Hernán E. Morales

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

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.

Integrative approaches for studying mitochondrial and nuclear genome co-evolution in oxidative phosphorylation

In animals, interactions among gene products of mitochondrial and nuclear genomes (mitonuclear interactions) are of profound fitness, evolutionary, and ecological significance. Most fundamentally, the oxidative phosphorylation (OXPHOS) complexes responsible for cellular bioenergetics are formed by the direct interactions of 13 mitochondrial-encoded and ∼80 nuclear-encoded protein subunits in most animals. It is expected that organisms will develop genomic architecture that facilitates co-adaptation of these mitonuclear interactions and enhances biochemical efficiency of OXPHOS complexes. In this perspective, we present principles and approaches to understanding the co-evolution of these interactions, with a novel focus on how genomic architecture might facilitate it. We advocate that recent interdisciplinary advances assist in the consolidation of links between genotype and phenotype. For example, advances in genomics allow us to unravel signatures of selection in mitochondrial and nuclear OXPHOS genes at population-relevant scales, while newly published complete atomic-resolution structures of the OXPHOS machinery enable more robust predictions of how these genes interact epistatically and co-evolutionarily. We use three case studies to show how integrative approaches have improved the understanding of mitonuclear interactions in OXPHOS, namely those driving high-altitude adaptation in bar-headed geese, allopatric population divergence in Tigriopus californicus copepods, and the genome architecture of nuclear genes coding for mitochondrial functions in the eastern yellow robin.

Patterns of diversification in islands: A comparative study across three gecko genera in the Socotra Archipelago☆

In this study we used the complete fauna of geckos of the Socotra Archipelago to test whether the three gecko genera co-occurring in the islands (Pristurus, Hemidactylus and Haemodracon) produced similar outcomes of morphological and climatic diversification. To test this, we produced a time-calibrated tree of 346 geckos including all 16 endemic species of the archipelago and 26 potential close-relatives in the continent. Our dating estimates revealed that most of the diversity of geckos in the archipelago was the consequence of in situ diversification. However not all genera shared similar patterns of diversification. While in Hemidactylus and Haemodracon this involved great differences in body size and low levels of climatic diversification (mostly involving sympatric distributions), an opposite pattern appeared in Pristurus in which most of the diversification involved shifts in climatic envelopes (mostly involving allopatric and parapatric distributions) but almost no size differentiation. Consistently with this, Pristurus was the only genus in which rates of size diversification in islands were substantially lower than in the continent. This illustrates how different groups can greatly differ in their patterns of intra-island diversification and highlights the importance of taxon-dependent factors at determining different patterns of diversification in the same insular context.

Perpendicular axes of differentiation generated by mitochondrial introgression

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).

Mitochondrial-nuclear interactions maintain geographic separation of deeply diverged mitochondrial lineages in the face of nuclear gene flow

Metabolic processes in eukaryotic cells depend on interactions between mitochondrial and nuclear gene products (mitonuclear interactions). These interactions could play a direct role in population divergence. We studied the evolution of mitonuclear interactions in a widespread passerine that experienced population divergence followed by bi-directional mitochondrial introgression into different nuclear backgrounds. Using >60,000 SNPs, we quantified patterns of nuclear genetic differentiation between populations that occupy different climates and harbour deeply divergent mitolineages despite ongoing nuclear gene flow. Analyses were performed independently for two sampling transects intersecting mitochondrial divergence in different nuclear backgrounds. In both transects, low genome-wide nuclear differentiation was accompanied by strong differentiation at a ~15.4 Mb region of chromosome 1A. This region is enriched for genes performing mitochondrial functions. Molecular signatures of selective sweeps in this region alongside those in the mitochondrial genome suggest a history of adaptive mitonuclear co-introgression. The chromosome 1A region has elevated linkage disequilibrium, suggesting that selection on genomic architecture may favour low recombination among nuclear-encoded genes with mitochondrial functions. In this system, mitonuclear interactions appear to maintain the geographic separation of two mitolineages in the face of nuclear gene flow, supporting mitonuclear co-evolution as an important vehicle for climatic adaptation and population divergence.Proteins encoded by interacting mitochondrial and nuclear genes catalyze essential metabolic processes in eukaryote cells. The correct functioning of such processes requires combinations of mitochondrial and nuclear alleles that work together (mitonuclear interactions) and the avoidance of mismatched combinations (mitonuclear incompatibilities). This interplay could have a major role during the early stages of population divergence. Here, we show that mitonuclear interactions maintain a deep mitochondrial divergence in the face of nuclear gene flow between two lineages of the songbird Eastern Yellow Robin (Eopsaltria australis) occupying contrasting climatic habitats. Using >60,000 SNPs we explored patterns of nuclear gene differentiation and introgression along two sampling transects intersecting the deep mitochondrial divergence between lineages. We found a replicated pattern of low genome-wide differentiation contrasting with two prominent regions of high differentiation (genomic islands of divergence) in different nuclear backgrounds. The largest island of divergence (~15.4 Mb) showed a significant excess of nuclear-encoded genes with mitochondrial functions (N-mt genes), low genetic diversity and high levels of linkage disequilibrium. Thus, genetic differentiation between the two adjacent but climatically divergent lineages is mostly limited to the mitochondrial genome and a nuclear genomic region containing tightly linked N-mt genes that presumably experience reduced recombination. The second island of divergence mapped to the Z-chromosome, suggesting that nuclear gene flow occurs primarily via male hybrids, in accordance with Haldane’s Rule. Our results are consistent with accumulating evidence that mitonuclear co-evolution could represent a key vehicle for climatic adaptation during population divergence.

