Temperature-Dependent Sex Determination in Hd-rR Medaka <i>Oryzias latipes:</i> Gender Sensitivity, Thermal Threshold, Critical Period, and <i>DMRT1</i> Expression Profile

Abstract

The developmental time and thermal threshold for temperature-dependent sex determination (TSD), gender differences in temperature sensitivity, the fertility of thermally sex reversed fish, and the effect of temperature on the expression of two major sex determination/differentiation genes (DMY/DMRT1bY and DMRT1) were examined in the Hd-rR strain of medaka, Oryzias latipes. Fertilized eggs were exposed from either shortly after fertilization (8–16 cells; embryonic stages 5–6) or from middle embryogenesis (heart development stage; stage 36) until hatching to temperatures ranging from 17°C to 34°C. Secondary sexual characteristics, gonadal histology, progeny testing, sex-linked body coloration and gene expression were used to determine phenotypic and genotypic sex. Sex determination was unaffected by low or high temperatures in genotypic (XY) males. In contrast, genotypic (XX) females treated from stages 5–6 showed increasing rates of sex reversal into phenotypic males at temperatures above 27°C up to 100% at 34°C. Thermal manipulation of sex was ineffective after stage 36, indicating that gonadal fate in medaka is determined considerably earlier than histological differentiation (stage 39). High temperature induced DMRT1 expression in genotypic females, which was observed already from stage 36. Sex-reversed males had histologically normal testes, were capable of sexual courtship and, with the exception of fish from 34°C, sired viable progeny when mating with fertile females. These results clarify the pattern of TSD in medaka and provide important clues to understand the mechanism of sex determination in this species. They also suggest that a brief exposure to high temperature early in life could impair the fertility of medaka as adults.

Dmrt1 mutation causes a male-to-female sex reversal after the sex determination by Dmy in the medaka

“…Scale bar0100 μm Steroid hormone or high temperature treatments have induced complete sex reversals. These facts have indicated that an XY bipotential gonad can develop into not only a testis but also a complete ovary in medaka (Yamamoto 1958;Sato et al 2005;Hattori et al 2007). Although our XY Dmrt1 mutant finally developed into a female, in the early stage before 5 days after hatching, the germ cell number was similar to that of wild-type XY gonads, and the expression patterns of the testis-specific genes were also more similar to that of the wild-type XY gonads than the XX gonads.…”

“…Dmrt1 appears to be a key gene in normal testicular development because in steroid hormone treatment-induced XX sexreversed testes, Dmrt1 is expressed in the Sertoli cell lineage, similar to the expression of Dmy in XY testes (Kobayashi et al 2004). High temperatures have also induced Dmrt1 expression in XX embryos (Hattori et al 2007). However, it remains unclear whether Dmrt1 is necessary for testicular development in medaka.…”

“…In the case of medaka, high-temperature treatment or steroid hormone treatment can induce XX sex reversal (Yamamoto 1958;Sato et al 2005;Hattori et al 2007). This means that a gonad lacking Dmy can develop into testis and that Dmy is not necessary for testicular development.…”

Fishes of southern South America: a story driven by temperature

“…It must be noted that these species show a different degree of temperaturedependent sex determination (TSD; Strüssmann et al 1997b), which supposedly confers an adaptive advantage to some species in a trade-off between intraspecific competition and genetic diversity (Hattori et al 2007). Temperature-dependent sex determination could represent a differential constraint for both species, within the biogeographical range established by thermal tolerance and body size during the first winter.…”

The Y Chromosome That Lost the Male-Determining Function Behaves as an X Chromosome in the Medaka Fish,Oryzias latipes

“…In fact, the Y chromosome-specific region is 260 kb in length (Kondo et al 2006). In addition, the genotypic sex can easily be reverted by sex hormone or high-temperature treatments (Kobayashi and Iwamatsu 2005;Sato et al 2005;Iwamatsu et al 2006;Hattori et al 2007). These results indicate that the medaka sex chromosomes are quite undifferentiated and suggest that sex determination in the medaka is at an early stage of evolution and has not reached a similar stability to that in other vertebrates like birds and mammals.…”