Genetic incompatibilities in reciprocal hybrids between populations of Tigriopus californicus with low to moderate mitochondrial sequence divergence

Abstract

All mitochondrial-encoded proteins and RNAs function through interactions with nuclear-encoded proteins. These interactions are critical for mitochondrial function and eukaryotic fitness, and coevolution maintains inter-genomic (i.e., mitonuclear) compatibility within taxa. Hybridization can disrupt coevolved interactions, resulting in hybrid breakdown, and mitonuclear incompatibilities may be important mechanisms underlying reproductive isolation and, potentially, speciation. Recently, signatures of strong selection to maintain compatible mitonuclear genotypes in hybrids have been detected in at least some inter-population crosses. However, this work has only been conducted in crosses between populations with extremely high levels of genetic divergence in both their mitochondrial and nuclear genomes, leaving the generality of strong selection for mitonuclear compatibility unclear. Here we address this limitation with reciprocal inter-population F2 hybrids between relatively low-divergence populations of the intertidal copepod Tigriopus californicus. Our results show that the dominance of mitonuclear effects consistent with coevolved mitonuclear genotypes in fast-developing (i.e., high-fitness) hybrids is reduced in low-divergence crosses, but that selection to maintain mitonuclear compatibility is still observed on some nuclear chromosomes. Consequently, we demonstrate that, even at low levels of genetic divergence between taxa, mitonuclear incompatibilities may play a key role in the early stages of reproductive isolation.