Ever-Young Sex Chromosomes in European Tree Frogs

Abstract

Non-recombining sex chromosomes are expected to undergo evolutionary decay, ending up genetically degenerated, as has happened in birds and mammals. Why are then sex chromosomes so often homomorphic in cold-blooded vertebrates? One possible explanation is a high rate of turnover events, replacing master sex-determining genes by new ones on other chromosomes. An alternative is that X-Y similarity is maintained by occasional recombination events, occurring in sex-reversed XY females. Based on mitochondrial and nuclear gene sequences, we estimated the divergence times between European tree frogs (Hyla arborea, H. intermedia, and H. molleri) to the upper Miocene, about 5.4–7.1 million years ago. Sibship analyses of microsatellite polymorphisms revealed that all three species have the same pair of sex chromosomes, with complete absence of X-Y recombination in males. Despite this, sequences of sex-linked loci show no divergence between the X and Y chromosomes. In the phylogeny, the X and Y alleles cluster according to species, not in groups of gametologs. We conclude that sex-chromosome homomorphy in these tree frogs does not result from a recent turnover but is maintained over evolutionary timescales by occasional X-Y recombination. Seemingly young sex chromosomes may thus carry old-established sex-determining genes, a result at odds with the view that sex chromosomes necessarily decay until they are replaced. This raises intriguing perspectives regarding the evolutionary dynamics of sexually antagonistic genes and the mechanisms that control X-Y recombination.

Molecular basis and genetic improvement of economically important traits in aquaculture animals

“…Of course, sex determination mechanisms are also intricate in fishes, because fishes, like other aquatic animals of amphibians and reptiles, include male or female heterogametic genetic sex determination with or without strongly differentiated sex chromosomes [88,89]. A recent report indicates that sex-chromosome homomorphy in European tree frogs does not result from a recent turnover but is maintained over evolutionary timescales by occasional X-Y recombination, implicating that seemingly ever-young sex chromosomes may thus carry old-established sex-determining genes [90]. Moreover, B chromosomes in addition to standard chromosomes are also found to have a functional effect on sex determination in one cichlid species (Lithochromis rubripinnis) from Lake Victoria [91], which implies that a portion of sex chromosomes has been derived from B chromosomes.…”

High-density sex-specific linkage maps of a European tree frog (Hyla arborea) identify the sex chromosome without information on offspring sex

“…Previous work on this species has shown that its sex determination system is at least 5 million years old, but that occasional X-Y recombination prevents degeneration of the Y chromosome (Stöck et al, 2011). The sex chromosome is largely homologous to chromosome 1 in Xenopus tropicalis, and contains the candidate sex determination gene Dmrt1 (Brelsford et al, 2013).…”

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).…”