Evolutionary Biology

, Volume 38, Issue 2, pp 208–213 | Cite as

Polymorphism at a Sex-Linked Transcription Cofactor in European Tree Frogs (Hyla arborea): Sex-Antagonistic Selection or Neutral Processes?

  • Christophe DufresnesEmail author
  • Emilien Luquet
  • Sandrine Plenet
  • Matthias Stöck
  • Nicolas Perrin
Research Article


Nascent sex chromosomes offer a unique opportunity to investigate the evolutionary fate of genes recently trapped in non-recombining segments. A house-keeping gene (MED15) was recently shown to lie on the nascent sex-chromosomes of the European tree frog (Hyla arborea), with different alleles fixed on the X and the Y chromosomes. Here we document a polymorphism (glutamine deletion) in the X copy of the gene, and use population surveys and experimental crosses to test whether this polymorphism is neutral or maintained by sex-antagonistic selection. Tadpoles from parents of known genotypes revealed significant discrepancies from Mendelian inheritance, suggesting possible sex-antagonistic effects under laboratory conditions. Quantitatively, however, these effects did not meet the conditions for polymorphism maintenance. Furthermore, field estimates of female genotypic frequencies did not differ from Hardy–Weinberg equilibrium and allelic frequencies on the X chromosome did not differ between sexes. In conclusion, although sex-antagonistic effects cannot be excluded given the laboratory conditions, the X-linked polymorphism under study appears neutral in the wild. Alternatively, sex-antagonistic selection might still account for the fixation of a male-specific allele on the Y chromosome.


Amphibians Hyla arborea Glutamine repeats Population genetics Sex chromosomes Transcription cofactor MED15 



Hardy–Weinberg equilibrium




Non significant



P. Joly, J. P. Léna, J. Prunier, J. Chiaffi, D. Serol, C. Vialet and R. Gautron provided much-welcome help for the fieldwork, R. Sermier and K. Ghali for the lab work. This study was supported by the Swiss National Science Foundation for Scientific Research (Grant 3100A0-108100 to NP) and the French National Research Agency (ANR Grant COLAPSE BLAN06-1_158236 to Pierre Joly).


