Sex determination and sex chromosome evolution in the medaka, <i>Oryzias latipes,</i> and the platyfish, <i>Xiphophorus maculatus</i>

Abstract

The first vertebrate master sex-determining gene different from Sry has been very recently discovered in a small aquarium fish, the medaka (Oryzias latipes). In this fish, the X and Y chromosomes apparently differ only by a 250-kb Y-specific region containing dmrt1bY (also called DMY and dmrt1Y), a male-specific copy of the autosomal gene dmrt1. Dmrt1 is a putative transcription factor probably involved in testis formation in different vertebrate lineages. Dmrt1bY is the only gene having escaped the drastic process of degeneration that devastated the small Y-specific region of the medaka. Mutations leading to truncation or lower expression of dmrt1bY result in XY male-to-female sex reversal. Hence, both genetic and functional evidences converge in making dmrt1bY an outstanding candidate for the function of a master sex-determining gene in fish. Nevertheless, dmrt1bY could not be detected in certain other Oryzias species or in more divergent fishes. Phylogenetic analysis revealed that the duplication of the autosomal dmrt1 that formed dmrt1bY is young in evolutionary terms. Hence, dmrt1bY is not the universal master sex-determining gene in fish. Because the classical fish models, such as zebrafish and pufferfish, are not very adequate to study the basis of genetic sex determination, alternative models, such as the platyfish (Xiphophorus maculatus), are re-emerging. In this fish, which is a well-suited laboratory organism, gene loci involved in pigmentation, melanoma formation, and sexual maturity have been mapped close to the master sex-determining gene. Interestingly, the platyfish can harbor three different sex chromosomes (W, X, and Y) in certain natural populations. Bacterial artificial chromosome contigs covering the sex-determining region of the platyfish are already available, and the positional cloning of the master sex-determining gene(s) should provide new insights into sex determination and sex chromosome evolution in fish and other vertebrates.

Genome evolution and biodiversity in teleost fish

“…This is particularly true for the sex chromosomes, and this phenomenon might be related to the amazing variety of sex determination systems observed in teleosts (for reviews, Baroiller and D'Cotta, 2001; Devlin and Nagahama, 2002; Volff and Schartl, 2002). All different forms of genetic sex determination have been observed in fish, including both male heterogamety (males are XY and females are XX) and female heterogamety (males are ZZ and females are ZW), autosomal influences and polygenic sex determination.…”

“…Several topics are investigated in parallel in different species. Sex determination and sex differentiation are studied in numerous fishes including medaka, zebrafish, salmonids, platyfish, sticklebacks, tilapia and others (Baroiller and D'Cotta, 2001;Devlin and Nagahama, 2002;Volff and Schartl, 2002). Such comparative analyses are of the highest importance to understand the mechanisms driving differential evolution in fish sublineages.…”

“…Dmrt1bY has probably been formed by a large transchromosomal duplication from linkage group 9 onto another autosome, which became the neo-Y-chromosome by this way Volff and Schartl, 2002;Schartl, 2004). Other genes were included in this duplication, but, in contrast to dmrt1bY, they all subsequently degenerated .…”

Mapping Loci Associated With Tail Color and Sex Determination in the Short-Lived Fish Nothobranchius furzeri

“…Sex can be determined either genetically or environmentally in fish (Volff 2005;Marshall Graves 2008). For example, medaka, platyfish, guppy, and sticklebacks all have recently evolved genetic sex-determining systems (Volff and Schartl 2002;Peichel et al 2004;Shapiro et al 2009;Tripathi et al 2009a), whereas zebrafish do not have a clear genetic basis of sex determination (von Hofsten and Olsson 2005).…”

Linkage Analysis Reveals the Independent Origin of Poeciliid Sex Chromosomes and a Case of Atypical Sex Inheritance in the Guppy (Poecilia reticulata)

“…Similarly, the sex-determining loci of different salmonids (Phillips et al 2005(Phillips et al , 2007Artieri et al 2006) and of two species of stickleback (Gasterosteus) have apparently evolved from loci originating on distinct ancestral chromosomes (Woram et al 2003;Charlesworth 2004;Peichel et al 2004). In the threespine stickleback Gasterosteus aculeatus (Peichel et al 2004), the tiger pufferfish Takifugu rubripes (Kikuchi et al 2007), the rainbow trout (Alfaqih et al 2009), and the platyfish Xiphophorus maculatus (Volff and Schartl 2002), the SDL could be mapped to a specific linkage group that represents the differentiating Y chromosome. Fine mapping of these loci is impeded by suppression of meiotic recombination and by frequent occurrence of repetitive sequences in the gonosomal region of the Y chromosome (Nanda et al 1993;Peichel et al 2004).…”