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

Abstract

Sex-chromosome differentiation was recently shown to vary among common frog populations in Fennoscandia, suggesting a trend of increased differentiation with latitude. By rearing families from two contrasted populations (respectively, from northern and southern Sweden), we show this disparity to stem from differences in sex-determination mechanisms rather than in XY-recombination patterns. Offspring from the northern population display equal sex ratios at metamorphosis, with phenotypic sexes that correlate strongly with paternal LG 2 haplotypes (the sex chromosome); accordingly, Y haplotypes are markedly differentiated, with male-specific alleles and depressed diversity testifying to their smaller effective population size. In the southern population, by contrast, a majority of juveniles present ovaries at metamorphosis; only later in development do sex ratios return to equilibrium. Even at these later stages, phenotypic sexes correlate only mildly with paternal LG 2 haplotypes; accordingly, there are no recognizable Y haplotypes. These distinct patterns of gonadal development fit the concept of 'sex races' proposed in the 1930s, with our two populations assigned to the 'differentiated' and 'semi-differentiated' races, respectively. Our results support the suggestion that 'sex races' differ in the genetic versus epigenetic components of sex determination. Analysing populations from the 'undifferentiated race' with high-density genetic maps should help to further test this hypothesis.

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

“…Consequently, paternal LG 2 and LG 7 haplotypes present identical patterns of inheritance. Association with offspring phenotypic sex was thus identical to that documented for LG 2 by Rodrigues et al (2015), that is, perfect at both metamorph and froglet stages (ϕ 2 = 1) in all families except A 1 and A 5 , where association scores in metamorphs were 0.88 and 0.90 respectively, because of a sex-reversed XY female in each (that is, two metamorphs that presented ovaries despite having inherited their father's Y haplotype).…”

“…Based on this latter result, all families were genotyped for 13 LG 7 markers, and data combined with the 13 LG 2 markers genotyped by Rodrigues et al (2015) for further analyses. Recombination maps (Figure 1a) show that LG 2 and LG 7 gather into a single linkage group in all Ammarnäs families, with no male recombination (male map = 0.0 cM).…”

“…The present study uses samples collected during spring 2013 from two Swedish populations (Table 1), already analyzed for 13 LG 2 markers by Rodrigues et al (2015). Eleven pairs were captured in amplexus from 16 to 20 April in the southern locality of Tvedöra (55°42'0.85'' N, 13°25'50.91'' E), and 20 pairs from 17 to 20 May in the northern-boreal population of Ammarnäs (65°58'12.60'' N,16°12'43.80'' E).…”

“…Following the second round of genotyping, sex differentiation at LG 7 was investigated in all adults from these two populations (2013 sampling) via within-(F IS ) and between-sexes (F ST ) fixation indices (FSTAT v. 2.9.4;Goudet, 1995). LG 7 sex haplotypes were then phased in Ammarnäs as described by Rodrigues et al (2015), and analyzed for expected heterozygosity H S and differentiation F ST (FSTAT v. 2.9.4;Goudet, 1995). Genetic diversity θ was calculated from H S as θ = ((1-H S ) − 2 − 1)/2, assuming a stepwise mutation model (Kimura and Ohta, 1975).…”

“…To distinguish among these hypotheses, Rodrigues et al (2015) analyzed with the same LG 2 markers six families from each of the two most contrasted populations (Ammarnäs and Tvedöra) for patterns of recombination and association with offspring phenotypic sex. Families from these two populations displayed very similar rates of recombination (very high in females and close to zero in males), hence discarding hypothesis (1).…”