Selection in males purges the mutation load on female fitness
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 gen...
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| Published in | Evolution letters Vol. 5; no. 4; pp. 328 - 343 |
|---|---|
| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
John Wiley & Sons, Inc
01.08.2021
John Wiley and Sons Inc Oxford University Press |
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| Abstract | 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. |
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| AbstractList | Abstract
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. 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 F(1)s as well as inbred parental "selfs," and we estimated the 4 x 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. 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 F 1 s 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. Abstract 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. 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. 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 F 1 s 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. 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. |
| Author | Maurizio, Paul L. Berger, David Arnqvist, Göran Grieshop, Karl |
| AuthorAffiliation | 2 Department of Ecology and Evolutionary Biology University of Toronto Toronto ON M5S 3B2 Canada 3 Department of Molecular Biosciences The Wenner‐Gren Institute Stockholm University Stockholm SE‐10691 Sweden 4 Section of Genetic Medicine, Department of Medicine University of Chicago Chicago Illinois 60637 1 Animal Ecology, Department of Ecology and Genetics Uppsala University Uppsala SE‐75236 Sweden |
| AuthorAffiliation_xml | – name: 1 Animal Ecology, Department of Ecology and Genetics Uppsala University Uppsala SE‐75236 Sweden – name: 3 Department of Molecular Biosciences The Wenner‐Gren Institute Stockholm University Stockholm SE‐10691 Sweden – name: 2 Department of Ecology and Evolutionary Biology University of Toronto Toronto ON M5S 3B2 Canada – name: 4 Section of Genetic Medicine, Department of Medicine University of Chicago Chicago Illinois 60637 |
| Author_xml | – sequence: 1 givenname: Karl orcidid: 0000-0001-8925-5066 surname: Grieshop fullname: Grieshop, Karl email: karlgrieshop@gmail.com organization: Stockholm University – sequence: 2 givenname: Paul L. orcidid: 0000-0002-5859-6260 surname: Maurizio fullname: Maurizio, Paul L. organization: University of Chicago – sequence: 3 givenname: Göran orcidid: 0000-0002-3501-3376 surname: Arnqvist fullname: Arnqvist, Göran organization: Uppsala University – sequence: 4 givenname: David orcidid: 0000-0003-0196-6109 surname: Berger fullname: Berger, David organization: Uppsala University |
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| Snippet | Theory predicts that the ability of selection and recombination to purge mutation load is enhanced if selection against deleterious genetic variants operates... Abstract Theory predicts that the ability of selection and recombination to purge mutation load is enhanced if selection against deleterious genetic variants... Abstract Theory predicts that the ability of selection and recombination to purge mutation load is enhanced if selection against deleterious genetic variants... |
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| SubjectTerms | Alleles Animal reproduction Asexuality Bayesian analysis Breeding success Diallel cross Females fitness Gender differences Genetic diversity Genetic load Genomes good genes Heterosis Heterozygosity Inbreeding Letter Letters Males Markov chains Mutation mutation load Population Population genetics Recombination Reproductive fitness Sex differences Sexes Sexual reproduction sexual selection |
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| Title | Selection in males purges the mutation load on female fitness |
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