Sex reversal and primary sex ratios in the common frog (Rana temporaria)

Abstract

Sex reversal has been suggested to have profound implications for the evolution of sex chromosomes and population dynamics in ectotherms. Occasional sex reversal of genetic males has been hypothesized to prevent the evolutionary decay of nonrecombining Y chromosomes caused by the accumulation of deleterious mutations. At the same time, sex reversals can have a negative effect on population growth rate. Here, we studied phenotypic and genotypic sex in the common frog (Rana temporaria) in a subarctic environment, where strongly female-biased sex ratios have raised the possibility of frequent sex reversals. We developed two novel sex-linked microsatellite markers for the species and used them with a third, existing marker and a Bayesian modelling approach to study the occurrence of sex reversal and to determine primary sex ratios in egg clutches. Our results show that a significant proportion (0.09, 95% credible interval: 0.04-0.18) of adults that were genetically female expressed the male phenotype, but there was no evidence of sex reversal of genetic males that is required for counteracting the degeneration of Y chromosome. The primary sex ratios were mostly equal, but three clutches consisted only of genetic females and three others had a significant female bias. Reproduction of the sex-reversed genetic females appears to create all-female clutches potentially skewing the population level adult sex-ratio consistent with field observations. However, based on a simulation model, such a bias is expected to be small and transient and thus does not fully explain the observed female-bias in the field.

First-generation linkage map for the common frog Rana temporaria reveals sex-linkage group

“…An interesting feature of this map is that six markers known to be linked to phenotypic sex in wild individuals in Northern Finland and Sweden (that is, Bfg201, Bf266 and RtSBO3 [Matsuba et al, 2008;Alho et al, 2010] and Bfg053, Bfg093 and Bfg191 [Matsuba, unpublished]) mapped to the same linkage group. Marker Bfg028, which was sex-linked in a population from Southern Sweden (Tvedöra 55142 0 N, 13126 0 E; Matsuba, unpublished), mapped to a different linkage group (that is, LG7).…”

“…In this species, males are the heterogametic sex (XX/XY), albeit heteromorphism in sex chromosomes is very weak (Popov and Dimitrov, 1999). Recent studies suggest that males tend to have a smaller genome size than females (Matsuba and Merilä, 2006), and three microsatellite loci with varying degree of linkage to sex in Fennoscandian common frog populations have been found (Matsuba et al, 2008;Alho et al, 2010). Genome-wide linkage studies would allow measurement of potential differences in recombination rates between the sexes, as well identification of the number and location of sex-determining loci.…”

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

“…In common frogs (Rana temporaria), sex associates with linkage group 2 (LG 2 ), as first discovered by sex differences in allele frequencies at microsatellite markers (Matsuba et al, 2008;Alho et al, 2010;Cano et al, 2011;Rodrigues et al, 2013). However, the strength of association varies within and among populations (Matsuba et al, 2008;Rodrigues et al, 2013), seemingly with a cline in sexchromosome differentiation along a latitudinal transect in Sweden (Rodrigues et al, 2014).…”

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

“…Evidence for genetic effects has been gathered from populations of Fennoscandia and Switzerland, where several markers display a clear association with sex, consistent with male heterogamety. However, the strength of the association varies between populations and families [22][23][24]. Those markers fall into linkage group 2 (LG 2 , which also includes the LG 15 of Cano et al [25]).…”