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

Terence J Robinson,Halina Cernohorska,Svatava Kubickova,Petra Musilova,Aurora Ruiz-Herrera,Miluse Vozdova

doi:10.1038/s41598-021-82859-0

Terence J Robinson, Halina Cernohorska + Show 4 more

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https://doi.org/10.1038/s41598-021-82859-0

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Abstract

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.

Highlights

Chromosome structural change has long been considered important in the evolution of post-zygotic reproductive isolation
We explore a novel hypothesis that suggests the expansion of heterochromatic blocks in the homogametic sex may, with certain conditions, contribute to post-zygotic isolation
A sister relationship was retrieved between R. campestris (RCA) and R. sharpei (RSH) with R. melanotis (RME) b asal[33,34] but more recently a basal RCA, with RSH and RME as sister taxa has been r eported[35]

Summary

Introduction

Chromosome structural change has long been considered important in the evolution of post-zygotic reproductive isolation. The chromosomal speciation t heory[1,2] referred to as the “Hybrid dysfunction model”[3], has been one of the most intriguing questions in biology for decades It relies on the development of chromosomal incompatibility between divergent lineages by invoking post-zygotic isolating mechanisms that lead to a point when a species eventually becomes two under a model of bifurcating evolutionary history. In a marked departure from the hybrid dysfunction model, chromosomal rearrangements could facilitate lineage divergence in the face of continuing gene flow and that reduction of recombination between chromosomes carrying different rearrangements was the sine qua non for speciation[6] This is perhaps best reasoned for instances involving inversions that permit the accumulation of incompatible alleles in regions protected from recombination, while genetic exchange in colinear segments of the rearranged chromosomes is freely permitted[8,9]. This contributes to a general framework for inversion-driven recombination suppression that may facilitate the accumulation of genetic incompatibilities, the so-called speciation g enes[15,16], and mutations that confer local adaptation that drive genetic divergence[17]

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