Integrative and Comparative Biology Advance Access published online on May 13, 2008
Integrative and Comparative Biology, doi:10.1093/icb/icn031
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Evolution of the gene network underlying gonadogenesis in turtles with temperature-dependent and genotypic sex determination
Department of Ecology, Evolution and Organismal Biology, Iowa State University, 253 Bessey Hall, Ames, IA 50011, USA
Correspondence: 1Email: nvalenzu{at}iastate.edu
The evolution of sex determination has long fascinated biologists, as it has paramount consequences for the evolution of a multitude of traits, from sex allocation to speciation and extinction. Explaining the diversity of sex-determining systems found in vertebrates (genotypic or GSD and temperature-dependent or TSD) requires a comprehensive and integrative examination from both a functional and an evolutionary perspective. Particularly revealing is the examination of the gene network that regulates gonadogenesis. Here, I review some advances in this field and propose some additional hypotheses about the composition of the gene network underlying sexual development, the functional links among some of its elements and their evolution in turtles. I focus on several pending questions about: (1) What renders TSD systems thermo-sensitive? (2) Is there one developmentally conserved or multiple TSD mechanisms? (3) Have evolutionarily derived GSD species lost all ancestral thermal-sensitivity? New data are presented on embryonic expression of Dax1 (the dosage-sensitive sex-reversal adrenal hypoplasia congenital on the X chromosome gene in the turtles Chrysemys picta (TSD) and Apalone mutica (GSD). No differential Dax1 expression was detected in C. picta at any of the stages examined, consistent with reports on two other TSD turtles and alligators. Notably, significantly higher Dax1 expression was found at 30°C than at 25°C at stage 15 in A. mutica (GSD), likely caused by Wt1's identical expression pattern previously reported. Because Sf1 is an immediate downstream target of Dax1 and its expression is not affected by temperature, it is proposed that Sf1 renders Dax1's differential signal ineffective to induce biased sex ratios in A. mutica, as previously proposed for Wt1's thermosensitive expression. Thus, it is hypothesized that Sf1 plays a major role in the lack of response of sex ratio to temperature of A. mutica, and may function as a sex-determining gene in this GSD species. These and previous data permit formulating several mechanistic hypotheses: (1) the postulation of Wt1 as a candidate thermal master switch alone, or in combination with Sf1, in the TSD turtle C. picta; (2) the proposition of Sf1 as a sex-determining gene in the GSD turtle A. mutica; and (3) the hypothesis that differing patterns of gene expression among TSD taxa reflect multiple traits from a developmental perspective. Moreover, the recent finding of relic differential Wt1 expression in A. mutica and the results for Dax1 in this species provide empirical evidence that GSD taxa can harbor thermal sensitivity at the level of gene expression, potentially co-optable during TSD evolution.
From the symposium "Developmental and Cell Biology and Evolutionary Developmental Biology" presented at the annual meeting of the Society for the Integrative and Comparative Biology, January 3–6, 2008, at San Antonio, Texas.
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  N. Valenzuela The Painted Turtle, Chrysemys picta: A Model System for Vertebrate Evolution, Ecology, and Human Health CSH Protocols, July 1, 2009; 2009(7): pdb.emo124 - pdb.emo124. [Abstract] [Full Text]
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