Intergenomic Epistasis for Fitness: Within-Population Interactions Between Cytoplasmic and Nuclear Genes in Drosophila melanogaster

Abstract

The symbiotic relationship between the mitochondrial and nuclear genomes coordinates metabolic energy production and is fundamental to life among eukaryotes. Consequently, there is potential for strong selection to shape interactions between these two genomes. Substantial research attention has focused on the possibility that within-population sequence polymorphism in mitochondrial DNA (mtDNA) is maintained by mitonuclear fitness interactions. Early theory predicted that selection will often eliminate mitochondrial polymorphisms. However, recent models demonstrate that intergenomic interactions can promote the maintenance of polymorphism, especially if the nuclear genes involved are linked to the X chromosome. Most empirical studies to date that have assessed cytonuclear fitness interactions have studied variation across populations and it is still unclear how general and strong such interactions are within populations. We experimentally tested for cytonuclear interactions within a laboratory population of Drosophila melanogaster using 25 randomly sampled cytoplasmic genomes, expressed in three different haploid nuclear genetic backgrounds, while eliminating confounding effects of intracellular bacteria (e.g., Wolbachia). We found sizable cytonuclear fitness interactions within this population and present limited evidence suggesting that these effects were sex specific. Moreover, the relative fitness of cytonuclear genotypes was environment specific. Sequencing of mtDNA (2752 bp) revealed polymorphism within the population, suggesting that the observed cytoplasmic genetic effects may be mitochondrial in origin.

Population structure and connectivity in Indo-Pacific deep-sea mussels of the Bathymodiolus septemdierum complex

“…Variation at the two protein-coding mitochondrial markers, ND4 and COI, appeared to be shaped by negative selective forces, as expected for a rapidly evolving clonal genome that is susceptible to an accumulation of slightly deleterious mutations (i.e., Muller's ratchet; reviewed in Stewart and Larsson 2014). Although purifying selection appears to be contradictory to the observed levels of polymorphism, mtDNA variation might be maintained due to increased mutation rates (Brown et al 1979), co-evolution with the nuclear genome (Dowling et al 2007) or doubly uniparental inheritance, which is known to occur in some mytilid species (Zouros et al 1994;Skibinski et al 1994;Hoeh et al 1996;Zouros 2013). Interestingly, the mitochondrial tRNAs showed contrasting results concerning the Indo-Pacific divergence.…”

Epigenetics and its implications for behavioral neuroendocrinology

“…Using populations of the seed beetle fixed for their cytoplasmic and nuclear lineages, Dowling et al [30] established that the effects of temperature, which dictates the rate of development in this species, and hence on fitness, are different in specific mito-nuclear genetic combinations. Studies similar to those with the seed beetle have been performed with Drosophila and demonstrate that the relative contributions of the mitochondrial and nuclear genomes in metabolic energy production can be manipulated; measurements of mito-nuclear fitness suggest both sex and environment specific effects due to mitochondrial polymorphisms [67,32].…”

“…Although the individual's capacity to respond to environmental change or insult with heritable phenotypic variation at a later stage is possible, it is during this early period that hormones and genotype predispose an individual's responses to future experiences throughout the life cycle as well as the susceptibility to developing disorders (e.g., [8,9,32,38,48,59]). Obviously, suites of genes underlie the fundamental plasticity of an organism, particularly during development or life history transitions.…”

Effect of intracellular Wolbachia on interspecific crosses between Drosophila melanogaster and Drosophila simulans

“…The different effects of infection in homospecific crosses in both species may be due to the interaction between the genomes of the parasite and the host (Reynolds et al, 2003;Dean, 2006;Dowling et al, 2007;Iturbe-Ormaetxe and O'Neill, 2007;Yamada et al, 2007;Xi et al, 2008). The genome of Drosophila plays an important role in the response to the effect of the bacterium on changes in biological efficacy, as has been shown by several authors (Fry and Rand, 2002;Charlat et al, 2003;McGraw and O'Neill, 2004).…”

“…Other authors conjecture about the interactions between the host-symbiont genotypes, and the combination of environmental and physiological factors to determine the positive or negative effects of infection and to explain the phenotypic variability of CI from homospecific crosses (Reynolds et al, 2003;Dean, 2006;Dowling et al, 2007;Iturbe-Ormaetxe and O'Neill, 2007;Yamada et al, 2007;Xi et al, 2008).…”