Mitochondrial-Y chromosome epistasis in Drosophila melanogaster

Abstract

The coordination between mitochondrial and nuclear genes is crucial to eukaryotic organisms. Predicting the nature of these epistatic interactions can be difficult because of the transmission asymmetry of the genes involved. While autosomes and X-linked genes are transmitted through both sexes, genes on the Y chromosome and in the mitochondrial genome are uniparentally transmitted through males and females, respectively. Here, we generate 36 otherwise isogenic Drosophila melanogaster strains differing only in the geographical origin of their mitochondrial genome and Y chromosome, to experimentally examine the effects of the uniparentally inherited parts of the genome, as well as their interaction, in males. We assay longevity and gene expression through RNA-sequencing. We detect an important role for both mitochondrial and Y-linked genes, as well as extensive mitochondrial-Y chromosome epistasis. In particular, genes involved in male reproduction appear to be especially sensitive to such interactions, and variation on the Y chromosome is associated with differences in longevity. Despite these interactions, we find no evidence that the mitochondrial genome and Y chromosome are co-adapted within a geographical region. Overall, our study demonstrates a key role for the uniparentally inherited parts of the genome for male biology, but also that mito-nuclear interactions are complex and not easily predicted from simple transmission asymmetries.

Keywords: gene expression; longevity; sexual antagonism; uniparental inheritance.

Figure 1

Mean lifespan (days) ± standard error across 36 mito-Y combinations. Geographical origin of the mitochondrial genome is stated at the bottom and colour coded for the Y chromosome. Solid and dashed lines represent sympatric and novel mito-Y combinations, respectively. (Online version in colour.)

Figure 2.

Semantic clustering of over-represented biological process GO terms found among genes sensitive to mitochondrial haplotype. Each rectangle represents a single cluster, which are joined into larger ‘superclusters’ as visualized by colour. Size of the rectangles indicates p-value significance (absolute value of the log₁₀ transformed p-value). (Online version in colour.)

Figure 3.

Box and scatter plots visualizing differential expression of genes sensitive to (a) Y haplotype, (b) mitochondrial haplogroup and (c) mitochondrial-Y interactions. Normalized read counts for (a) Dup99B, a male sex peptide, which shows a reduced expression in the Netherlands haplotypes, (b) mt:COII, a mitochondrial subunit of cytochrome oxidase II, which shows variable expression across all six mitochondrial haplotypes, (c) Gβ76C, a Y-sensitive hit, linked to visual perception that shows significant differences in expression across all six Y haplotypes. (Online version in colour.)

Figure 4.

Expression profile of genes sensitive to mitochondrial-Y interactions. Samples (36 mito-Y combinations with two replicates, labelled A and B, for each) and genes of interest are listed along the x- and y-axis respectively. Colour indicates either overexpression (red) or underexpression (blue) compared to the mean expression level of that gene across all samples. (Online version in colour.)