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

Abstract

The patterns of sex determination and sex differentiation have been shown to differ among geographic populations of common frogs. Notably, the association between phenotypic sex and linkage group 2 (LG 2 ) has been found to be perfect in a northern Swedish population, but weak and variable among families in a southern one. By analyzing these populations with markers from other linkage groups, we bring two new insights: (1) the variance in phenotypic sex not accounted for by LG 2 in the southern population could not be assigned to genetic factors on other linkage groups, suggesting an epigenetic component to sex determination; (2) a second linkage group (LG 7 ) was found to co-segregate with sex and LG 2 in the northern population. Given the very short timeframe since post-glacial colonization (in the order of 1000 generations) and its seemingly localized distribution, this neo-sex chromosome system might be the youngest one described so far. It does not result from a fusion, but more likely from a reciprocal translocation between the original Y chromosome (LG 2 ) and an autosome (LG 7 ), causing their cosegregation during male meiosis. By generating a strict linkage between several important genes from the sex-determination cascade (Dmrt1, Amh and Amhr2), this neo-sex chromosome possibly contributes to the 'differentiated sex race' syndrome (strictly genetic sex determination and early gonadal development) that characterizes this northern population.

A reciprocal translocation radically reshapes sex‐linked inheritance in the common frog

“…Our results provide compelling support for the earlier suggestion from a linkage study (Rodrigues et al, ) that there is a reciprocal translocation between the ancestral sex chromosome (Chromosome 1) and an autosome (Chromosome 2) in Ammarnäs Rana temporaria that is absent from two other populations, Kilpisjärvi and Tvedöra. Analysis of molecular variation shows that two pairs of sex chromosomes are cotransmitted even though they are not physically linked.…”

“…The third population we studied is in Tvedöra. Recall that a previous linkage mapping study found that only Chromosome 1 is sex‐linked here (Rodrigues et al, ). Consistent with those data, we detect elevated F ST and sex‐biased heterozygosity on Chromosome 1 (Figure and Table ), but not on any other chromosomes.…”

Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs

“…The same rationale applies when interpreting biological results from model organisms under a phylogeographic framework. Because of its abundance and broad ecological niche, its wide geographic and altitudinal distribution, as well as its high genomic and phenotypic plasticity, the common frog has been a model system to address fundamental topics in ecological, evolutionary, and conservation sciences, e.g., local adaptation (e.g., Muir, Biek, Thomas, & Mable, ), dispersal (e.g., Dolmen & Seland, ; Palo et al, ), epidemiology (e.g., Duffus, Garner, Nichols, Standridge, & Earl, ), resistance to abiotic stresses (e.g., Marquis, Miaud, & Lena, ), sex determination mechanisms (e.g., Rodrigues, Vuille, Brelsford, Merilä, & Perrin, ), or sex‐chromosome evolution (e.g., Rodrigues, Studer, Dufresnes, & Perrin, ). The present survey thus provides the necessary context to carry out more comprehensive studies on Iberian common frogs, where the overlooked diversity offers a promising playground for future research.…”

Sex-linked markers in the North American green frog (Rana clamitans) developed using DArTseq provide early insight into sex chromosome evolution

“…To date, all amphibians are known to have genotypic sex determination (GSD), although the mode of sex determination (i.e., XX-XY or ZZ-ZW) has repeatedly switched throughout amphibian evolutionary history [4, 5]. Some amphibian species even show substantial geographic variation in sex determining modes [2, 6–9]. Despite GSD, numerous laboratory experiments show that amphibian sexual differentiation is sensitive to environmental factors such as temperature [10, 11] or chemical exposure [12, 13].…”