Mother’s Curse alleles represent a significant source of potential male fitness defects. The maternal inheritance of mutations with the pattern of sex-specific fitness effects, s♀>0>s♂, allows Mother’s Curse alleles to spread through a population even though they reduce male fitness. Although the mitochondrial genomes of animals contain only a handful of protein-coding genes, mutations in many of these genes have been shown to have a direct effect on male fertility. The evolutionary process of nuclear compensation is hypothesized to counteract the male-limited mitochondrial defects that spread via Mother’s Curse. Here we use population genetic models to investigate the evolution of compensatory autosomal nuclear mutations that act to restore the loss of fitness caused by mitochondrial mutation pressures. We derive the rate of male fitness deterioration by Mother’s Curse and the rate of restoration by nuclear compensatory evolution. We find that the rate of nuclear gene compensation is many times slower than that of its deterioration by cytoplasmic mutation pressure, resulting in a significant lag in the recovery of male fitness. Thus, the numbers of nuclear genes capable of restoring male mitochondrial fitness defects must be large in order to sustain male fitness in the face of mutation pressures.
- Award ID(s):
- 1736249
- NSF-PAR ID:
- 10179062
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 59
- Issue:
- 4
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- 890 to 899
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Maternal inheritance of mitochondrial DNA (mtDNA) renders selection blind to mutations whose effects are limited to males. Evolutionary theory predicts this will lead to the accumulation of a male-specific genetic load within the mitochondrial genomes of populations; that is, a pool of mutations that negatively affects male, but not female, fitness components. This principle has been termed the Mother’s Curse hypothesis. While the hypothesis has received some empirical support, its relevance to natural populations of metazoans remains unclear, and these ambiguities are compounded by the lack of a clear predictive framework for studies attempting to test Mother’s Curse. Here, we seek to redress this by outlining the core predictions of the hypothesis, as well as the key features of the experimental designs that are required to enable direct testing of the predictions. Our goal is to provide a roadmap for future research seeking to elucidate the evolutionary significance of the Mother’s Curse hypothesis.
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Abstract Maternal inheritance of mitochondria creates a sex‐specific selective sieve through which mitochondrial mutations harmful to males but not females accumulate and contribute to sexual differences in longevity and disease susceptibility. Because eggs and sperm are under disruptive selection, sperm are predicted to be particularly vulnerable to the genetic load generated by maternal inheritance, yet evidence for mitochondrial involvement in male fertility is limited and controversial. Here, we exploit the coexistence of two divergent mitochondrial haplogroups (A and B2) in a Neotropical arachnid to investigate the role of mitochondria in sperm competition. DNA profiling demonstrated that B2‐carrying males sired more than three times as many offspring in sperm competition experiments than A males, and this B2 competitive advantage cannot be explained by female mitochondrial haplogroup or male nuclear genetic background. RNA‐Seq of testicular tissues implicates differential expression of mitochondrial oxidative phosphorylation (OXPHOS) genes in the B2 competitive advantage, including a 22‐fold upregulation of
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/icb/icz091
