Genetic Architecture of Metabolic Rate: Environment Specific Epistasis Between Mitochondrial and Nuclear Genes in an Insect

Abstract

The extent to which mitochondrial DNA (mtDNA) variation is involved in adaptive evolutionary change is currently being reevaluated. In particular, emerging evidence suggests that mtDNA genes coevolve with the nuclear genes with which they interact to form the energy producing enzyme complexes in the mitochondria. This suggests that intergenomic epistasis between mitochondrial and nuclear genes may affect whole-organism metabolic phenotypes. Here, we use crossed combinations of mitochondrial and nuclear lineages of the seed beetle Callosobruchus maculatus and assay metabolic rate under two different temperature regimes. Metabolic rate was affected by an interaction between the mitochondrial and nuclear lineages and the temperature regime. Sequence data suggests that mitochondrial genetic variation has a role in determining the outcome of this interaction.Our genetic dissection of metabolic rate reveals a high level of complexity, encompassing genetic interactions over two genomes, and genotype × genotype × environment interactions. The evolutionary implications of these results are twofold. First, because metabolic rate is at the root of life histories, our results provide insights into the complexity of life-history evolution in general, and thermal adaptation in particular. Second, our results suggest a mechanism that could contribute to the maintenance of nonneutral mtDNA polymorphism.K E Y W O R D S : Epistasis, life-history evolution, metabolism, mtDNA, polymorphism, thermal adaptation.

Population genetic structure of serotine bats (Eptesicus serotinus) across Europe and implications for the potential spread of bat rabies (European bat lyssavirus EBLV-1)

“…Similarly, one haplotype common to eastern England was also identified in a roost in the west, consistent with female dispersal and recruitment. However, the pattern of isolation by distance found over Europe suggests limits to female dispersal, although this could also reflect local selection for different haplotypes (Arnqvist et al, 2010;Balloux, 2010). Furthermore, no haplotypes are shared among continental sites.…”

Mitonuclear interactions: evolutionary consequences over multiple biological scales

“…Further compelling evidence for the profundity of mitonuclear interactions and their impact on key fitness traits comes from research in seed beetles [55,78] and yeast [79]. Arnqvist et al [78] generated 25 fully crossed mitonuclear genotypes, via introgressive backcrossing of mtDNA haplotypes sourced from five distinct populations into the nuclear backgrounds associated with the same five populations, and subsequently measured the carbon dioxide production under two different temperature regimes.…”

“…Arnqvist et al [78] generated 25 fully crossed mitonuclear genotypes, via introgressive backcrossing of mtDNA haplotypes sourced from five distinct populations into the nuclear backgrounds associated with the same five populations, and subsequently measured the carbon dioxide production under two different temperature regimes. While no overall differences in metabolic performance between mitochondrial haplotypes or nucleotypes were detected, complex gene-by-gene-byenvironment interactions existed in the form of mitonuclear interactions whose outcomes were thermally sensitive.…”

Mitochondrial-Nuclear Epistasis Contributes to Phenotypic Variation and Coadaptation in Natural Isolates of Saccharomyces cerevisiae

“…These interactions have been shown to have direct consequences on healthrelated and life-history phenotypes in several taxa. In insects such as Drosophila and Callosobruchus (seed beetle), exchanging mtDNA variants between distinct populations has led to lowered metabolic rate (Arnqvist et al 2010), decreased egg-to-adult survival (Dowling et al 2007a;Montooth et al 2010), and shortened life span (Clancy 2008;Zhu et al 2014). Interpopulation hybrids of the marine copepod Tigriopus suffered compromised oxidative phosphorylation (OXPHOS) capacities Burton 2006, 2008b) and reduced mitochondrial transcription (Ellison and Burton 2008a), most likely influenced by interactions between alleles of the nuclearencoded RNA polymerase and mtDNA variants (Ellison and Burton 2010).…”