Mitochondrial genetic effects on reproductive success: signatures of positive intrasexual, but negative intersexual pleiotropy

Theory predicts that maternal inheritance of mitochondria will facilitate the accumulation of mtDNA mutations that are male biased, or even sexually antagonistic, in effect. While there are many reported cases of mtDNA mutations conferring cytoplasmic male sterility in plants, historically it was as...

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Bibliographic Details
Published in:Proceedings of the Royal Society. B, Biological sciences Biological sciences, 2018-05, Vol.285 (1879), p.20180187-20180187
Main Authors: Camus, M. Florencia, Dowling, Damian K.
Format: Article
Language:English
Subjects:
Animal reproduction
Animals
Breeding success
Correlation
Cytoplasmic male sterility
Drosophila melanogaster - genetics
Drosophila melanogaster - physiology
Evolution
Female
Fitness
Fruit flies
Genes, Mitochondrial - genetics
Genetic diversity
Genetic effects
Genetic Pleiotropy
Genetic Variation
Genomes
Haplotypes
Historical account
Life History
Male
Male sterility
Males
Maternal Inheritance
Mitochondria
Mitochondrial DNA
Mutation
Phenotypic variations
Pleiotropy
Reproduction
Reproductive fitness
Sex
Sexual Antagonism
Sexual Conflict
Success
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Summary:Theory predicts that maternal inheritance of mitochondria will facilitate the accumulation of mtDNA mutations that are male biased, or even sexually antagonistic, in effect. While there are many reported cases of mtDNA mutations conferring cytoplasmic male sterility in plants, historically it was assumed such mutations would not persist in the streamlined mitochondrial genomes of bilaterian metazoans. Intriguingly, recent cases of mitochondrial variants exerting male biases in effect have come to light in bilaterians. These cases aside, it remains unknown whether the mitochondrial genetic variation affecting phenotypic expression, and in particular reproductive performance, in bilaterians is routinely composed of sex-biased or sex-specific variation. If selection consistently favours mtDNA variants that augment female fitness, but at cost to males, this could shape patterns of pleiotropy and lead to negative intersexual correlations across mtDNA haplotypes. Here, we show that genetic variation across naturally occurring mitochondrial haplotypes affects components of reproductive success in both sexes, in the fruit fly Drosophila melanogaster. We find that intrasexual correlations across mitochondrial haplotypes, for components of reproductive success, are generally positive, while intersexual correlations are negative. These results accord with theoretical predictions, suggesting that maternal inheritance has led to the fixation of numerous mutations of sexually antagonistic effect.
ISSN:0962-8452
1471-2954
DOI:10.1098/rspb.2018.0187