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Results for “mitonuclear interactions”

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PubMed2026

Genetic and environmental interactions outweigh mitonuclear coevolution for complex traits in Drosophila.

The interdependent relationship between mitochondrial and nuclear genomes is a powerful model for understanding how epistasis shapes the architecture and evolution of complex traits. Once considered a neutral marker, mitochondrial DNA variation is now recognized as critical to phenotypic evolution because of its epistatic interactions and history of coevolution with the nuclear genome. A central challenge in evolutionary genetics is to quantify the relative importance of stabilizing and directional selection shaping complex trait distributions within and among species. Both can act on interacting and/or co-evolving genes contributing to quantitative traits, but resolving their relative roles is complicated by the complex architecture of most traits. Here, we use a panel of 90 Drosophila mitonuclear genotypes to quantify the relative contributions of mitochondrial, nuclear, and environmental variation and their interactions to four metabolically demanding complex traits. We sample both within-species and between-species mitochondrial variation and observe stronger interaction effects attributable to within-species variation, consistent with stabilizing selection maintaining mitonuclear function. Additionally, culturing the flies on a mitochondrial Complex I inhibitor, rotenone, reveals significant genotype x environment (G×E and G×G×E) interaction effects, providing insight into how genetic variation can be maintained across changing environments. Our results have broader implications in medicine, where mitochondrial DNA donors with longer purifying selection histories may be safer for mitochondrial replacement therapies.

Journal Article↗
PubMed2026

Mitochondrial genetic effects mediate the response to stress through development, but not adult metabolic rate in Drosophila.

Energy expenditure is fundamental to physiology, behaviour, ecology, and life history, yet the mechanisms that regulate metabolic rate remain poorly understood. At the cellular level, incompatibilities between the maternally inherited mitochondrial genome and the nuclear genome can impair energy production, signalling and gene expression, with potential to disrupt a wide range of physiological processes. However, how these often-subtle genomic mismatches influence whole-organism traits such as metabolic rate, activity, and fitness remains unclear. Here, we generated mitonuclear-mismatched fly lines to test how early-life dietary and metabolic stress affect larval and adult physiology. Our results revealed sex and line-specific physiological effects, with larval development, survival and female fertility strongly contingent on the haplotypes and treatment, while adult resting metabolic rate and activity were not influenced by mitochondrial haplotype, nor by developmental stress.

Drosophila melanogaster↗
PubMed2025

Admixture Mapping Reveals Evidence for Multiple Mitonuclear Incompatibilities in Swordtail Fish Hybrids.

How barriers to gene flow arise between closely related species is one of the oldest questions in evolutionary biology. Classic models in evolutionary biology predict that negative epistatic interactions between variants in the genomes of diverged lineages, known as hybrid incompatibilities, will reduce viability or fertility in hybrids. The genetic architecture of these interactions and the evolutionary paths through which they arise have profound implications for the efficacy of hybrid incompatibilities as barriers to gene flow between species. While these questions have been studied using theoretical approaches for several decades, only recently has it become possible to genetically map larger numbers of hybrid incompatibilities. Here, we use admixture mapping in natural hybrid populations of swordtail fish (Xiphophorus) to identify hybrid incompatibilities involving genetic interactions between the mitochondrial and nuclear genomes. We find that at least nine regions of the genome are involved in mitonuclear incompatibilities. These incompatibilities involve interactions between the nuclear genome and the X. malinche mitochondria, the X. birchmanni mitochondria, or both. Moreover, they vary in the strength of selection they experience and the degree to which they limit gene flow in natural hybrid populations. Our results build a deeper understanding of the complex architecture of selection against incompatibilities in naturally hybridising species and highlight an important role of mitonuclear interactions in the evolution of reproductive barriers between closely related species.

Animals↗
PubMed2026

Disruption of mitonuclear coadaptation and compensatory evolution after an extreme dietary shift in carnivorous butterflies.

Mitochondrial function depends on tight coordination between mitochondrial and nuclear genomes, which requires long-term coevolution to maintain mitonuclear coadaptation. While mitonuclear incompatibility is typically studied in the context of hybridization, other evolutionary scenarios that may disrupt coadaptation between the two genomes remain less explored. Here, we propose that extreme ecological niche shifts may disrupt mitonuclear coadaptation, which we test in carnivorous Miletinae butterflies with an extreme dietary transition. By generating high-quality genome assemblies, we found that Miletinae exhibit extensive chromosomal rearrangements. Comparative phylogenomic analyses revealed a striking asymmetric mitonuclear evolutionary response: Miletinae exhibit elevated mitochondrial nucleotide substitution rates compared to phytophagous relatives, whereas nuclear rates remain stable. This shift reverses the typical lepidopteran pattern where nuclear rates exceed mitochondrial rates. Interestingly, this mitochondrial acceleration is driven primarily by relaxed purifying selection rather than positive selection. To sustain mitochondrial function, the nuclear genome of Miletinae underwent pervasive, multilayered compensatory evolution. We detected strong signatures of positive selection and accelerated evolution in nuclear genes directly interacting with mitochondrial components across oxidative phosphorylation (OXPHOS) complexes, the mitochondrial translation, and replication and transcription machinery. Furthermore, this nuclear compensatory response extends to systems governing mitochondrial homeostasis, including protein quality control and RNA degradation and stabilization. Our results support a model in which extreme ecological transitions can disrupt ancestral mitonuclear coadaptation and promote the emergence of a new coadapted state through systemic nuclear compensation. This study broadens the conceptual framework of mitonuclear coevolution and highlights its role in facilitating evolutionary persistence after major ecological shifts.

Animals↗
PubMed2026

Dissecting contributions of directional and balancing selection to trajectories of mitochondrial haplotype evolution in Drosophila melanogaster.

Emerging evidence suggests mtDNA haplotypes contribute to fitness variation and local adaptation, with directional thermal selection and negative frequency-dependent selection shaping haplotype diversity. However, their interplay remains unexplored. We conducted experimental evolution using Drosophila melanogaster populations from opposite ends of an Australian latitudinal cline (Melbourne and Townsville), exposing them to contrasting temperatures (17°C versus 27°C) and varying starting frequencies of two mtDNA haplotypes (A1 and B1) that occur at appreciable frequencies in these populations. We paired this with population genetic simulations to estimate selection and its influence on haplotype trajectories. Haplotype frequencies were influenced by interactions involving temperature, starting frequency, and nuclear genomic background (Melbourne, Townsville, or admixed). Although prior work predicted A1 should be favoured at the warmer temperature and B1 at the cooler temperature, A1 was generally favoured across both temperatures. Simulations supported directional selection in populations evolving at 17°C in the Melbourne background; otherwise dynamics were best explained by balancing selection shaped by negative frequency-dependent fitness effects. Patterns also varied across nuclear backgrounds, suggestive of mito-nuclear epistasis. These findings challenge a simple thermal adaptation model of mtDNA dynamics, suggesting that mtDNA evolution is shaped by interacting effects of temperature, frequency-dependence, nuclear background and experimental environment.

adaptation↗