Faster adaptation but slower divergence of X chromosomes under paternal genome elimination

Abstract Differences in transmission and ploidy between sex chromosomes and autosomes drive divergent evolutionary trajectories, with sex chromosomes generally evolving faster. Because sex-linked genes are transmitted less frequently, they are under less efficient selection. Conversely, exposure of...

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Main Authors: Robert B. Baird, Thomas J. Hitchcock, Jan Ševčík, Katy M. Monteith, Andy Gardner, Laura Ross, Andrew J. Mongue
Format: Article
Language:English
Published: Nature Portfolio 2025-06-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-60114-8
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author Robert B. Baird
Thomas J. Hitchcock
Jan Ševčík
Katy M. Monteith
Andy Gardner
Laura Ross
Andrew J. Mongue
author_facet Robert B. Baird
Thomas J. Hitchcock
Jan Ševčík
Katy M. Monteith
Andy Gardner
Laura Ross
Andrew J. Mongue
author_sort Robert B. Baird
collection DOAJ
description Abstract Differences in transmission and ploidy between sex chromosomes and autosomes drive divergent evolutionary trajectories, with sex chromosomes generally evolving faster. Because sex-linked genes are transmitted less frequently, they are under less efficient selection. Conversely, exposure of recessive mutations on haploid sex chromosomes creates more efficient selection. In most systems, these effects occur simultaneously and are confounded. The fly families Sciaridae (fungus gnats) and Cecidomyiidae (gall midges) have X0 sex determination, but males transmit only maternally inherited chromosomes. This phenomenon results in equal transmission of the X and autosomes, allowing the effect of haploid selection to be studied in isolation. We discover that, unlike well-studied systems, X chromosomes diverge more slowly than autosomes in these flies. Using population genomic and expression data, we show that despite the X evolving more adaptively, stronger purifying selection explains slower divergence. Our findings demonstrate the utility of non-Mendelian inheritance systems for understanding fundamental evolutionary processes.
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spelling doaj-art-b4e4105c0f4243f5be091a41235f83ea2025-08-20T02:07:41ZengNature PortfolioNature Communications2041-17232025-06-0116111210.1038/s41467-025-60114-8Faster adaptation but slower divergence of X chromosomes under paternal genome eliminationRobert B. Baird0Thomas J. Hitchcock1Jan Ševčík2Katy M. Monteith3Andy Gardner4Laura Ross5Andrew J. Mongue6Institute of Ecology and Evolution, University of EdinburghRIKEN Center for Interdisciplinary Theoretical and Mathematical Sciences (iTHEMS), RIKENDepartment of Biology and Ecology, Faculty of Science, University of OstravaInstitute of Ecology and Evolution, University of EdinburghSchool of Biology, University of St AndrewsInstitute of Ecology and Evolution, University of EdinburghDepartment of Entomology and Nematology, University of FloridaAbstract Differences in transmission and ploidy between sex chromosomes and autosomes drive divergent evolutionary trajectories, with sex chromosomes generally evolving faster. Because sex-linked genes are transmitted less frequently, they are under less efficient selection. Conversely, exposure of recessive mutations on haploid sex chromosomes creates more efficient selection. In most systems, these effects occur simultaneously and are confounded. The fly families Sciaridae (fungus gnats) and Cecidomyiidae (gall midges) have X0 sex determination, but males transmit only maternally inherited chromosomes. This phenomenon results in equal transmission of the X and autosomes, allowing the effect of haploid selection to be studied in isolation. We discover that, unlike well-studied systems, X chromosomes diverge more slowly than autosomes in these flies. Using population genomic and expression data, we show that despite the X evolving more adaptively, stronger purifying selection explains slower divergence. Our findings demonstrate the utility of non-Mendelian inheritance systems for understanding fundamental evolutionary processes.https://doi.org/10.1038/s41467-025-60114-8
spellingShingle Robert B. Baird
Thomas J. Hitchcock
Jan Ševčík
Katy M. Monteith
Andy Gardner
Laura Ross
Andrew J. Mongue
Faster adaptation but slower divergence of X chromosomes under paternal genome elimination
Nature Communications
title Faster adaptation but slower divergence of X chromosomes under paternal genome elimination
title_full Faster adaptation but slower divergence of X chromosomes under paternal genome elimination
title_fullStr Faster adaptation but slower divergence of X chromosomes under paternal genome elimination
title_full_unstemmed Faster adaptation but slower divergence of X chromosomes under paternal genome elimination
title_short Faster adaptation but slower divergence of X chromosomes under paternal genome elimination
title_sort faster adaptation but slower divergence of x chromosomes under paternal genome elimination
url https://doi.org/10.1038/s41467-025-60114-8
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