwell, and D. Zarkower 2011. DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 476:101-105.
21. Matsuba, C., I. Miura, and J. Merilä 2008. Disentangling genetic vs. environmental causes of sex determination in the common frog, Rana temporaria. BMC Genet. 9:3.
22. Matsuda, M., Y. Nagahama, A. Shinomiya, T. Sato, C. Matsuda, T. Kobayashi, C. E. Morrey, N. Shibata, S. Asakawa, N. Shimizu, et al. 2002. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 18;417:559-563.
23. Miura, I. 1995. The late replication banding patterns of chromosomes are highly conserved in the genera Rana, Hyla, and Bufo (Amphibia: Anura). Chromosoma 103:567-574.
24. Miura, I. 2007. An evolutionary witness: the frog Rana rugosa underwent change of heterogametic sex from XY male to ZW female. Sex. Dev. 1:323-331.
25. Miura, I., H. Ohtani, M. Nakamura, Y. Ichikawa, and K. Saitoh 1998. The origin and differentiation of the heteromorphic sex chromosomes Z, W, X, and Y in the frog Rana rugosa, inferred from the sequences of a sex-linked gene, ADP/ATP translocase. Mol. Biol. Evol. 15:1612-1619.
26. Nanda, I., M. Kondo, U. Hornung, S. Asakawa, C. Winkler, A. Shimizu, Z. H. Shan, T. Haaf, N. Shimizu, A. Shima, et al. 2002. A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc. Natl. Acad. Sci. USA 99:11778-11783.
27. Niculita-Hirzel, H., M. Stöck, and N. Perrin 2008. A key transcription cofactor on the nascent sex-chromosomes of European tree frogs (Hyla arborea). Genetics 179:1721-1723.
28. O'Meally, D., T. Ezaz, A. Georges, S. D. Sarre, and J. A. M. Graves 2012. Are some chromosomes particularly good at sex? Insights from amniotes. Chromosome Res. 20:7-19.
29. Olmstead, A. W., A. Lindberg-Livingston, and S. J. Degitz 2010. Genotyping sex in the amphibian, Xenopus (Silurana) tropicalis, for endocrine disruptor bioassays. Aquat. Toxicol. 98:60-66.
30. Oshima, Y., K. Naruse, Y. Nakamura, and M. Nakamura 2009. Sox3: a transcription factor for Cyp19 expression in the frog Rana rugosa. Gene 445:38-48.
31. Pease, J. B., and M. W. Hahn 2012. Sex chromosomes evolved from independent ancestral linkage groups in winged insects. Mol. Biol. Evol. 29:1645-1653.
32. Raymond, C. S., C. E. Shamu, M. M. Shen, K. J. Seifert, B. Hirsch, J. Hodgkin, and D. Zarkower 1998. Evidence for evolutionary conservation of sex-determining genes. Nature 391:691-695.
33. Rice, W. R. 1984. Sex chromosomes and the evolution of sexual dimorphism. Evolution. 38:735-742.
34. Rodrigues, N., C. Betto-Colliard, H. Jourdan-Pineau, and N. Perrin Within-population polymorphism of sex-determination systems in the common frog (Rana temporaria). J. Evol. Biol.: In press.
35. Schartl, M., 2004. Sex chromosome evolution in non-mammalian vertebrates. Curr. Opin. Genet. Dev. 14:634-641.
36. Smith, C. A., K. N. Roeszler, T. Ohnesorg, D. M. Cummins, P. G. Farlie, T. J. Doran, and A. H. Sinclair 2009. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461:267-271.
37. Stöck, M., A. Horn, C. Grossen, D. Lindtke, R. Sermier, C. Betto-Colliard, C. Dufresnes, E. Bonjour, Z. Dumas, E. Luquet, et al. 2011a. Ever-young sex chromosomes in European tree frogs. PLoS Biol. 9:e1001062.
38. Stöck, M., D. Croll, Z. Dumas, S. Biollay, J. Wang, and N. Perrin 2011b. A cryptic heterogametic transition revealed by sex-linked DNA markers in Palearctic green toads. J. Evol. Biol. 24:1064-1070.
39. Stöck, M., R. Savary, C. Betto-Colliard, S. Biollay, H. Jourdan-Pineau, and N. Perrin 2013. Low rates of X-Y recombination, not turnovers, account for homomorphic sex chromosomes in several diploid species of Palearctic green toads (Bufo viridis subgroup). J. Evol. Biol. 26:674-682.
40. Stöck, M., R. Savary, A. Zaborowska, G. Gorecki, A. Brelsford, B. Rozenblut-Koscisty, M. Ogielska, and N. Perrin Maintenance of ancestral sex chromosomes in Palearctic tree frogs: direct evidence from Hyla orientalis. Sex. Dev.: In press.
41. Uno, Y., C. Nishida, Y. Oshima, S. Yokoyama, I. Miura, Y. Matsuda, and M. Nakamura 2008. Comparative chromosome mapping of sex-linked genes and identification of sex chromosomal rearrangements in the Japanese wrinkled frog (Rana rugosa, Ranidae) with ZW and XY sex chromosome systems. Chromosome Res. 16:637-647.
42. van Doorn, G. S., and M. Kirkpatrick 2007. Turnover of sex chromosomes induced by sexual conflict. Nature 449:909-912.
43. Vicoso, B., and B. Charlesworth 2006. Evolution on the X chromosome: unusual patterns and processes. Nat. Rev. Genet. 7:645-653.
44. Volff, J. N., I. Nanda, M. Schmid, and M. Schartl 2007. Governing sex determination in fish: regulatory putsches and ephemeral dictators. Sex. Dev. 1:85-99.
45. Wells, D. E., L. Gutierrez, Z. Xu, V. Krylov, J. Macha, K. P. Blankenburg, M. Hitchens, L. J. Bellot, M. Spivey, D. L. Stemple, et al. 2011. A genetic map of Xenopus tropicalis. Dev. Biol. 354:1-8.
46. Wilkins, A. S. 1995. Moving up the hierarchy: a hypothesis on the evolution of a genetic sex determination pathway. BioEssays 17:71-77
47. Woram, R. A., K. Gharbi, T. Sakamoto, B. Hoyheim, L. E. Holm, K. Naish, C. McGowan, M. M. Ferguson, R. B. Phillips, J. Stein, et al. 2003. Comparative genome analysis of the primary sex-determining locus in salmonid fishes. Genome Res. 13:272-280.
48. Yano, A., B. Nicol, E. Jouanno, E. Quillet, A. Fostier, R. Guyomard, and Y. Guiguen 2013. The sexually dimorphic on the Y-chromosome gene (sdY) is a conserved male-specific Y-chromosome sequence in many salmonids. Evol. Appl. 6:486-496.
49. Yoshimoto, S., E. Okada, H. Umemoto, K. Tamura, Y. Uno, C. Nishida-Umehara, Y. Matsuda, N. Takamatsu, T. Shiba, and M. Ito 2008. A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc. Natl. Acad. Sci. USA 105:2469-2474.