Perched at the mito-nuclear crossroads: Divergent mitochondrial lineages correlate with environment in the face of ongoing nuclear gene flow in an Australian bird

Abstract

Relationships among multilocus genetic variation, geography, and environment can reveal how evolutionary processes affect genomes. We examined the evolution of an Australian bird, the eastern yellow robin Eopsaltria australis, using mitochondrial (mtDNA) and nuclear (nDNA) genetic markers, and bioclimatic variables. In southeastern Australia, two divergent mtDNA lineages occur east and west of the Great Dividing Range, perpendicular to latitudinal nDNA structure. We evaluated alternative scenarios to explain this striking discordance in landscape genetic patterning. Stochastic mtDNA lineage sorting can be rejected because the mtDNA lineages are essentially distinct geographically for > 1500 km. Vicariance is unlikely: the Great Dividing Range is neither a current barrier nor was it at the Last Glacial Maximum according to species distribution modeling; nuclear gene flow inferred from coalescent analysis affirms this. Female philopatry contradicts known female-biased dispersal. Contrasting mtDNA and nDNA demographies indicate their evolutionary histories are decoupled. Distance-based redundancy analysis, in which environmental temperatures explain mtDNA variance above that explained by geographic position and isolation-by-distance, favors a nonneutral explanation for mitochondrial phylogeographic patterning. Thus, observed mito-nuclear discordance accords with environmental selection on a female-linked trait, such as mtDNA, mtDNA–nDNA interactions or genes on W-chromosome, driving mitochondrial divergence in the presence of nuclear gene flow.