Perpendicular axes of differentiation generated by mitochondrial introgression

Abstract

Differential introgression of mitochondrial vs. nuclear DNA generates discordant patterns of geographic variation and can promote population divergence and speciation. We examined a potential case of mitochondrial introgression leading to two perpendicular axes of differentiation. The Eastern Yellow Robin Eopsaltria australis, a widespread Australian bird, shows a deep mitochondrial split that is perpendicular to north-south nuclear DNA and plumage colour differentiation. We propose a scenario to explain this pattern: (i) first, both nuclear and mitochondrial genomes differentiated in concert during north-south population divergence; (ii) later, their histories disconnected after two mitochondrial introgression events resulting in a deep mitochondrial split perpendicular to the nuclear DNA structure. We explored this scenario by coalescent modelling of ten mitochondrial genes and 400 nuclear DNA loci. Initial mitochondrial and nuclear genome divergences were estimated to have occurred in the early Pleistocene, consistent with the proposed scenario. Subsequent climatic transitions may have driven later mitochondrial introgression. We consider neutral introgression unlikely and instead propose that the evidence is more consistent with adaptive mitochondrial introgression and selection against incompatible mitochondrial-nuclear combinations. This likely generated an axis of coastal-inland mitochondrial differentiation in the face of nuclear gene flow, perpendicular to the initial north-south axis of differentiation (reflected in genomewide nuclear DNA and colour variation).

Climate‐driven mitochondrial selection: A test in Australian songbirds

“…For eastern yellow robin (Pavlova et al., ) and grey shrike‐thrush (Lamb, Sunnucks, Gonçalves Da Silva, Joseph, & Pavlova, unpublished manuscript), drift in small populations is an unlikely explanation for three of seven candidates for positive selection (ND5 A574T , ND6 V123G and ND6 F114S ), because N e proxies (e.g., nucleotide diversity for introns, allelic richness for microsatellites) are either larger or similar in populations with putatively positively selected mitolineages (EYR‐A in eastern yellow robin, and southwest and southeast in grey shrike‐thrush, respectively) compared to populations with other mitolineages. Even though congruence of nuclear and mitochondrial structure for the grey shrike‐thrush (Lamb, Sunnucks, Gonçalves Da Silva, Joseph, & Pavlova, unpublished manuscript) suggests drift in isolation as a major force of mitochondrial divergence, it is possible that local selection drove beneficial alleles to fixation in large populations with limited gene flow (Morales, Sunnucks, Joseph, & Pavlova, ; Morales et al., ). In the absence of adequate nuclear estimates, N e could be approximated by the relative ranges of respective mitolineages, assuming that population densities across the species range are comparable.…”

Genomic scans reveal multiple mito‐nuclear incompatibilities in population crosses of the copepod Tigriopus californicus

“…There is no doubt that DMI involving sex chromosomes are important in taxa that possess them, exemplified by the large number of species that obey Haldane's Rule (where the heterogametic sex is affected disproportionately by intrinsic postzygotic isolation; Haldane 1922), but even in some of these cases mito-nuclear incompatibilities can also contribute to decreased hybrid fitness, as has been observed in birds (McFarlane et al 2016;Hill 2017;Morales et al 2017;Lamb et al 2018). One reason why the importance of mito-nuclear incompatibilities may have been underappreciated in these cases is because other reproductive barriers evolve very early in divergence for some of the most studied taxa.…”

The Mitonuclear Dimension of Neanderthal and Denisovan Ancestry in Modern Human Genomes

“…By incorporating models of molecular structures, various studies have investigated the possibility that physically interacting residues in mitochondrial- and nuclear-encoded subunits can undergo coevolutionary changes that lead to coadapted mitonuclear genotypes (Schmidt et al 2001; Melvin et al 2008; Osada and Akashi 2012; Aledo et al 2014; Havird et al 2015). However, researchers have only recently begun using genomic data sets to examine the effect of selection on maintaining associations between coadapted combinations of mitochondrial haplotypes and N-mt alleles during genetic admixture/hybridization (Trier et al 2014; Bar-Yaacov et al 2015; Beck et al 2015; Sloan et al 2015; McKenzie et al 2016; Baris et al 2017; Morales et al 2017; Runemark et al 2017). These studies have produced mixed results about the extent to which selection can preferentially act on N-mt loci relative to the rest of the nuclear genome.…”