Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance

Abstract

Diversifying selection on metabolic pathways can reduce intraspecific gene flow and promote population divergence. An opportunity to explore this arises from mitonuclear discordance observed in an Australian bird Eopsaltria australis. Across >1500 km, nuclear differentiation is low and latitudinally structured by isolation by distance, whereas two highly divergent, parapatric mitochondrial lineages (>6.6% in ND2) show a discordant longitudinal geographic pattern and experience different climates. Vicariance, incomplete lineage sorting and sex-biased dispersal were shown earlier to be unlikely drivers of the mitonuclear discordance; instead, natural selection on a female-linked trait was the preferred hypothesis. Accordingly, here we tested for signals of positive, divergent selection on mitochondrial genes in E. australis. We used codon models and physicochemical profiles of amino acid replacements to analyse complete mitochondrial genomes of the two mitochondrial lineages in E. australis, its sister species Eopsaltria griseogularis, and outgroups. We found evidence of positive selection on at least five amino acids, encoded by genes of two oxidative phosphorylation pathway complexes NADH dehydrogenase (ND4 and ND4L) and cytochrome bc1 (cyt-b) against a background of widespread purifying selection on all mitochondrial genes. Three of these amino acid replacements were fixed in ND4 of the geographically most widespread E. australis lineage. The other two replacements were fixed in ND4L and cyt-b of the geographically more restricted E. australis lineage. We discuss whether this selection may reflect local environmental adaptation, a by-product of other selective processes, or genetic incompatibilities, and propose how these hypotheses can be tested in future.

Matching loci surveyed to questions asked in phylogeography

“…Thousands of studies have been based solely on mtDNA and the question has arisen as to whether the results of such studies can be accepted or whether they must be tested by corresponding analyses of nuclear loci. In our opinion, a relatively few instances of discordance between mitochondrial and nuclear genes has been emphasized [41][42][43], despite more frequent cases of congruence between the two types of markers [2,8,44 -46]. Our systematic examinations suggest that mtDNA can be an efficient estimator of population divergence, but not effective population size, which requires multiple loci for accurate estimate [2,8].…”

Experimental Support That Natural Selection Has Shaped the Latitudinal Distribution of Mitochondrial Haplotypes in Australian Drosophila melanogaster

“…Additional support for the hypothesis has been provided from studies of other metazoans, some of which have reported signatures of positive selection on mtDNA genes sampled from populations inhabiting particular thermal environments (Foote, et al 2011;Silva, et al 2014;80 Ma, et al 2015;Morales, et al 2015), and others which have documented variation in mitochondrial gene or haplotype frequencies along clinal gradients associated with climate, such as latitude (Silva, et al 2014;Consuegra, et al 2015), altitude (Fontanillas, et al 2005; Cheviron and Brumfield 2009), or with temperature itself (Quintela, et al 2014). Such clinal patterns are, however, based on correlations between haplotype frequencies and 85 environmental gradients.…”

Pleistocene divergence across a mountain range and the influence of selection on mitogenome evolution in threatened Australian freshwater cod species

“…However, despite a background of strong purifying selection, particular sites in the mitochondrial genome can experience positive selection in response to environmental pressures. Many studies have reported positive selection acting on mitochondrial protein-coding genes in vertebrates in response to environmental factors, including in mammals (da Fonseca et al, 2008), birds (Stager et al, 2014;Morales et al, 2015) and fish (Silva et al, 2014). Many of these studies find that candidate sites for positive selection are disproportionately concentrated in the NADH complex genes (OXPHOS complex I), which produces~40% of the proton flux required for ATP synthesis (Garvin et al, 2014).…”