Selection for biparental inheritance of mitochondria under hybridization and mitonuclear fitness interactions

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.