ABSTRACT
Proteins encoded by interacting mitochondrial and nuclear genes catalyze essential metabolic processes in eukaryote cells. The correct functioning of such processes requires combinations of mitochondrial and nuclear alleles that work together (mitonuclear interactions) and the avoidance of mismatched combinations (mitonuclear incompatibilities). This interplay could have a major role during the early stages of population divergence. Here, we show that mitonuclear interactions maintain a deep mitochondrial divergence in the face of nuclear gene flow between two lineages of the songbird Eastern Yellow Robin (Eopsaltria australis) occupying contrasting climatic habitats. Using >60,000 SNPs we explored patterns of nuclear gene differentiation and introgression along two sampling transects intersecting the deep mitochondrial divergence between lineages. We found a replicated pattern of low genome-wide differentiation contrasting with two prominent regions of high differentiation (genomic islands of divergence) in different nuclear backgrounds. The largest island of divergence (~15.4 Mb) showed a significant excess of nuclear-encoded genes with mitochondrial functions (N-mt genes), low genetic diversity and high levels of linkage disequilibrium. Thus, genetic differentiation between the two adjacent but climatically divergent lineages is mostly limited to the mitochondrial genome and a nuclear genomic region containing tightly linked N-mt genes that presumably experience reduced recombination. The second island of divergence mapped to the Z-chromosome, suggesting that nuclear gene flow occurs primarily via male hybrids, in accordance with Haldane’s Rule. Our results are consistent with accumulating evidence that mitonuclear co-evolution could represent a key vehicle for climatic adaptation during population divergence.