Genetic Determinants Of Reproductive Isolation In Xenopus
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Haldane's rule states that in F1 interspecific hybrids the heterogametic sex (XY or ZW) suffers the most dysfunctional effects of hybridization. Frogs of the genus Xenopus have ZW sex determination yet hybrid males are completely sterile and hybrid females are fertile, a pattern exactly opposite of Haldane's rule. One of the most compelling hypotheses to explain this pattern is faster male evolution. The faster male evolution hypothesis suggests that hybrid male sterility is more common than hybrid female sterility because of faster divergence of male reproductive genes (due to sexual selection), or inherent sensitivity with the process of spermatogenesis. This hypothesis emphasizes the sex of the individual regardless of which sex is heterogametic and provides an explanation for examples that may go against Haldane's rule. Microarray expression data reveal numerically more male-biased genes but female-biased genes have a larger divergance in expression between species. Hybrid males (X. laevis x X. muelleri) have a dramatically lower abundance of motile sperm, increased numbers of undifferentiated sperm cells, and larger mature sperm cells compared to parental species. The gene expression pattern for hybrid males shows a striking asymmetric pattern in that relatively few genes are misexpressed between hybrids and the maternal species (X. laevis) whereas there are dramatically more genes misexpressed between hybrid males and the paternal species, X. muelleri. microRNA expression profiles of hybrid males provide several microRNAs that are misregulated in hybrids and these may play a role in the sterility pattern. Expression analysis of hybrid females reveals about 20 times more misexpression compared to hybrid males. A novel sex-reversal experiment shows that the sterility phenotype does not depend on genetic background but rather on physiological sex; hybrid males are sterile and hybrid females are fertile irrespective of their genetic background. Gene expression profiles match these adult phenotypes in that no genes were detected to be differentially expressed. Our results suggest that faster male evolution and in particular, the sensitive spermatogenesis component, is the most likely mechanism operating to produce patterns of reproductive isolation in Xenopus.