Can paternal leakage maintain sexually antagonistic polymorphism in the cytoplasm?
B Kuijper1, N Lane, A Pomiankowski
1CoMPLEX, Centre for Mathematics and Physics in the Life Sciences and Experimental Biology, University College London, London, UK; Department of Genetics, Evolution and Environment, University College London, London, UK.
Abstract:
A growing number of studies in multicellular organisms highlight low or moderate frequencies of paternal transmission of cytoplasmic organelles, including both mitochondria and chloroplasts. It is well established that strict maternal inheritance is selectively blind to cytoplasmic elements that are deleterious to males - 'mother's curse'. But it is not known how sensitive this conclusion is to slight levels of paternal cytoplasmic leakage. We assess the scope for polymorphism when individuals bear multiple cytoplasmic alleles in the presence of paternal leakage, bottlenecks and recurrent mutation. When fitness interactions among cytoplasmic elements within an individual are additive, we find that sexually antagonistic polymorphism is restricted to cases of strong selection on males. However, when fitness interactions among cytoplasmic elements are nonlinear, much more extensive polymorphism can be supported in the cytoplasm. In particular, mitochondrial mutants that have strong beneficial fitness effects in males and weak deleterious fitness effects in females when rare (i.e. 'reverse dominance') are strongly favoured under paternal leakage. We discuss how such epistasis could arise through preferential segregation of mitochondria in sex-specific somatic tissues. Our analysis shows how paternal leakage can dampen the evolution of deleterious male effects associated with predominant maternal inheritance of cytoplasm, potentially explaining why 'mother's curse' is less pervasive than predicted by earlier work.
Insights
Paternal leakage of cytoplasmic organelles, like mitochondria, can reduce the negative effects on males. This genetic variation, or polymorphism, is more extensive when fitness effects are nonlinear, challenging the
Area of Science:
- Evolutionary genetics
- Mitochondrial genetics
- Cytoplasmic inheritance
Background:
- Multicellular organisms often exhibit maternal inheritance of cytoplasmic organelles (mitochondria, chloroplasts).
- Strict maternal inheritance can lead to 'mother's curse,' where cytoplasmic elements deleterious to males persist.
- The impact of low-level paternal leakage on this phenomenon is not well understood.
Purpose of the Study:
- To assess the potential for cytoplasmic polymorphism under paternal leakage, bottlenecks, and mutation.
- To investigate how fitness interactions among cytoplasmic elements influence sexually antagonistic polymorphism.
- To explore the role of nonlinear fitness interactions and 'reverse dominance' in supporting polymorphism.
Main Methods:
- Theoretical modeling of cytoplasmic inheritance with paternal leakage.
- Analysis of additive and nonlinear fitness interactions among cytoplasmic alleles.
- Evaluation of conditions favoring sexually antagonistic polymorphism.
Main Results:
- Sexually antagonistic polymorphism is limited with additive fitness effects, requiring strong male selection.
- Nonlinear fitness interactions support more extensive cytoplasmic polymorphism.
- Mitochondrial mutants with 'reverse dominance' (beneficial in males, deleterious in females when rare) are favored under paternal leakage.
Conclusions:
- Paternal leakage can significantly dampen the 'mother's curse' by allowing for greater cytoplasmic variation.
- Nonlinear epistasis, potentially via sex-specific tissue segregation, can explain observed patterns.
- The extent of 'mother's curse' may be less pervasive than predicted due to paternal leakage.
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