Genomic Analysis Suggests That Mitonuclear Coevolution Proceeds Over Rapid Timescales in the Amazonian <i>Pipra</i> Manakin Complex

Mitonuclear coevolution is defined as reciprocal selection between the nuclear and mitochondrial genomes and is necessary to maintain compatibility between nuclear- and mitochondrially-encoded products that interact during mitochondrial processes including mitochondrial genome replication, transcription and translation and oxidative phosphorylation. Theory predicts that mitonuclear coevolution may play a crucial role in the early phases of speciation by generating strong genetic incompatibilities between recently diverged taxa that have evolved unique mitochondrial-mitonuclear haplotypes. However, the timescale over which mitonuclear coevolution proceeds remains unclear, making it difficult to definitively link this process with early speciation. Here, we test for expected genomic signals of mitonuclear coevolution across the Amazonian Pipra manakin complex, which includes recently and more deeply diverged avian lineages. Using dN/dS ratio analyses, we compared signals of positive selection in mitonuclear gene categories and functionally equivalent nuclear gene categories that do not participate in mitonuclear coevolution for each pair of Pipra lineages separately and for all the lineages simultaneously. For the ribosomal protein and aminoacyl tRNA synthetase (AARS) gene categories, we identified genomic patterns consistent with stronger positive selection in mitonuclear versus nuclear genes, which is suggestive of mitonuclear coevolution having occurred across the Pipra complex. Significantly, we determined that expected genomic signals of mitonuclear coevolution could be identified between lineages that diverged as recently as 0.35-0.4 MYA. This time span is in keeping with the initial stages of avian speciation and suggests that mitonuclear coevolution may operate on a timescale that would allow it to play an important role during early speciation.