An experimental test of temperature‐dependent selection on mitochondrial haplotypes in Callosobruchus maculatus seed beetles

Abstract

Mitochondrial DNA (mtDNA) consists of few but vital maternally inherited genes that interact closely with nuclear genes to produce cellular energy. How important mtDNA polymorphism is for adaptation is still unclear. The assumption in population genetic studies is often that segregating mtDNA variation is selectively neutral. This contrasts with empirical observations of mtDNA haplotypes affecting fitness‐related traits and thermal sensitivity, and latitudinal clines in mtDNA haplotype frequencies. Here, we experimentally test whether ambient temperature affects selection on mtDNA variation, and whether such thermal effects are influenced by intergenomic epistasis due to interactions between mitochondrial and nuclear genes, using replicated experimental evolution in Callosobruchus maculatus seed beetle populations seeded with a mixture of different mtDNA haplotypes. We also test for sex‐specific consequences of mtDNA evolution on reproductive success, given that mtDNA mutations can have sexually antagonistic fitness effects. Our results demonstrate natural selection on mtDNA haplotypes, with some support for thermal environment influencing mtDNA evolution through mitonuclear epistasis. The changes in male and female reproductive fitness were both aligned with changes in mtDNA haplotype frequencies, suggesting that natural selection on mtDNA is sexually concordant in stressful thermal environments. We discuss the implications of our findings for the evolution of mtDNA.

Mitonuclear interactions alter sex-specific longevity in a species without sex chromosomes

“…Natural selection can operate in females; therefore, male harming mtDNA mutations may accumulate if they fail to decrease female fitness, referred to as the Mother's Curse [11]. Although under thermally stressful conditions, functional mitochondrial variation can result in sexually concordant selection [12]. The most rigorous tests of the Mother's Curse hypothesis have been conducted in Drosophila, where some studies find support for the hypothesis (e.g.…”

The Role of Mitonuclear Incompatibility in Bipolar Disorder Susceptibility and Resilience Against Environmental Stressors

“…Strains with concordant mitonuclear genomes exhibited increased relative fitness compared to strains with differing mitonuclear genomes. At colder temperatures, Brazilian and Yemen mitotypes introgressed with California nuclear genomes showed opposite effects in fitness, again suggesting that temperature contributes to mitonuclear effects on relative fitness (Immonen et al, 2020). Kumarasamy et al (2013) constructed conplastic rat strains using two common rat models for cardiovascular disease, in which the mtDNA of the Dahl salt-sensitive (S) rat was exchanged with the mtDNA of the spontaneously hypertensive rat (SHR) and vice versa.…”

“…Strains with concordant mitonuclear genomes exhibited increased relative fitness compared to strains with differing mitonuclear genomes. At colder temperatures, Brazilian and Yemen mitotypes introgressed with California nuclear genomes showed opposite effects in fitness, again suggesting that temperature contributes to mitonuclear effects on relative fitness ( Immonen et al, 2020 ).…”

Temperature-Specific and Sex-Specific Fitness Effects of Sympatric Mitochondrial and Mito-Nuclear Variation in Drosophila obscura

“…In this study, it is advocated that differences in protein interactions at varying temperatures are the reason why specific mito-nuclear combinations are favoured at a given temperature range. Oscillating temperature settings over space and time could act to maintain not only mitochondrial but mito-nuclear variation within populations, when this mtDNA × nuDNA × environment epistasis occurs [54].…”