Sperm competition intensity shapes divergence in both sperm morphology and reproductive genes across murine rodents

It remains unclear how variation in the intensity of sperm competition shapes phenotypic and molecular evolution across clades. Mice and rats in the subfamily Murinae are a rapid radiation exhibiting incredible diversity in sperm morphology and production. We combined phenotypic and genomic data to perform phylogenetic comparisons of male reproductive traits and genes across 78 murine species. We identified several shifts towards smaller relative testes mass (RTM), presumably reflecting reduced sperm competition. Several sperm traits were associated with RTM, suggesting that mating system evolution selects for convergent suites of traits related to sperm competitive ability. We predicted that sperm competition would also drive more rapid molecular divergence in species with large testes. Contrary to this, we found that many spermatogenesis genes evolved more rapidly in species with smaller RTM due to relaxed purifying selection. While some reproductive genes evolved rapidly under recurrent positive selection, relaxed selection played a greater role in underlying rapid evolution in small testes species. Our work demonstrates that postcopulatory sexual selection can impose strong purifying selection shaping the evolution of male reproduction and that broad patterns of molecular evolution may help identify genes that contribute to male fertility.

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Publication Details

Journal
Evolution
Published
2024-10-09
DOI
https://doi.org/10.1093/evolut/qpae146
Citations
3
Primary Topic
Evolutionary Psychology and Human Behavior
Type
article
Field-Weighted Citation Impact
1.52

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article

Sperm competition intensity shapes divergence in both sperm morphology and reproductive genes across murine rodents

Jacob A. Esselstyn, Carl R. Hutter, Gregg W.C. Thomas, Colin M. Callahan et al.
3 citations
Evolution
Evolutionary Psychology and Human Behavior
1.52
article

Sperm competition intensity shapes divergence in both sperm morphology and reproductive genes across murine rodents

Jacob A. Esselstyn, Carl R. Hutter, Gregg W.C. Thomas, Colin M. Callahan, Jeffrey M. Good, Kevin C. Rowe, Emily Roycroft, W. G. Breed, Nathan L Clark, Anang S. Achmadi, Sebastian M. E. Mortimer, Emily E. K. Kopania
article en
3 citations

Abstract

It remains unclear how variation in the intensity of sperm competition shapes phenotypic and molecular evolution across clades. Mice and rats in the subfamily Murinae are a rapid radiation exhibiting incredible diversity in sperm morphology and production. We combined phenotypic and genomic data to perform phylogenetic comparisons of male reproductive traits and genes across 78 murine species. We identified several shifts towards smaller relative testes mass (RTM), presumably reflecting reduced sperm competition. Several sperm traits were associated with RTM, suggesting that mating system evolution selects for convergent suites of traits related to sperm competitive ability. We predicted that sperm competition would also drive more rapid molecular divergence in species with large testes. Contrary to this, we found that many spermatogenesis genes evolved more rapidly in species with smaller RTM due to relaxed purifying selection. While some reproductive genes evolved rapidly under recurrent positive selection, relaxed selection played a greater role in underlying rapid evolution in small testes species. Our work demonstrates that postcopulatory sexual selection can impose strong purifying selection shaping the evolution of male reproduction and that broad patterns of molecular evolution may help identify genes that contribute to male fertility.

EvolutionVol. 79(1)
Australian National University (AU), Louisiana State University (US), Houston Museum of Natural Science (US), Harvard University (US), The University of Melbourne (AU), University of Pittsburgh (US), Indonesian Institute of Sciences (ID), University of Utah (US), Museums Victoria (AU), Harvard University Press (US), Museum am Rothenbaum (DE), The University of Adelaide (AU), University of Montana (US)
National Science Foundation, M.J. Murdock Charitable Trust, University of Pittsburgh, Louisiana State University, University of Montana, Australian Government, University of Canberra, Muséum National d'Histoire Naturelle, National Institutes of Health, Center for Research Computing, University of Pittsburgh, National Human Genome Research Institute, National Institute of Child Health and Human Development
Openalex Percentile: Top 16%
Evolutionary Psychology and Human Behavior
1.52
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