Homologous Sex Chromosomes in Three Deeply Divergent Anuran Species

Abstract

Comparative genomic studies are revealing that, in sharp contrast with the strong stability found in birds and mammals, sex determination mechanisms are surprisingly labile in cold-blooded vertebrates, with frequent transitions between different pairs of sex chromosomes. It was recently suggested that, in context of this high turnover, some chromosome pairs might be more likely than others to be co-opted as sex chromosomes. Empirical support, however, is still very limited. Here we show that sex-linked markers from three highly divergent groups of anurans map to Xenopus tropicalis scaffold 1, a large part of which is homologous to the avian sex chromosome. Accordingly, the bird sex determination gene DMRT1, known to play a key role in sex differentiation across many animal lineages, is sex linked in all three groups. Our data provide strong support for the idea that some chromosome pairs are more likely than others to be co-opted as sex chromosomes because they harbor key genes from the sex determination pathway. K E Y W O R D S :Amphibian, Bufo siculus, convergent evolution, conserved synteny, DMRT1, Hyla arborea, Rana temporaria, sex chromosome turnover.

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

“…If the X and Y chromosomes show significant genetic differentiation, heterozygosity will be higher in the male than the female for that chromosome only. By plotting male-informative markers against female-informative markers for each of 12 linkage groups, we show that linkage group 1 is an outlier with nearly three times as many male-information as female-informative markers, consistent with previous studies (Berset-Brändli et al, 2008;Brelsford et al, 2013) identifying this as the sex chromosome.…”

“…Marker order is conserved on the linkage group 1, with the exception of a small region. Brelsford et al (2013) Figure 1 Linkage group 1, the sex chromosome in H. arborea, contains nearly three times as many informative markers on the male-specific map compared with the female-specific map. The 11 autosomal linkage groups fall close to the dashed line, illustrating equal marker numbers between the sexes.…”

“…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). Males and females differ strongly in recombination rate (Berset-Brändli et al, 2008;Dufresnes et al, 2014a, b), but X-Y recombination is higher and X-Y differentiation is lower in Balkan glacial refugia than in recently colonized northwestern Europe (Dufresnes et al, 2014b).…”

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

“…LG 2 maps to Xt chromosome 1 (Brelsford et al, 2013(Brelsford et al, , 2016 that contains the candidate sex-determining genes Dmrt1 and Amh. The former is thought to determine sex in birds (Smith et al, 2009), whereas paralogs play this role in species of fish and frogs (Matsuda et al, 2002;Nanda et al, 2002;Yoshimoto et al, 2010).…”

Origin and genome evolution of polyploid green toads in Central Asia: evidence from microsatellite markers

“…Accordingly, the translocation events documented here in polyploid green toads contrast with the strong synteny that otherwise characterizes diploid species from this group, and amphibians in general (e.g., Miura, 1995;Sumida and Nishioka, 2000;Brelsford et al, 2013). It might also be meaningful that such translocations were limited not only to the paternal subgenomes, but also to the supposed sex-chromosome pairs.…”