Selection in males purges the mutation load on female fitness

Grieshop, Karl ORCID:, Maurizio, Paul L., Arnqvist, Göran and Berger, David (2021) Selection in males purges the mutation load on female fitness. Evolution Letters, 5 (4). pp. 328-343. ISSN 2056-3744

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Theory predicts that the ability of selection and recombination to purge mutation load is enhanced if selection against deleterious genetic variants operates more strongly in males than females. However, direct empirical support for this tenet is limited, in part because traditional quantitative genetic approaches allow dominance and intermediate-frequency polymorphisms to obscure the effects of the many rare and partially recessive deleterious alleles that make up the main part of a population's mutation load. Here, we exposed the partially recessive genetic load of a population of Callosobruchus maculatus seed beetles via successive generations of inbreeding, and quantified its effects by measuring heterosis—the increase in fitness experienced when masking the effects of deleterious alleles by heterozygosity—in a fully factorial sex-specific diallel cross among 16 inbred strains. Competitive lifetime reproductive success (i.e., fitness) was measured in male and female outcrossed F1s as well as inbred parental “selfs,” and we estimated the 4 × 4 male-female inbred-outbred genetic covariance matrix for fitness using Bayesian Markov chain Monte Carlo simulations of a custom-made general linear mixed effects model. We found that heterosis estimated independently in males and females was highly genetically correlated among strains, and that heterosis was strongly negatively genetically correlated to outbred male, but not female, fitness. This suggests that genetic variation for fitness in males, but not in females, reflects the amount of (partially) recessive deleterious alleles segregating at mutation-selection balance in this population. The population's mutation load therefore has greater potential to be purged via selection in males. These findings contribute to our understanding of the prevalence of sexual reproduction in nature and the maintenance of genetic variation in fitness-related traits.

Item Type: Article
Additional Information: Funding Information: We thank A. F. Agrawal (and lab members) and J. M. Kreiner for comments on earlier drafts of the manuscript; S. M. Drobniak and J. Radwan for very helpful conversations; R. Augusto, M. Fei, and J. Liljestrand Rönn for invaluable laboratory technical support; B. Stenerlöw for access to the irradiation facilities; and I. Glitho for the collection of beetles. We also thank Jon Slate (Editor in Chief), Andy Gardner (Associate Editor), Tim Connallon (referee) and an anonymous referee for very helpful suggestions. This research was supported by the Swedish Research Council (2018‐06775 to KG, 621‐2010‐5266 to GA, and 2015‐05223 to DB), the European Research Council (GENCON AdG‐294333 to GA), the National Institutes of Health (F32AG064883 to PLM), the University of Toronto's Faculty of Arts and Science (Postdoctoral Fellowship to KG), Stiftelsen för Zoologisk Forskning (to KG), and a Liljewalch's Resestipendier (to KG). Publisher Copyright: © 2021 The Authors. Evolution Letters published by Wiley Periodicals LLC on behalf of Society for the Study of Evolution (SSE) and European Society for Evolutionary Biology (ESEB).
Uncontrolled Keywords: diallel cross,fitness,good genes,heterosis,mutation load,sexual selection,ecology, evolution, behavior and systematics,genetics ,/dk/atira/pure/subjectarea/asjc/1100/1105
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 07 Oct 2023 01:24
Last Modified: 07 Oct 2023 01:24
DOI: 10.1002/evl3.239


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