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.

Figure 1.—

Schematic of karyotypes for offspring of the 75 mt line × nuclear background crosses. Small circles, of different shades, within each eclipse indicate particular cyto/mito types. The first set of rectangles on the left side of the eclipse indicates the sex chromosomes: Y denotes the Y chromosome, and a rectangle the X chromosome. The three pairs of rectangles to the right of this are autosomes. The shading of all chromosomes indicates their origin: solid indicates random wild-type chromosomes from the base population and paler shades of three different intensities indicate chromosomes inherited from males of each of the three nuclear backgrounds. Thus, each offspring receives its cyto/mito type from its mt line of origin; 50% of its nuclear DNA is inherited from a specific, controlled nuclear background, while 50% represents random, wild-type nuclear DNA from the base population.

Figure 2.—

Interaction plot of adult female fitness for the 75 mt line × nuclear background combinations (cytonuclear genotypes) for each block. The substantial crossing over of the reaction norms illustrates that the relative order of fitness per cytonuclear genotype differs across blocks.

Figure 3.—

Cytonuclear effects on adult female fitness within each block. Interaction plots for each block of female fitness for the 25 mt lines expressed in three different nuclear genetic backgrounds. The substantial crossing over of reaction norms indicates that the relative order of fitness per mt line changes according to nuclear background: (a) block 1, (b) block 2, and (c) block 3.