An Evolutionary Witness: the Frog <i>Rana rugosa</i> Underwent Change of Heterogametic Sex from XY Male to ZW Female

Abstract

There are two basic types of heterogamety for genetic sex determination in animals and plants: male heterogamety (XX/XY) and female heterogamety (ZZ/ZW). Although apparently in opposition, the two distinct types may in fact be interchangeable. For example, in amphibians it has been shown that the heterogametic sex was originally female and may have become male at some branching point in their phylogenetic evolution. In particular, there is evidence that the male heterogametic sex determination of the frog Rana rugosa returned to its previous female state during speciation that occurred when the distribution range of the frog expanded across Japan. This change is quite recent in the phylogenetic time scale. This paper presents a review of the sex chromosomes and sex determination in the frog R. rugosa, an evolutionary witness proving the viability of changing heterogametic sex, and introduces recent findings and on-going studies in the frog. Change of the heterogametic sex will also be discussed, relating data from frogs (Rana) and other animals to the replacement of a master sex-determining gene in the course of speciation.

The genetic contribution to sex determination and number of sex chromosomes vary among populations of common frogs (Rana temporaria)

“…Homomorphy may result from occasional X-Y recombination and/or frequent sex-chromosome turnovers (see, for example, Stöck et al, 2011;Dufresnes et al, 2015), two mechanisms possibly driven by incomplete genetic control over sex determination (Perrin, 2009;Grossen et al, 2011). Sexdetermination systems seem particularly labile in Ranidae, where sex chromosomes may differ between closely related species or even conspecific populations (Nishioka and Sumida, 1994;Miura, 2007).…”

Sex-chromosome differentiation and ‘sex races’ in the common frog ( Rana temporaria )

“…In amphibians, all species investigated so far present a genetic component to sex determination (as supported by co-segregation of sex with genetic markers; reviewed in [14]), sometimes with temperature effects, but cytogenetically differentiated sex chromosomes occur in less than 4% of species [14]. Particularly frequent transitions have been reported in ranid frogs, where different chromosome pairs have been co-opted for sex determination depending on species [15]. Temperature effects have been documented in a few species, mostly consisting of masculinization of XX individuals at high temperatures (e.g.…”

Sex determination by multiple sex chromosomes in Xenopus tropicalis

“…For three of these the different male sex-determining genes have been identified (11,12), providing clear evidence for nonhomologous turnover. Similarly, within the frog family Ranidae at least five different candidates for male sex-determiners on different chromosomes have evolved (13).…”

“…A well-known case is that of the Japanese wrinkled frogs, Rana rugosa, where separate XY and ZW populations exist. All four sex chromosomes are descendants of the same linkage group (13). They have diverged independently already carrying different sets of lethal genes.…”