Mitochondrial-nuclear interactions maintain geographic separation of deeply diverged mitochondrial lineages in the face of nuclear gene flow

Abstract

Metabolic processes in eukaryotic cells depend on interactions between mitochondrial and nuclear gene products (mitonuclear interactions). These interactions could play a direct role in population divergence. We studied the evolution of mitonuclear interactions in a widespread passerine that experienced population divergence followed by bi-directional mitochondrial introgression into different nuclear backgrounds. Using >60,000 SNPs, we quantified patterns of nuclear genetic differentiation between populations that occupy different climates and harbour deeply divergent mitolineages despite ongoing nuclear gene flow. Analyses were performed independently for two sampling transects intersecting mitochondrial divergence in different nuclear backgrounds. In both transects, low genome-wide nuclear differentiation was accompanied by strong differentiation at a ~15.4 Mb region of chromosome 1A. This region is enriched for genes performing mitochondrial functions. Molecular signatures of selective sweeps in this region alongside those in the mitochondrial genome suggest a history of adaptive mitonuclear co-introgression. The chromosome 1A region has elevated linkage disequilibrium, suggesting that selection on genomic architecture may favour low recombination among nuclear-encoded genes with mitochondrial functions. In this system, mitonuclear interactions appear to maintain the geographic separation of two mitolineages in the face of nuclear gene flow, supporting mitonuclear co-evolution as an important vehicle for climatic adaptation and population divergence.