Chromosomal evolution in Raphicerus antelope suggests divergent X chromosomes may drive speciation through females, rather than males, contrary to Haldane's rule

Chromosome structural change has long been considered important in the evolution of post-zygotic reproductive isolation. The premise that karyotypic variation can serve as a possible barrier to gene flow is founded on the expectation that heterozygotes for structurally distinct chromosomal forms would be partially sterile (negatively heterotic) or show reduced recombination. We report the outcome of a detailed comparative molecular cytogenetic study of three antelope species, genus Raphicerus, that have undergone a rapid radiation. The species are largely conserved with respect to their euchromatic regions but the X chromosomes, in marked contrast, show distinct patterns of heterochromatic amplification and localization of repeats that have occurred independently in each lineage. We argue a novel hypothesis that postulates that the expansion of heterochromatic blocks in the homogametic sex can, with certain conditions, contribute to post-zygotic isolation. i.e., female hybrid incompatibility, the converse of Haldane's rule. This is based on the expectation that hybrids incur a selective disadvantage due to impaired meiosis resulting from the meiotic checkpoint network's surveillance of the asymmetric expansions of heterochromatic blocks in the homogametic sex. Asynapsis of these heterochromatic regions would result in meiotic silencing of unsynapsed chromatin and, if this persists, germline apoptosis and female infertility.

Automated summary

The study focuses on the role of chromosome structural changes in post-zygotic isolation in three antelope species of the genus Raphicerus. While the species are largely conserved in euchromatic regions, their X chromosomes exhibit distinct patterns of heterochromatic amplification and repeat localization. A new hypothesis is proposed suggesting that expansions of heterochromatic blocks in the homogametic sex may contribute to post-zygotic isolation, specifically female hybrid incompatibility.