Ever-young sex chromosomes in European tree frogs

PLoS Biology

Volumn 9, Issue 5, 2011, Pages

  Stöck, Matthias ^a   Horn, Agnès ^a   Grossen, Christine ^a   Lindtke, Dorothea ^a,b   Sermier, Roberto ^a   Betto Colliard, Caroline ^a   Dufresnes, Christophe ^a   Bonjour, Emmanuel ^a   Dumas, Zoé ^a,c   Luquet, Emilien ^d   Maddalena, Tiziano ^e   Sousa, Helena Clavero ^a,f   Martinez Solano, Iñigo ^g   Perrin, Nicolas ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY OF FRIBOURG   (Switzerland)

^c SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

^d UNIVERSITÉ DE LYON   (France)

^e Gordevio   (Switzerland)

^f Perpetuo Socorro   (Spain)

^g INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS IREC CSIC UCLM JCCM   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHEEK MUCOSA; CHROMOSOME ANALYSIS; CHROMOSOME STRUCTURE; CONTROLLED STUDY; FEMALE; FROG; GENE; GENE SEQUENCE; GENETIC POLYMORPHISM; GENETIC RECOMBINATION; GENETIC REGULATION; GENETIC VARIABILITY; MALE; MICROSATELLITE MARKER; MITOCHONDRIAL GENE; NONHUMAN; NUCLEAR GENE; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEX CHROMOSOME HOMOMORPHY; SEX LINKAGE; SEX TRANSFORMATION; SPECIES COMPARISON; SRY GENE; TREE FROG; UPPER MIOCENE; X CHROMOSOME; Y CHROMOSOME; ANIMAL; BIOLOGICAL MODEL; FROGS AND TOADS; GENE FREQUENCY; GENETIC LINKAGE; GENETIC MARKER; GENETICS; SEX DETERMINATION PROCESS; SPECIES DIFFERENTIATION; STATISTICAL MODEL; X CHROMOSOMAL INHERITANCE; Y CHROMOSOMAL INHERITANCE;

AVES; HYLA ARBOREA; HYLIDAE; MAMMALIA; VERTEBRATA;

ANIMALS; ANURA; FEMALE; GENE FREQUENCY; GENES, X-LINKED; GENES, Y-LINKED; GENETIC LINKAGE; GENETIC MARKERS; GENETIC SPECIATION; LIKELIHOOD FUNCTIONS; MALE; MODELS, GENETIC; PHYLOGENY; RECOMBINATION, GENETIC; SEX DETERMINATION PROCESSES; X CHROMOSOME; Y CHROMOSOME;

EID: 79958037603     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001062     Document Type: Article

References (53)

