Reconciling the Mitonuclear Compatibility Species Concept with Rampant Mitochondrial Introgression

Abstract

The mitonuclear compatibility species concept defines a species as a population that is genetically isolated from other populations by uniquely coadapted mitochondrial (mt) and nuclear genes. A key prediction of this hypothesis is that the mt genotype of each species will be functionally distinct and that introgression of mt genomes will be prevented by mitonuclear incompatibilities that arise when heterospecific mt and nuclear genes attempt to cofunction to enable aerobic respiration. It has been proposed, therefore, that the observation of rampant introgression of mt genotypes from one species to another constitutes a strong refutation of the mitonuclear speciation. The displacement of a mt genotype from a nuclear background with which it co-evolved to a foreign nuclear background will necessarily lead to fitness loss due to mitonuclear incompatibilities. Here I consider two potential benefits of mt introgression between species that may, in some cases, overcome fitness losses arising from mitonuclear incompatibilities. First, the introgressed mt genotype may be better adapted to the local environment than the native mt genotype such that higher fitness is achieved through improved adaptation via introgression. Second, if the mitochondria of the recipient taxa carry a high mutational load, then introgression of a foreign, less corrupt mt genome may enable the recipient taxa to escape its mutational load and gain a fitness advantage. Under both scenarios, fitness gains from novel mt genotypes could theoretically compensate for the fitness that is lost via mitonuclear incompatibility. I also consider the role of endosymbionts in non-adaptive rampant introgression of mt genomes. I conclude that rampant introgression is not necessarily evidence against the idea of tight mitonuclear coadaptation or the mitonuclear compatibility species concept. Rampant mt introgression will typically lead to erasure of species but in some cases could lead to hybrid speciation.