Geographic variation in sex‐chromosome differentiation in the common frog (Rana temporaria)

Abstract

In sharp contrast with birds and mammals, sex-determination systems in ectothermic vertebrates are often highly dynamic and sometimes multifactorial. Both environmental and genetic effects have been documented in common frogs (Rana temporaria). One genetic linkage group, mapping to the largest pair of chromosomes and harbouring the candidate sex-determining gene Dmrt1, associates with sex in several populations throughout Europe, but association varies both within and among populations. Here, we show that sex association at this linkage group differs among populations along a 1500-km transect across Sweden. Genetic differentiation between sexes is strongest (FST = 0.152) in a northern-boreal population, where male-specific alleles and heterozygote excesses (FIS = -0.418 in males, +0.025 in females) testify to a male-heterogametic system and lack of X-Y recombination. In the southernmost population (nemoral climate), in contrast, sexes share the same alleles at the same frequencies (FST = 0.007 between sexes), suggesting unrestricted recombination. Other populations show intermediate levels of sex differentiation, with males falling in two categories: some cluster with females, while others display male-specific Y haplotypes. This polymorphism may result from differences between populations in the patterns of X-Y recombination, co-option of an alternative sex-chromosome pair, or a mixed sex-determination system where maleness is controlled either by genes or by environment depending on populations or families. We propose approaches to test among these alternative models, to disentangle the effects of climate and phylogeography on the latitudinal trend, and to sort out how this polymorphism relates to the 'sexual races' described in common frogs in the 1930s.

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

“…At the extreme (E 3 ), all individuals are XX and sex determination becomes purely environmental (ESD). Adapted from [28].…”

“…The same 13 sex-linked markers used by Rodrigues et al [24,28] were amplified by polymerase chain reaction (PCR). Electronic supplementary material, table S1 provides information on primers (GenBank accession numbers, repeat motifs, primer sequences, range of allele sizes and references) and the two multiplex mixes used.…”

“…Rodrigues et al [28] recently found sex differentiation at LG 2 to differ among populations along a 1500 km latitudinal transect in Sweden, seemingly with a latitudinal trend: differentiation was strongest in the northern-boreal population of Ammarnäs (with high F ST between sexes, heterozygote excess in males and male-specific alleles and haplotypes) but null in the southernmost population of Tvedöra (nemoral climate). Other populations displayed intermediate patterns, with an apparently bimodal distribution of males: some clustered on their own, while others were genetically undistinguishable from females.…”

“…Intermediate populations would present a mix of ESD and GSD families, and belong to the semi-differentiated race. This hypothesis is formalized in figure 1 (adapted from [28]). There are, however, alternative interpretations to the empirical trend documented by Rodrigues et al [28].…”

“…This hypothesis is formalized in figure 1 (adapted from [28]). There are, however, alternative interpretations to the empirical trend documented by Rodrigues et al [28]. An obvious one is that all populations harbour the same GSD system, with the same master sex-determination gene on LG 2 , but differ in the patterns of recombination.…”