1. Lahn B. T, Page D. C, (1999) Four evolutionary strata on the human X chromosome. Science 286: 964-967.
2. Graves J. A. M, (2006) Sex chromosome specialization and degeneration in mammals. Cell 124: 901-914.
3. Rice W. R, (1996) Evolution of the Y sex chromosome in animals. Bioscience 46: 331-343.
4. Charlesworth B, Charlesworth D, (2000) The degeneration of Y chromosomes. Phil Trans R Soc Lond B 355: 1563-1572.
5. Lawson Handley L. J, Ceplitis H, Ellegren H, (2004) Evolutionary strata on the chicken Z chromosome: implications for sex chromosome evolution. Genetics 167: 367-376.
6. Steinemann S, Steinemann M, (2005) Y chromosomes: born to be destroyed. BioEssays 27: 1076-1083.
7. Hughes J. F, Skaletsky H, Pyntikova T, Graves T. A, van Daalen S. K. M, et al. (2010) Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature 463: 536-539.
8. Eggert C, (2001) Sex determination: the amphibian model. Reprod Nutr Dev 44: 539-549.
9. Devlin R. H, Nagahama Y, (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208: 191-364.
10. Volff J. N, Nanda I, Schmid M, Schartl M, (2007) Governing sex determination in fish: regulatory putches and ephemeral dictators. Sex Dev 1: 85-99.
11. Tanaka K, Takehana K, Naruse K, Hamaguchi S, Sakaizumi M, (2007) Evidence for different origins of sex chromosomes in closely related Oryzias fishes: substitution of the master sex-determining gene. Genetics 177: 2075-2081.
12. Ross J. A, Urton J. R, Boland J, Shapiro M. D, Peichel C. L, (2009) Turnover of sex chromosomes in the stickleback fishes. PLoS Genet 5: e1000391 doi:10.1371/journal.pgen.1000391.
13. Cnaani A, Lee B. Y, Zilberman N, Ozouf-Costaz C, Hulata G, et al. (2008) Genetics of sex determination in Tilapiine species. Sex Dev 2: 43-54.
14. 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.
15. Hillis D. M, Green D. M, (1990) Evolutionary changes of heterogametic sex in the phylogenetic history of amphibians. J Evol Biol 3: 49-64.
16. Perrin N, (2009) Sex reversal, a fountain of youth for sex chromosomes? Evolution 63: 3043-3049.
17. Inoue H, Fukumori Y, Hiroyoshi T, (1983) Mapping of autosomal male-determining factors of the housefly, Musca domestica L., by means of sex-reversal. Japan J Genet 58: 451-461.
18. Wallace H, Wallace B. M. N, Badawy G. M. I, (1997) Lampbrush chromosomes and chiasmata of sex-reversed crested newts. Chromosoma 106: 526-533.
19. Lynn A, Schrump S, Cherry J, Hassold T, Hunt P, (2005) Sex, not genotype, determines recombination levels in mice. Am J Hum Genet 77: 670-675.
20. Campos-Ramos R, Harvey S. C, Penman D. J, (2009) Sex-specific differences in the synaptonemal complex in the genus Oreochromis (Cichlidae). Genetica 135: 325-332.
21. Matsuda M, Sotoyama S, Hamaguchi S, Sakaizumi M, (1999) Male-specific restriction of recombination frequency in the sex chromosomes of the medaka, Oryzias latipes. Genet Res 73: 225-231.
22. Kondo M, Nagao E, Mitani H, Shima A, (2001) Differences in recombination frequencies during female and male meioses of the sex chromosomes of the medaka, Oryzias latipes. Genet Res 78: 23-30.
23. Matsuba C, Alho J, Merilä J, (2010) Recombination rate between sex chromosomes depends on phenotypic sex in the common frog. Evolution 64: 3634-3637.
24. Dournon C, Houillon C, Pieau C, (1990) Temperature sex-reversal in amphibians and reptiles. Int J Dev Biol 34: 81-92.
25. Baroiller J. F, D'Cotta H, Bezault E, Wessels S, Hoerstgen-Schwark G, (2009) Tilapia sex determination: where temperature and genetics meet. Comp Biochem Physiol A 153: 30-38.
26. Grossen C, Neuenschwander S, Perrin N, (2011) Temperature-dependent turnovers in sex-determination mechanisms: a quantitative model. Evolution 65: 64-78.
27. Anderson K, (1991) Chromosome evolution in Holarctic Hyla treefrogs. In: Green D. M, Sessions S. K, editors. Amphibian cytogenetics and evolution San Diego Academic Press pp. 299-312.
28. Berset-Brändli L, Jaquiéry J, Dubey S, Perrin N, (2006) A sex-specific marker reveals male heterogamety in European tree frogs. Mol Biol Evol 23: 1104-1106.