  1. Albert, A. Y. K., & Otto, S. P. (2005). Sexual selection can resolve sex-linked sexual antagonism. Science, 310, 119–121.PubMedCrossRefGoogle Scholar
  2. Arens, P., Van’t Westende, W., Bugter, R., Smulders, M. J. M., & Vosman, B. (2000). Microsatellite markers for the European tree frog Hyla arborea. Molecular Ecology, 9, 1944–1946.PubMedCrossRefGoogle Scholar
  3. Bachtrog, D. (2004). Evidence that positive selection drives Y-chromosome degeneration in Drosophila miranda. Nature Genetics, 36, 518–522.PubMedCrossRefGoogle Scholar
  4. Berset-Brändli, L., Jaquiery, J., Dubey, S., & Perrin, N. (2006). A sex-specific marker reveals male heterogamety in European tree frogs. Molecular Biology and Evolution, 23, 1104–1106.PubMedCrossRefGoogle Scholar
  5. Berset-Brändli, L., Jaquiery, J., & Perrin, N. (2007). Recombination is suppressed and variability reduced in a nascent Y chromosome. Journal of Evolutionary Biology, 20, 1182–1188.PubMedCrossRefGoogle Scholar
  6. Broquet, T., Berset-Brändli, L., Emaresi, G., & Fumagalli, L. (2007). Buccal swabs allow efficient and reliable microsatellite genotyping in amphibians. Conservation Genetics, 8, 509–511.CrossRefGoogle Scholar
  7. Buchanan, G., Yang, M., Cheong, A., Harris, J. M., Irvine, R. A., Lambert, P. F., et al. (2004). Structural and functional consequences of glutamine tract variation in the androgen receptor. Human Molecular Genetics, 13, 1677–1692.PubMedCrossRefGoogle Scholar
  8. Charlesworth, B. (1991). The evolution of sex-chromosomes. Science, 251, 1030–1033.PubMedCrossRefGoogle Scholar
  9. Charlesworth, B. (2002). The evolution of chromosomal sex determination. In D. Chadwick & J. Goode (Eds.), The genetics and biology of sex determination: Novartis foundation symposium 244 (pp. 207–224). Chichester: John Wiley & Sons Ltd.Google Scholar
  10. Charlesworth, B. (2004). Sex determination: Primitive Y chromosomes in fish. Current Biology, 14, R745–R747.PubMedCrossRefGoogle Scholar
  11. Charlesworth, B., & Charlesworth, D. (2000). The degeneration of Y chromosomes. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 355, 1563–1572.CrossRefGoogle Scholar
  12. Filatov, D. A., Moneger, F., Negrutiu, I., & Charlesworth, D. (2000). Low variability in a Y-linked plant gene and its implications for Y-chromosome evolution. Nature, 404, 388–390.PubMedCrossRefGoogle Scholar
  13. Gerber, H. P., Seipel, K., Georgiev, O., Hofferer, M., Hug, M., Rusconi, S., et al. (1994). Transcriptional activation modulated by homopolymeric glutamine and proline stretches. Science, 263, 808–811.PubMedCrossRefGoogle Scholar
  14. Gibson, J. R., Chippindale, A. K., & Rice, W. R. (2002). The X chromosome is a hot spot for sexually antagonistic fitness variation. Proceedings of the Royal Society of London Series B-Biological Sciences, 269, 499–505.CrossRefGoogle Scholar
  15. Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16, 8.Google Scholar
  16. Haldane, J. B. S. (1922). Sex ratio and unisexual sterility in hybrid animals. Journal of Genetics, 12, 101–109.CrossRefGoogle Scholar
  17. Hancock, J. M., Worthey, E. A., & Santibanez-Koref, M. F. (2001). A role for selection in regulating the evolutionary emergence of disease-causing and other coding CAG repeats in humans and mice. Molecular Biology and Evolution, 18, 1014–1023.PubMedGoogle Scholar
  18. Kondo, M., Nanda, I., Hornung, U., Schmid, M., & Schartl, M. (2004). Evolutionary origin of the medaka Y chromosome. Current Biology, 14, 1664–1669.PubMedCrossRefGoogle Scholar
  19. Liu, Z. Y., Moore, P. H., Ma, H., Ackerman, C. M., Ragiba, M., Yu, Q. Y., et al. (2004). A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature, 427, 348–352.PubMedCrossRefGoogle Scholar
  20. McAllister, B. F., & Charlesworth, B. (1999). Reduced sequence variability on the neo-Y chromosome of Drosophila americana americana. Genetics, 153, 221–233.PubMedGoogle Scholar
  21. Mularoni, L., Veitia, R. A., & Alba, M. M. (2007). Highly constrained proteins contain an unexpectedly large number of amino acid tandem repeats. Genomics, 89, 316–325.PubMedCrossRefGoogle Scholar
  22. Nanda, I., Kondo, M., Hornung, U., Asakawa, S., Winkler, C., Shimizu, A., et al. (2002). A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proceedings of the National Academy of Sciences of the United States of America, 99, 11778–11783.PubMedCrossRefGoogle Scholar
  23. Nei, M. (1969). Linkage modification and sex differences in recombination. Genetics, 63, 681–699.PubMedGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. Peichel, C. L., Ross, J. A., Matson, C. K., Dickson, M., Grimwood, J., Schmutz, J., et al. (2004). The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome. Current Biology, 14, 1416–1424.PubMedCrossRefGoogle Scholar
  26. Perutz, M. F., Johnson, T., Suzuki, M., & Finch, J. T. (1994). Glutamine repeats as polar zippers–their possible role in inherited neurodegenerative diseases. Proceedings of the National Academy of Sciences of the United States of America, 91, 5355–5358.PubMedCrossRefGoogle Scholar
  27. Pidancier, N., Miquel, C., & Miaud, C. (2003). Buccal swabs as a non-destructive tissue sampling method for DNA analysis in amphibians. Herpetological Journal, 13, 175–178.Google Scholar
  28. R Development Core Team. (2007). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
  29. Rice, W. R. (1984). Sex-chromosomes and the evolution of sexual dimorphism. Evolution, 38, 735–742.CrossRefGoogle Scholar
  30. Rice, W. R. (1987). The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex-chromosomes. Evolution, 41, 911–914.CrossRefGoogle Scholar
  31. Rice, W. R., & Chippindale, A. K. (2001). Intersexual ontogenetic conflict. Journal of Evolutionary Biology, 14, 685–693.CrossRefGoogle Scholar
  32. Shimohata, T., Nakajima, T., Yamada, M., Uchida, C., Onodera, O., Naruse, S., et al. (2000). Expanded polyglutamine stretches interact with TAF(II)130, interfering with CREB-dependent transcription. Nature Genetics, 26, 29–36.PubMedCrossRefGoogle Scholar
  33. Steinemann, S., & Steinemann, M. (2005). Y chromosomes: Born to be destroyed. Bioessays, 27, 1076–1083.PubMedCrossRefGoogle Scholar
  34. Stöck, M., Sicilia, A., Belfiore, N. M., Buckley, D., Lo Brutto, S., Lo Valvo, M., et al. (2008). Post-Messinian evolutionary relationships across the Sicilian channel: Mitochondrial and nuclear markers link a new green toad from Sicily to African relatives. BMC Evolutionary Biology, 8, 56.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Christophe Dufresnes
    • 1
    Email author
  • Emilien Luquet
    • 2
  • Sandrine Plenet
    • 2
  • Matthias Stöck
    • 1
  • Nicolas Perrin
    • 1
  1. 1.Department of Ecology and EvolutionUniversity of LausanneLausanneSwitzerland
  2. 2.CNRS UMR 5023, Ecologie des Hydrosystèmes FluviauxUniversité Claude Bernard Lyon1VilleurbanneFrance

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