Perpendicular axes of incipient speciation generated by mitochondrial introgression

Differential introgression of mitochondrial versus nuclear DNA generates discordant patterns of geographic variation and can promote speciation. We examined a potential case of mitochondrial introgression leading to two perpendicular axes of differentiation. The Eastern Yellow Robin, a widespread Australian bird, shows a deep mitochondrial split that is perpendicular to north-south nuclear DNA and plumage colour differentiation. We proposed a scenario to explain this pattern: (1) the two nuclear and mitochondrial genomes differentiated in concert during north-south population divergence; (2) later, their histories disconnected after two mitochondrial introgression events resulting in a deep mitochondrial split perpendicular to the nuclear DNA structure. We tested 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 reject neutral introgression and consider evidence consistent with adaptive mitochondrial introgression and selection against incompatible mitochondrial-nuclear combinations. This likely generated an axis of incipient speciation associated with mitochondrial differentiation in the face of nuclear gene flow, perpendicular to the initial north-south axis of incipient speciation (reflected in nuclear differentiation and colour variation).

Population mitogenomics provides insights into evolutionary history, source of invasions and diversifying selection in the House Crow (Corvus splendens)

The House Crow (Corvus splendens) is a useful study system for investigating the genetic basis of adaptations underpinning successful range expansion. The species originates from the Indian subcontinent, but has successfully spread through a variety of thermal environments across Asia, Africa and Europe. Here, population mitogenomics was used to investigate the colonisation history and to test for signals of molecular selection on the mitochondrial genome. We sequenced the mitogenomes of 89 House Crows spanning four native and five invasive populations. A Bayesian dated phylogeny, based on the 13 mitochondrial protein-coding genes, supports a mid-Pleistocene (~630,000 years ago) divergence between the most distant genetic lineages. Phylogeographic patterns suggest that northern South Asia is the likely centre of origin for the species. Codon-based analyses of selection and assessments of changes in amino acid properties provide evidence of positive selection on the ND2 and ND5 genes against a background of purifying selection across the mitogenome. Protein homology modelling suggests that four amino acid substitutions inferred to be under positive selection may modulate coupling efficiency and proton translocation mediated by OXPHOS complex I. The identified substitutions are found within native House Crow lineages and ecological niche modelling predicts suitable climatic areas for the establishment of crow populations within the invasive range. Mitogenomic patterns in the invasive range of the species are more strongly associated with introduction history than climate. We speculate that invasions of the House Crow have been facilitated by standing genetic variation that accumulated due to diversifying selection within the native range.

Genomic architecture of parallel ecological divergence: beyond a single environmental contrast

The genetic basis of parallel ecological divergence provides important clues to the operation of natural selection and the predictability of evolution. Many examples exist where binary environmental contrasts seem to drive parallel divergence. However, this simplified view can conceal important components of parallel divergence because environmental variation is often more complex. Here, we disentangle the genetic basis of parallel divergence across two axes of environmental differentiation (crab-predation vs. wave-action and low-shore vs. high-shore habitat contrasts) in the marine snail Littorina saxatilis, a well established natural system of parallel ecological divergence. We used whole-genome resequencing across multiple instances of these two environmental axes, at local and regional scales from Spain to Sweden. Overall, sharing of genetic differentiation is generally low but it is highly heterogeneous across the genome and increases at smaller spatial scales. We identified genomic regions, both overlapping and non-overlapping with recently described candidate chromosomal inversions, that are differentially involved in adaptation to each of the environmental axis. Thus, the evolution of parallel divergence in L. saxatilis is largely determined by the joint action of geography, history, genomic architecture and congruence between environmental axes. We argue that the maintenance of standing variation, perhaps as balanced polymorphism, and/or the re-distribution of adaptive variants via gene flow can facilitate parallel divergence in multiple directions as an adaptive response to heterogeneous environments.

Concordant divergence of mitogenomes and a mitonuclear gene cluster in bird lineages inhabiting different climates

Metabolic processes in eukaryotic cells depend on interactions between mitochondrial and nuclear gene products (mitonuclear interactions). These interactions could have a direct role in population divergence. Here, we study mitonuclear co-evolution in a widespread bird that experienced population divergence followed by bidirectional mitochondrial introgression into different nuclear backgrounds. Using >60,000 single nucleotide polymorphisms, we quantify patterns of nuclear genetic differentiation between populations that occupy areas with different climates and harbour deeply divergent mitochondrial lineages despite ongoing nuclear gene flow. We find that strong genetic differentiation and sequence divergence in a region of ~15.4 megabases on chromosome 1A mirror the geographic pattern of mitochondrial DNA divergence. This result is seen in two different transects representing populations with different nuclear backgrounds. The chromosome 1A region is enriched for genes performing mitochondrial functions (N-mt genes). Molecular signatures of selective sweeps in this region alongside those in the mitochondrial genome suggest a history of adaptive mitonuclear co-introgression. Moreover, evidence for large linkage disequilibrium blocks in this genomic region suggests that low recombination could facilitate functional interactions between co-evolved nuclear alleles. Our results are consistent with mitonuclear co-evolution as an important mechanism for population divergence and local adaptation.Mitonuclear interactions can promote population divergence. Here, the authors find a genomic cluster of differentiation and signatures of selection in a region with an over-representation of nuclear genes that interact with mitochondrial genes in a songbird.