29. Berset-Brändli L, Jaquiéry J, Perrin N, (2007) Recombination is suppressed and variability reduced in a nascent Y chromosome. J Evol Biol 20: 1182-1188.
30. Berset-Brändli L, Jaquiéry J, Broquet T, Ulrich Y, Perrin N, (2008) Extreme heterochiasmy and nascent sex chromosomes in European tree frogs. Proc R Soc B 275: 1577-1585.
31. Niculita-Hirzel H, Stöck M, Perrin N, (2008) A key transcription cofactor on the nascent sex chromosomes of European tree frogs (Hyla arborea). Genetics 179: 1721-1723.
32. Stöck M, Dubey S, Kluetsch K, Litvinchuk L. S, Scheidt U, et al. (2008) Mitochondrial and nuclear phylogeny of circum-Mediterranean tree frogs from the Hyla arborea group. Mol Phylogenet Evol 49: 1019-1024.
33. Graves J. A. M, Peichel C. L, (2010) Are homologies in vertebrate sex determination due to shared ancestry or to limited options? Gen Biol 11: 205-217.
34. Morton N. E, (1956) The detection and estimation of linkage between the genes for elliptocytosis and the Rh blood type. Amer J Hum Genet 8: 80-96.
35. Pecon Slattery J, Sanner-Wachter L, O'Brien S. J, (2000) Novel gene conversion between X-Y homologues located in the non-recombining region of the Y chromosome in Felidae (Mammalia). Proc Natl Acad Sci U S A 97: 5307-5312.
36. Marais G, Galtier N, (2003) Sex chromosomes: how X-Y recombination stops. Curr Biol 13: R641-R643.
37. Andolfatto P, Depaulis F, Navarro A, (2001) Inversion polymorphisms and nucleotide variability in Drosophila. Genet Res Camb 77: 1-8.
38. Tease C, Hulten M. A, (2004) Inter-sex variation in synaptonemal complex lengths largely determines the different recombination rates in male and female germ cells. Cytogenet Genome Res 107: 208-215.
39. Ogielska M, (2009) Reproduction of amphibians. Enfield Science Publishers.
40. Smalley S. L, (1993) Sex-specific recombination frequencies: a consequence of imprinting? Am J Hum Genet 52: 210-212.
41. Paldi A, Gyapay G, Jami J, (1995) Imprinted chromosomal regions of the human genome display sex-specific meiotic recombination frequencies. Curr Biol 5: 1030-1035.
42. Kirkpatrick M, Guerrero R. F, Scarpino S. V, (2010) Patterns of neutral genetic variation on recombining sex chromosomes. Genetics 184: 1141-1152.
43. van Doorn G. S, Kirkpatrick M, (2010) Transitions between male and female heterogamety caused by sex-antagonistic selection. Genetics 186: 629-645.
44. Broquet T, Berset-Brändli L, Emaresi G, Fumagalli L, (2007) Buccal swabs allow efficient and reliable microsatellite genotyping in amphibians. Conserv Gene 8: 509-511.
45. Berset-Brändli L, Jaquiéry J, Broquet T, Perrin N, (2008) Isolation and characterization of microsatellite loci for the European tree frog (Hyla arborea). Mol Ecol Res 8: 1095-1097.
46. Arens P, Van't Westende W, Butger R, Smulders M. J. M, Vosman B, (2000) Microsatellite markers for the European tree frog Hyla arborea. Mol Ecol 9: 1919-1952.
47. Goudet J, (2001) FSTAT 2.9.3, a program to estimate and test gene diversities and fixation indices. Available:http://www2.unil.ch/popgen/softwares/fstat.htm.
48. Green P, Falls K. A, Crooks S, (1990) CRIMAP, 2.4. St Louis, MO: Washington University School of Medicine.http://linkage.rockefeller.edu/soft/crimap/.
49. Guindon S, Gascuel O, (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.http://www.atgc-lirmm.fr/phyml/.
50. Mulcahy D. G, Mendelson J. R, (2000) Phylogeography and speciation of the morphologically variable, widespread species Bufo valliceps, based on molecular evidence from mtDNA. Mol Phyl Evol 17: 173-189.
51. Rowe D, Harris D. J, Beebee T. J. C, (2006) Lusitania revisited: a phylogeographic analysis of the natterjack toad Bufo calamita across its entire biogeographical range. Mol Phyl Evol 39: 335-346.
52. Drummond A. J, Ho S. Y. W, Rawlence N, Rambaut A, (2007) A rough guide to BEAST 1.4. Available:http://code.google.com/p/beast-mcmc/downloads/detail?name=BEAST14_Manual_6July2007.pdf.
53. Hoegg S, Vences M, Brinkmann H, Meyer A, (2004) Phylogeny and comparative substitution rates of frogs inferred from sequences of three nuclear genes. Mol Biol Evol 21: 1188-1200.