Pleistocene-dated biogeographic barriers drove divergence within the Australo-Papuan region in a sex-specific manner: an example in a widespread Australian songbird.

Understanding how environmental change has shaped species evolution can inform predictions of how future climate change might continue to do so. Research of widespread biological systems spanning multiple climates that have been subject to environmental change can yield generalizable inferences about the neutral and adaptive processes driving lineage divergence during periods of environmental change. We contribute to the growing body of multi-locus phylogeographic studies investigating the effect of Pleistocene climate change on species evolution by focusing on a widespread Australo-Papuan songbird with several mitochondrial lineages that diverged during the Pleistocene, the grey shrike-thrush (Colluricincla harmonica). We employed multi-locus phylogenetic, population genetic and coalescent analyses to (1) assess whether nuclear genetic diversity suggests a history congruent with that based on phenotypically defined subspecies ranges, mitochondrial clade boundaries and putative biogeographical barriers, (2) estimate genetic diversity within and genetic differentiation and gene flow among regional populations and (3) estimate population divergence times. The five currently recognized subspecies of grey shrike-thrush are genetically differentiated in nuclear and mitochondrial genomes, but connected by low levels of gene flow. Divergences among these populations are concordant with recognized historical biogeographical barriers and date to the Pleistocene. Discordance in the order of population divergence events based on mitochondrial and nuclear genomes suggests a history of sex-biased gene flow and/or mitochondrial introgression at secondary contacts. This study demonstrates that climate change can impact sexes with different dispersal biology in different ways. Incongruence between population and mitochondrial trees calls for a genome-wide investigation into dispersal, mitochondrial introgression and mitonuclear evolution.

Climate-driven mitochondrial selection: A test in Australian songbirds.

Diversifying selection between populations that inhabit different environments can promote lineage divergence within species and ultimately drive speciation. The mitochondrial genome (mitogenome) encodes essential proteins of the oxidative phosphorylation (OXPHOS) system and can be a strong target for climate-driven selection (i.e., associated with inhabiting different climates). We investigated whether Pleistocene climate changes drove mitochondrial selection and evolution within Australian birds. First, using phylogeographic analyses of the mitochondrial ND2 gene for 17 songbird species, we identified mitochondrial clades (mitolineages). Second, using distance-based redundancy analyses, we tested whether climate predicts variation in intraspecific genetic divergence beyond that explained by geographic distances and geographic position. Third, we analysed 41 complete mitogenome sequences representing each mitolineage of 17 species using codon models in a phylogenetic framework and a biochemical approach to identify signals of selection on OXPHOS protein-coding genes and test for parallel selection in mitolineages of different species existing in similar climates. Of 17 species examined, 13 had multiple mitolineages (range: 2-6). Climate was a significant predictor of mitochondrial variation in eight species. At least two amino acid replacements in OXPHOS complex I could have evolved under positive selection in specific mitolineages of two species. Protein homology modelling showed one of these to be in the loop region of the ND6 protein channel and the other in the functionally critical helix HL region of ND5. These findings call for direct tests of the functional and evolutionary significance of mitochondrial protein candidates for climate-associated selection.