Impact of mitonuclear interactions on life-history responses to diet

Abstract

Mitochondria are central to both energy metabolism and biosynthesis. Mitochondrial function could therefore influence resource allocation. Critically, mitochondrial function depends on interactions between proteins encoded by the mitochondrial and nuclear genomes. Severe incompatibilities between these genomes can have pervasive effects on both fitness and longevity. How milder deficits in mitochondrial function affect life-history trade-offs is less well understood. Here, we analyse how mitonuclear interactions affect the trade-off between fecundity and longevity in Drosophila melanogaster. We consider a panel of 10 different mitochondrial DNA haplotypes against two contrasting nuclear backgrounds (w¹¹¹⁸ (WE) and Zim53 (ZIM)) in response to high-protein versus standard diet. We report strikingly different responses between the two nuclear backgrounds. WE females have higher fecundity and decreased longevity on high protein. ZIM females have much greater fecundity and shorter lifespan than WE flies on standard diet. High protein doubled their fecundity with no effect on longevity. Mitochondrial haplotype reflected nuclear life-history trade-offs, with a negative correlation between longevity and fecundity in WE flies and no correlation in ZIM flies. Mitonuclear interactions had substantial effects but did not reflect genetic distance between mitochondrial haplotypes. We conclude that mitonuclear interactions can have significant impact on life-history trade-offs, but their effects are not predictable by relatedness. This article is part of the theme issue 'Linking the mitochondrial genotype to phenotype: a complex endeavour'.

Keywords: fecundity; life-history trade-off; longevity; mitonuclear interactions; nutrition; resource allocation.

Figure 1.

Schematic showing how mitochondrial function might affect resource allocation: (a) mitonuclear incompatibilities force a shift in resource allocation towards either fecundity or longevity, giving a negative correlation between these fitness components; or (b) the null hypothesis: if mitonuclear incompatibilities undermine mitochondrial function but resource allocation is unchanged, then both fecundity and longevity would be suppressed, generating a positive correlation in which better mitochondrial function increases both fecundity and lifespan.

Figure 2.

Mean longevity estimates across all experimental treatments. (a) Female estimates and (b) male survival estimates. Within each sex, we show the mean longevity for the ZIM (blue) and WE (red) nuclear background for both diet treatments.

Figure 3.

Total number of eggs (mean ± s.e.) produced by a single female across five timepoints. Fecundity measures were obtained for each mito-nuclear combination and both diets (ST, standard; PRO, high-protein).

Figure 4.

Longevity versus fecundity relationship across all treatments. Correlations within each nuclear genotype are highlighted with each datapoint being a mitonuclear genotype. Black datapoints denote genotypes that are coevolved (WE_nu–WE_mt, ZIM_nu–ZIM_mt).