Sex-Chromosome Recombination in Common Frogs Brings Water to the Fountain-of-Youth

Abstract

According to the canonical model of sex-chromosome evolution, the degeneration of Y or W chromosomes (as observed in mammals and birds, respectively) results from an arrest of recombination in the heterogametic sex, driven by the fixation of sexually antagonistic mutations. However, sex chromosomes have remained homomorphic in many lineages of fishes, amphibians, and nonavian reptiles. According to the "fountain-of-youth" model, this homomorphy results from occasional events of sex reversal. If recombination arrest in males is controlled by maleness per se (and not by genotype), then Y chromosomes are expected to recombine in XY females, preventing their long-term degeneration. Here, we provide field support for the fountain-of-youth, by showing that sex-chromosome recombination in Rana temporaria only depends on phenotypic sex: naturally occurring XX males show the same restriction of recombination as XY males (average map length ∼2 cM), while XY females recombine as much as XX females (average map length ∼150 cM). Our results challenge several common assumptions regarding the evolution of sex chromosomes, including the role of sexually antagonistic genes as drivers of recombination arrest, and that of chromosomal inversions as underlying mechanisms.

Phylogeography, more than elevation, accounts for sex chromosome differentiation in Swiss populations of the common frog ( Rana temporaria )*

“…This shows not only that its mother was XY A , but also that the X and Y A did not recombine in this mother (in sharp contrast with the high recombination rate of the XY B mother documented by Rodrigues et al. (), and with the fact that the two Y B Y B individuals documented in the present study had recombined, proto‐sex chromosomes). Finally, selective causes might also be responsible for a drop in the effective population size of Y A , such as a selective sweep stemming from male‐beneficial alleles fixed on the Y chromosome.…”

Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs

“…The same rationale applies when interpreting biological results from model organisms under a phylogeographic framework. Because of its abundance and broad ecological niche, its wide geographic and altitudinal distribution, as well as its high genomic and phenotypic plasticity, the common frog has been a model system to address fundamental topics in ecological, evolutionary, and conservation sciences, e.g., local adaptation (e.g., Muir, Biek, Thomas, & Mable, ), dispersal (e.g., Dolmen & Seland, ; Palo et al, ), epidemiology (e.g., Duffus, Garner, Nichols, Standridge, & Earl, ), resistance to abiotic stresses (e.g., Marquis, Miaud, & Lena, ), sex determination mechanisms (e.g., Rodrigues, Vuille, Brelsford, Merilä, & Perrin, ), or sex‐chromosome evolution (e.g., Rodrigues, Studer, Dufresnes, & Perrin, ). The present survey thus provides the necessary context to carry out more comprehensive studies on Iberian common frogs, where the overlooked diversity offers a promising playground for future research.…”

A reciprocal translocation radically reshapes sex‐linked inheritance in the common frog

“…This effectively blocks recombination between the X and Y over most of their length. However, sex‐reversed XY females have been found in some populations, and they show female‐typical patterns of recombination (Rodrigues, Studer, Dufresnes, & Perrin, ). Recombination in sex‐reversed females could therefore result in very rare recombination events between the X and Y.…”