No evidence that Y‐chromosome differentiation affects male fitness in a Swiss population of common frogs

Abstract

The canonical model of sex‐chromosome evolution assigns a key role to sexually antagonistic (SA) genes on the arrest of recombination and ensuing degeneration of Y chromosomes. This assumption cannot be tested in organisms with highly differentiated sex chromosomes, such as mammals or birds, owing to the lack of polymorphism. Fixation of SA alleles, furthermore, might be the consequence rather than the cause of recombination arrest. Here we focus on a population of common frogs (Rana temporaria) where XY males with genetically differentiated Y chromosomes (nonrecombinant Y haplotypes) coexist with both XY° males with proto‐Y chromosomes (only differentiated from X chromosomes in the immediate vicinity of the candidate sex‐determining locus Dmrt1) and XX males with undifferentiated sex chromosomes (genetically identical to XX females). Our study finds no effect of sex‐chromosome differentiation on male phenotype, mating success or fathering success. Our conclusions rejoin genomic studies that found no differences in gene expression between XY, XY° and XX males. Sexual dimorphism in common frogs might result more from the differential expression of autosomal genes than from sex‐linked SA genes. Among‐male variance in sex‐chromosome differentiation seems better explained by a polymorphism in the penetrance of alleles at the sex locus, resulting in variable levels of sex reversal (and thus of X‐Y recombination in XY females), independent of sex‐linked SA genes.

Novel genetic sex markers reveal high frequency of sex reversal in wild populations of the agile frog (Rana dalmatina) associated with anthropogenic land use

“…10 ‐6 to 10 –3 probability). Sex‐reversed individuals were found to be fertile in some ectothermic vertebrates (Devlin & Nagahama, 2002; Edmunds, McCarthy, & Ramsdell, 2000; Holleley et al., 2015), and in common frogs, XX males appear to be fertile and as successful in mating as XY males (Alho et al., 2010; Veltsos et al., 2019). If sex‐reversed individuals do reproduce in nature, the biased sex ratios of their progeny may lead to changes in the population sex ratio, sex chromosome frequencies and ultimately the sex‐determination system (Bókony et al., 2017; Quinn, Sarre, Ezaz, Marshall Graves, & a, & Georges, A., 2011; Wedekind, 2017).…”

Evolutionary and demographic consequences of temperature-induced masculinization under climate warming: the effects of mate choice

“…Here we found that the ZW/ZZ system may maintain healthier sex ratios for longer, and persist more than two times longer, than the XX/XY system if the sex-reversed males can reproduce like normal males and produce viable, fertile WW offspring that are resistant to masculinization. These conditions stand in various taxa [ 10 , 17 , 33 , 41 – 43 , 56 ], although our empirical knowledge on WW or masculinized individuals in nature is scarce. Moreover, most ectothermic vertebrates possess homomorphic sex chromosomes that show no signs of degeneration, suggesting that sex-reversed and WW individuals should be viable and fertile in the majority of these taxa [ 4 , 44 , 53 ].…”

Novel genetic sex markers reveal high frequency of sex reversal in wild populations of the agile frog (Rana dalmatina) associated with anthropogenic land use

“…0.0002 probability). Sex-reversed individuals were found to be fertile in some ectothermic vertebrates (Devlin & Nagahama, 2002;Edmunds, McCarthy, & Ramsdell, 2000;Holleley et al, 2015), and in common frogs XX males appear to be fertile and as successful in mating as XY males (Alho et al, 2010;Veltsos et al, 2019). If sex-reversed individuals do reproduce in nature, the biased sex ratios of their progeny may lead to changes in the population sex ratio, sex-chromosome frequencies, and ultimately the sex-determination system (Bókony et al, 2017;Quinn et al, 2011;Wedekind, 2017).…”