Extreme heterochiasmy and nascent sex chromosomes in European tree frogs

Abstract

We investigated sex-specific recombination rates in Hyla arborea, a species with nascent sex chromosomes and male heterogamety. Twenty microsatellites were clustered into six linkage groups, all showing suppressed or very low recombination in males. Seven markers were sex linked, none of them showing any sign of recombination in males (rZ0.00 versus 0.43 on average in females). This opposes classical models of sex chromosome evolution, which envision an initially small differential segment that progressively expands as structural changes accumulate on the Y chromosome. For autosomes, maps were more than 14 times longer in females than in males, which seems the highest ratio documented so far in vertebrates. These results support the pleiotropic model of Haldane and Huxley, according to which recombination is reduced in the heterogametic sex by general modifiers that affect recombination on the whole genome.

High-density sex-specific linkage maps of a European tree frog (Hyla arborea) identify the sex chromosome without information on offspring sex

“…If the X and Y chromosomes show significant genetic differentiation, heterozygosity will be higher in the male than the female for that chromosome only. By plotting male-informative markers against female-informative markers for each of 12 linkage groups, we show that linkage group 1 is an outlier with nearly three times as many male-information as female-informative markers, consistent with previous studies (Berset-Brändli et al, 2008;Brelsford et al, 2013) identifying this as the sex chromosome.…”

“…Most frogs with known systems of sex determination are male heterogametic. In Hyla, Bufo and Rana, recombination is reduced in males (Berset-Brändli et al, 2008;Stöck et al, 2013;Rodrigues et al, 2013), consistent with the Haldane-Huxley rule. However, we still do not know whether one of these patterns is the cause of the other.…”

“…The sex chromosome is largely homologous to chromosome 1 in Xenopus tropicalis, and contains the candidate sex determination gene Dmrt1 (Brelsford et al, 2013). Males and females differ strongly in recombination rate (Berset-Brändli et al, 2008;Dufresnes et al, 2014a, b), but X-Y recombination is higher and X-Y differentiation is lower in Balkan glacial refugia than in recently colonized northwestern Europe (Dufresnes et al, 2014b). In this study, we validate our method for identifying sex chromosomes by showing that only linkage group 1, homologous to X. tropicalis chromosome 1, has a strongly different number of markers between paternal and maternal linkage maps.…”

The Birds and the Bees and the Flowers and the Trees: Lessons from Genetic Mapping of Sex Determination in Plants and Animals

“…In some species, recombination is absent, or nearly absent, throughout the genome in the heterogametic sex (Huxley 1928;Berset-Brändli et al 2008). More often, recombination is suppressed in one sex in limited genomic regions (Naruse et al 2000;Chen et al 2007b;Yin et al 2008), including the familiar situations in organisms such as mammals with no crossing over across most of the X and Y chromosomes in males.…”

Origin and genome evolution of polyploid green toads in Central Asia: evidence from microsatellite markers

“…Sex, but not ploidy level, affects recombination rates Our data also provided indications that sex had a major impact on recombination rates: all linkage groups and species investigated displayed strongly female-biased recombination. Heterochiasmy (i.e., sex differences in recombination rates) seems widespread throughout animals, with a trend for strongly reduced male recombination across amphibians (e.g., Sumida and Nishioka, 2000;Berset-Brändli et al, 2008;Rodrigues et al, 2013) and fishes (Moens et al, 2004). Heterochiasmy might have evolved as a pleiotropic consequence of selection on sex chromosomes (Haldane, 1922;Huxley, 1928;Nei, 1969): the easiest or quickest way to reduce sex-chromosome recombination in the heterogametic sex might be to reduce recombination over the whole genome in this sex.…”