Different origins of ZZ/ZW sex chromosomes in closely related medaka fishes, Oryzias javanicus and O. hubbsi

Abstract

Although the sex-determining gene DMY has been identified on the Y chromosome in the medaka, Oryzias latipes, this gene is absent in most Oryzias species. Recent comparative studies have demonstrated that, in the javanicus species group, Oryzias dancena and Oryzias minutillus have an XX/XY sex determination system, while Oryzias hubbsi has a ZZ/ZW system. Furthermore, sex chromosomes were not homologous in these species. Here, we investigated the sex determination mechanism in Oryzias javanicus, another species in the javanicus group. Linkage analysis of isolated sex-linked DNA markers showed that this species has a ZZ/ZW sex determination system. The sex-linkage map showed a conserved synteny to the linkage group 16 of O. latipes, suggesting that the sex chromosomes in O. javanicus are not homologous to those in any other Oryzias species. Fluorescence in-situ hybridization analysis confirmed that the ZW sex chromosomes of O. javanicus and O. hubbsi are not homologous, and showed that O. javanicus has the morphologically heteromorphic sex chromosomes, in which the W chromosome has 4,6-diamino-2-phenylindole-positive heterochromatin at the centromere. These findings suggest the repeated evolution of new sex chromosomes from autosomes in Oryzias, probably through the emergence of new sex-determining genes.

Patterns of Neutral Genetic Variation on Recombining Sex Chromosomes

“…Sex chromosomes in several families of plants (including campion, papaya, and poplar) evolved recently from hermaphroditic ancestors (Charlesworth and Guttman 1999;Ming and Moore 2007). A second way that new sex chromosomes originate is found in several groups of animals, where the sex-determining region has moved between linkage groups, recruiting autosomes into the role of sex chromosomes [e.g., in fishes such as sticklebacks (Peichel et al 2004), cichlids (Cnaani et al 2008), and medakas (Takehana et al 2008)]. Ancient recombining sex chromosome are also known, for example, in boid snakes (Ohno 1967) and ratite birds ( Janes et al 2009).…”

“…We then study 1 the consequences of the invasion of a neo-Y chromosome that converts an ancestral pair of autosomes into sex chromosomes. This model is motivated by the numerous species of plants (see Ming and Moore 2007;Bernasconi et al 2009) and animals (see Peichel et al 2004;Mank et al 2006;Cnaani et al 2008;McAllister et al 2008;Takehana et al 2008;Kitano et al 2009;Ser et al 2010) in which sex chromosomes have been recently derived from autosomes (see also van Doorn and Kirkpatrick 2007).…”

Molecular cloning and characterization of the repetitive DNA sequences that comprise the constitutive heterochromatin of the W chromosomes of medaka fishes

“…The same specimens were also used in our previous studies (Takehana et al 2007b(Takehana et al , 2008 (Takehana et al 2007b). Fosmid clones containing sex-linked expressed sequence tags (ESTs) of O. hubbsi were isolated by colony hybridization.…”

“…Morphologically homomorphic sex chromosomes have been observed in four species, Oryzias latipes, Oryzias curvinotus, Oryzias luzonensis, and Oryzias dancena (Kondo et al 2004;Matsuda et al 1998;Takehana et al 2007a;Tanaka et al 2007). On the other hand, Oryzias hubbsi and Oryzias javanicus have heteromorphic ZW sex chromosomes with different origins (Takehana et al 2007b(Takehana et al , 2008.…”

“…In O. javanicus, a heterochromatin block is located at the centromeric region on the W chromosome, but not on the Z chromosome (Takehana et al 2008). Differentiation of the sex chromosomes has progressed to a stage at which they have become cytogenetically distinct in these species.…”