Abstract
Reproductive isolation is crucial for the process of speciation to progress. Sex chromosomes have been assigned a key role in driving reproductive isolation but empirical evidence from natural population processes has been restricted to organisms with degenerated sex chromosomes such as mammals and birds. Here we report restricted introgression at sex-linked compared to autosomal markers in a hybrid zone between two incipient species of European tree frog, Hyla arborea and H. orientalis, whose homologous X and Y sex chromosomes are undifferentiated. This large X-effect cannot result from the dominance or faster-X aspects of Haldane’s rule, which are specific to degenerated sex chromosomes, but rather supports a role for faster-heterogametic-sex or faster-male evolutionary processes. Our data suggest a prominent contribution of undifferentiated sex chromosomes to speciation.
Highlights
Reproductive isolation is crucial for the process of speciation to progress, and biologists have started to learn about the genomics and ecology of evolving reproductive barriers[1,2]
With few exceptions[43], these studies reported restricted introgression at sex chromosomes, advocating their prominent role in driving speciation. It remains empirically unexplored whether this holds for species with homomorphic sex chromosomes, where dominance and faster-X effects are not at play, and whether this translates into differential introgression patterns in natural hybrid zones. We address this open question in the European tree frogs Hyla arborea and H. orientalis, which feature undifferentiated sex chromosomes
Ancestry coefficients correspond to estimates of hybrid index (HI)
Summary
Reproductive isolation is crucial for the process of speciation to progress, and biologists have started to learn about the genomics and ecology of evolving reproductive barriers[1,2]. The dominance hypothesis suggests that, if alleles responsible for Dobzhanski-Muller incompatibilities are partially recessive, they will have a greater impact when located on hemizygous X (or Z) chromosomes, being exposed in the heterogametic sex[17,18] Such effects can accelerate the rate of genetic changes on X- or Z-linked genomic regions (i.e. the faster-X theory)[3], which can contribute to Haldane’s and Coyne’s empirical patterns. Or in complement, the faster-male theory hypothesizes that stronger sexual selection on males would drive faster evolution of male-expressed genes[19] This would result in more male than female incompatibilities in hybrids[20,21], and can explain Haldane’s rule in XY systems. Estimating the contribution of sex-linked genes to postzygotic isolation in taxa with different sex-determining systems and levels of sex-chromosome degeneracy can increase our understanding of the underlying mechanisms
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