Mitonuclear co-introgression opposes genetic differentiation between phenotypically divergent songbirds

Abstract

Comparisons of genomic variation among closely related species often show more differentiation in mitochondrial DNA (mtDNA) and sex chromosomes than in autosomes, a pattern expected due to the differing effective population sizes and evolutionary dynamics of these genomic components. Yet, introgression can cause species pairs to deviate dramatically from general differentiation trends. The yellowhammer (Emberiza citrinella) and the pine bunting (E. leucocephalos) are hybridizing avian sister species that differ greatly in appearance and moderately in nuclear DNA, but that show no mtDNA differentiation. This mitonuclear discordance is best explained by adaptive mtDNA introgression--a process that can select for co-introgression at nuclear genes with mitochondrial functions (mitonuclear genes). To better understand the extent of mitonuclear discordance and characterize nuclear differentiation patterns in this system, we investigated genome-wide differentiation between allopatric yellowhammers and pine buntings and compared it to what was seen previously in mtDNA. We found significant nuclear differentiation that was highly heterogeneous across the genome, with a particularly wide differentiation peak on the sex chromosome Z. We further tested for preferential introgression of mitonuclear genes and found statistical support for this process in yellowhammers. A role for mitonuclear coevolution in this system is supported by a stronger signal of co-introgression in genes coding for subunits of the mitoribosome and electron transport chain complexes. Altogether, our study emphasizes the extreme variation seen in differentiation across genomic components and study systems as well as highlights the ramifications of this variation in species evolution.