High‐density linkage maps fail to detect any genetic component to sex determination in a Rana temporaria family

Abstract

Sex chromosome differentiation in Rana temporaria varies strikingly among populations or families: whereas some males display well-differentiated Y haplotypes at microsatellite markers on linkage group 2 (LG2), others are genetically undistinguishable from females. We analysed with RADseq markers one family from a Swiss lowland population with no differentiated sex chromosomes, and where sibship analyses had failed to detect any association between the phenotypic sex of progeny and parental haplotypes. Offspring were reared in a common tank in outdoor conditions and sexed at the froglet stage. We could map a total of 2177 SNPs (1123 in the mother, 1054 in the father), recovering in both adults 13 linkage groups (= chromosome pairs) that were strongly syntenic to Xenopus tropicalis despite > 200 My divergence. Sexes differed strikingly in the localization of crossovers, which were uniformly distributed in the female but limited to chromosome ends in the male. None of the 2177 markers showed significant association with offspring sex. Considering the very high power of our analysis, we conclude that sex determination was not genetic in this family; which factors determined sex remain to be investigated.

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

“…Hence, although we cannot exclude a polygenic system involving many genes with minor effects spread on multiple chromosomes, our present data might also suggest that the part of variance in phenotypic sex not accounted for by LG 2 in this population is not of genetic origin. This suggestion is corroborated by recent RADseq evidence for a complete absence of any genetic component to sex determination in a R. temporaria family from a Swiss lowland population (Brelsford et al, 2016). Altogether, these results provide additional support for the suggestion that 'sex races' in R. temporaria differ in the epigenetic Figure 1 Sex-specific recombination maps of 62 loci for Ammarnäs and Tvedöra.…”

“…Of these, only LG 2 shows some sex linkage in Tvedöra that is furthermore incomplete and variable among families (Rodrigues et al, 2015). Sibship analyses with sexed offspring have a very high power to detect genetic sex-determination systems, thanks to strong within-family linkage (Brelsford et al, 2016). Hence, although we cannot exclude a polygenic system involving many genes with minor effects spread on multiple chromosomes, our present data might also suggest that the part of variance in phenotypic sex not accounted for by LG 2 in this population is not of genetic origin.…”

“…The only noticeable difference concerned Bfg203 and Bfg238 (Figure 1b), known to belong to the same linkage group (Rodrigues et al, 2013), but not significantly associated in the present data set because of insufficient polymorphism (LOD score = 1.54). Correspondences between R. temporaria linkage groups and Xt chromosomes are provided in Figure 1 with the same nomenclature as in Brelsford et al (2016). Separate male and female maps were produced because of large sex differences in recombination rates (92.4 cM total map in males vs 1603.2 cM in females, including…”

“…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).…”

“…Following the second round of genotyping, population-and sex-specific maps were performed for LG 2 and LG 7 by including all 594 offspring from the 12 families. Correspondences between R. temporaria linkage groups and Xenopus tropicalis (Xt) chromosomes were established based on one Swiss R. temporaria family (C1) that was analyzed for both microsatellites (Rodrigues et al, 2013) and genotyping-by-sequencing reads (Brelsford et al, 2016). See Brelsford et al (2016) for details of the procedure of orthology search.…”