Abstract
Uniparental inheritance (UPI) of mitochondria predominates over biparental inheritance (BPI) in most eukaryotes. However, examples of BPI of mitochondria, or paternal leakage, are becoming increasingly prevalent. Most reported cases of BPI occur in hybrids of distantly related sub-populations. It is thought that BPI in these cases is maladaptive; caused by a failure of female or zygotic autophagy machinery to recognize divergent male-mitochondrial DNA ‘tags’. Yet recent theory has put forward examples in which BPI can evolve under adaptive selection, and empirical studies across numerous metazoan taxa have demonstrated outbreeding depression in hybrids attributable to disruption of population-specific mitochondrial and nuclear genotypes (mitonuclear mismatch). Based on these developments, we hypothesize that BPI may be favoured by selection in hybridizing populations when fitness is shaped by mitonuclear interactions. We test this idea using a deterministic, simulation-based population genetic model and demonstrate that BPI is favoured over strict UPI under moderate levels of gene flow typical of hybridizing populations. Our model suggests that BPI may be stable, rather than a transient phenomenon, in hybridizing populations.
Highlights
It is commonly held that mitochondrial DNA is inherited strictly down the maternal line in most eukaryotes
Our results show that u is always beneficial to hosts that possess the uncommon N-mt allele for a given region of the cline and that higher gene flow allows this benefit to be realized in more cells, explaining the link between gene flow and invasion of the mate-specific biparental inheritance (BPI) allele
We sought to provide a mathematical test of the hypothesis that BPI of mitochondria confers an adaptive advantage during episodes of hybridization between populations
Summary
It is commonly held that mitochondrial DNA (mtDNA) is inherited strictly down the maternal line in most eukaryotes. Recent theory has identified scenarios in which BPI may persist adaptively within species; either as a result of sexual conflict over primary control of mitochondrial inheritance (with male control favouring some paternal leakage), or because paternal leakage may mitigate the hypothesized accumulation of male-harming mtDNA variants expected under strictly maternal inheritance [4,28] While insightful, this previous work focused on situations where there is variation in mtDNA but no variation in the mitochondrialassociated nuclear genotype (i.e. among nuclear genes with mitochondrial function) and it fails to capture the dynamics in hybridizing populations where variation in both genomes may exist. We term this allele ‘mate-specific BPI’, and provide a mathematical model competing strict UPI against mate-specific BPI, to assess whether such an allele would be favoured or eliminated in hybridizing populations, under an assumption of a mitonuclear interactive effect on fitness
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