Sex-Chromosome Homomorphy in Palearctic Tree Frogs Results from Both Turnovers and X–Y Recombination

Abstract

Contrasting with birds and mammals, poikilothermic vertebrates often have homomorphic sex chromosomes, possibly resulting from high rates of sex-chromosome turnovers and/or occasional X-Y recombination. Strong support for the latter mechanism was provided by four species of European tree frogs, which inherited from a common ancestor (∼ 5 Ma) the same pair of homomorphic sex chromosomes (linkage group 1, LG1), harboring the candidate sex-determining gene Dmrt1. Here, we test sex linkage of LG1 across six additional species of the Eurasian Hyla radiation with divergence times ranging from 6 to 40 Ma. LG1 turns out to be sex linked in six of nine resolved cases. Mapping the patterns of sex linkage to the Hyla phylogeny reveals several transitions in sex-determination systems within the last 10 My, including one switch in heterogamety. Phylogenetic trees of DNA sequences along LG1 are consistent with occasional X-Y recombination in all species where LG1 is sex linked. These patterns argue against one of the main potential causes for turnovers, namely the accumulation of deleterious mutations on nonrecombining chromosomes. Sibship analyses show that LG1 recombination is strongly reduced in males from most species investigated, including some in which it is autosomal. Intrinsically low male recombination might facilitate the evolution of male heterogamety, and the presence of important genes from the sex-determination cascade might predispose LG1 to become a sex chromosome.

Sex Determination and Sex Chromosomes in Amphibia

“…However, in the European tree frog group ( H. arborea, H. intermedia, and H. molleri ), it was observed that the sex chromosomes did not experience any turnover for a long time (5 MY), although they remain homomorphic in both sexes [Dufresnes et al, 2015]. In contrast, sex chromosomes turned over between geographic populations within a single species of the Japanese, European, and North American frog species mentioned earlier.…”

Phylogeography reveals an ancient cryptic radiation in East-Asian tree frogs (Hyla japonica group) and complex relationships between continental and island lineages

“…For nuclear data, we amplified and cloned a ~500 bp part α-Fibrinogen intron 1 (methods and cross-amplifying primers: [29]) in a representative subset of individuals ( H. japonica : n  = 36, H. immaculata : n  = 2; we included published sequences for H. suweonensis , see below). At least eight clones were sequenced per sample in order to capture the two alleles of heterozygotes.…”

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).…”