Random Mating in a Hybrid Zone Between Two Putative Climate-Adapted Bird Lineages With Predicted Mitonuclear Incompatibilities

Biochemical and evolutionary interactions between mitochondrial and nuclear genomes (‘mitonuclear interactions’) are proposed to underpin fundamental aspects of biology including evolution of sexual reproduction, adaptation and speciation. We investigated the role of pre-mating isolation in maintaining functional mitonuclear interactions in wild populations bearing diverged, putatively co-adapted mitonuclear genotypes. Two lineages of eastern yellow robin Eopsaltria australis—putatively climate-adapted to ‘inland’ and ‘coastal’ climates—differ by ~7% of mitogenome nucleotides, whereas nuclear genome differences are concentrated into a sex-linked region enriched with mitochondrial functions. Female-specific selection and male-mediated gene flow across the hybrid zone where the lineages coexist and interbreed can explain this pattern. It remains unknown whether lineage divergence is driven by intrinsic incompatibilities (particularly in females; Haldane's rule), extrinsic selection, both, or other drivers. We tested whether lineage divergence could be facilitated by non-random mate-pairing with respect to partners' mitolineage and/or mitonuclear genes encoded by the Z sex-chromosome, which differ between the lineages. We used field-, Z-linked- and mitolineage data from two locations where lineages hybridise to test whether females mate disproportionately with (1) males of their own mitolineage and/or bearing similar Z-linked variation, as might be expected if hybrids experience intrinsic incompatibilities, or (2) putatively locally-adapted males, as might be expected under environmental selection. Comparing field observations with simulations provided no evidence of non-random mating, thus drivers of observed population genetic patterns are consistent with reduced female gene flow likely acting post-mating. Future tests of female-biased mortality at different life stages and habitat selection may clarify mechanisms of selection.