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

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...

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Main Authors: Terence J. Robinson, Halina Cernohorska, Svatava Kubickova, Miluse Vozdova, Petra Musilova, Aurora Ruiz-Herrera
Format: Article
Language:English
Published: Nature Portfolio 2021-02-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-82859-0
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author Terence J. Robinson
Halina Cernohorska
Svatava Kubickova
Miluse Vozdova
Petra Musilova
Aurora Ruiz-Herrera
author_facet Terence J. Robinson
Halina Cernohorska
Svatava Kubickova
Miluse Vozdova
Petra Musilova
Aurora Ruiz-Herrera
author_sort Terence J. Robinson
collection DOAJ
description 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.
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spelling doaj.art-a4e413c620cb4789a375448c7b41fc682022-12-21T20:47:09ZengNature PortfolioScientific Reports2045-23222021-02-0111111110.1038/s41598-021-82859-0Chromosomal evolution in Raphicerus antelope suggests divergent X chromosomes may drive speciation through females, rather than males, contrary to Haldane's ruleTerence J. Robinson0Halina Cernohorska1Svatava Kubickova2Miluse Vozdova3Petra Musilova4Aurora Ruiz-Herrera5Department of Botany and Zoology, Stellenbosch UniversityVeterinary Research InstituteVeterinary Research InstituteVeterinary Research InstituteVeterinary Research InstituteDepartament de Biologia Cel·lular, Fisiologia i Immunologia, Universitat Autònoma de Barcelona (UAB)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.https://doi.org/10.1038/s41598-021-82859-0
spellingShingle Terence J. Robinson
Halina Cernohorska
Svatava Kubickova
Miluse Vozdova
Petra Musilova
Aurora Ruiz-Herrera
Chromosomal evolution in Raphicerus antelope suggests divergent X chromosomes may drive speciation through females, rather than males, contrary to Haldane's rule
Scientific Reports
title Chromosomal evolution in Raphicerus antelope suggests divergent X chromosomes may drive speciation through females, rather than males, contrary to Haldane's rule
title_full Chromosomal evolution in Raphicerus antelope suggests divergent X chromosomes may drive speciation through females, rather than males, contrary to Haldane's rule
title_fullStr Chromosomal evolution in Raphicerus antelope suggests divergent X chromosomes may drive speciation through females, rather than males, contrary to Haldane's rule
title_full_unstemmed Chromosomal evolution in Raphicerus antelope suggests divergent X chromosomes may drive speciation through females, rather than males, contrary to Haldane's rule
title_short Chromosomal evolution in Raphicerus antelope suggests divergent X chromosomes may drive speciation through females, rather than males, contrary to Haldane's rule
title_sort chromosomal evolution in raphicerus antelope suggests divergent x chromosomes may drive speciation through females rather than males contrary to haldane s rule
url https://doi.org/10.1038/s41598-021-82859-0
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