Evolutionary implications of mitochondrial genetic variation: mitochondrial genetic effects on OXPHOS respiration and mitochondrial quantity change with age and sex in fruit flies

Abstract

The ancient acquisition of the mitochondrion into the ancestor of modern-day eukaryotes is thought to have been pivotal in facilitating the evolution of complex life. Mitochondria retain their own diminutive genome, with mitochondrial genes encoding core subunits involved in oxidative phosphorylation. Traditionally, it was assumed that there was little scope for genetic variation to accumulate and be maintained within the mitochondrial genome. However, in the past decade, mitochondrial genetic variation has been routinely tied to the expression of life-history traits such as fertility, development and longevity. To examine whether these broad-scale effects on life-history trait expression might ultimately find their root in mitochondrially mediated effects on core bioenergetic function, we measured the effects of genetic variation across twelve different mitochondrial haplotypes on respiratory capacity and mitochondrial quantity in the fruit fly, Drosophila melanogaster. We used strains of flies that differed only in their mitochondrial haplotype, and tested each sex separately at two different adult ages. Mitochondrial haplotypes affected both respiratory capacity and mitochondrial quantity. However, these effects were highly context-dependent, with the genetic effects contingent on both the sex and the age of the flies. These sex- and age-specific genetic effects are likely to resonate across the entire organismal life-history, providing insights into how mitochondrial genetic variation may contribute to sex-specific trajectories of life-history evolution.

The Cytoplasm Affects the Epigenome in Drosophila melanogaster

“…Cyto-nuclear interactions are, therefore, part of the inheritance system in D. melanogaster. A haplotype-specific influence of mitochondrial metabolism on nuclear gene expression has been outlined for ageing, cancer, and other diseases [9] as well as for evolutionary processes [18,20,22,34]. Our study now indicates that cytoplasmatically mediated modifications of the nuclear epigenome should also be considered as possible regulators of these effects on downstream components of health [12,[29][30][31].…”

“…2 of 11 Mitochondrial genomes have been widely reported to interact with nuclear genomes to affect phenotypic expression [6][7][8][9][10][11][12][13][14][15][16][17]. Nuclear and mitochondrial genomes also routinely coevolve within populations as suggested from studies reporting hybrid disadvantages observed when coadapted combinations of mito-nuclear genotypes have been experimentally disrupted by placing the mt genotype of one population alongside the nuclear genome of another population [13,[18][19][20]. Mito-nuclear interactions, therefore, are part of the same inheritance system.…”

Perpendicular axes of differentiation generated by mitochondrial introgression

“…The strong fitness consequences of mitochondrial DNA variation (Wolff et al . ) are likely to be amplified through mitonuclear co‐evolution of essential metabolic and physiological functions (Bar‐Yaacov et al . ; Deremiens et al .…”

Sex-specific mitonuclear epistasis and the evolution of mitochondrial bioenergetics, ageing, and life history in seed beetles

“…Assays of the energy‐producing reactions of the ETC can therefore be used to provide mechanistic and biochemical links between genotypes and life‐history phenotypes (Das ; Ballard and Melvin ; Ballard and Pichaud ; Wolff et al. ).…”