Mitonuclear interactions and early-life diet shape adult nutritional behaviour

Mitochondrial function relies on close coordination between the
mitochondrial and nuclear genomes. Disruption to this coordination—via
mitonuclear mismatch—can impair metabolic efficiency, particularly under
energetically demanding conditions such as during development. The
nutritional environment further modulates mitochondrial demands,
suggesting that mitonuclear genotype and diet may interact to shape
life-history traits and behaviour. Here, we investigate how early-life
diet and mitonuclear genotype jointly influence development time, adult
body size, and nutritional preference in Drosophila melanogaster. Using a
full-factorial panel of putatively matched and mismatched combinations
(cybrids) of mitonuclear genotype derived from natural Australian
populations, we reared flies on diets varying in their ratio of
macronutrients and assessed how this influenced larval development and
subsequent adult diet preference. Developmental rate was significantly
influenced by mitonuclear coevolution and diet, with cybrids showing
delayed development under all conditions, with dietary extremes
exacerbating this effect. Despite this, egg-to-adult viability remained
unaffected. Adult nutritional behaviour exhibited clear genotype- and
diet-dependent effects. Flies reared on high-protein diets increased
carbohydrate intake as adults, while those reared on high-carbohydrate
diets increased protein intake, suggesting compensatory feeding responses.
Mitonuclear mismatch further modulated nutrient consumption, particularly
in females, whose carbohydrate intake was influenced by intergenomic
compatibility and early-life dietary conditions. Males’ protein
consumption was also impacted by mitonuclear coevolution across all
developmental diets. Finally, body size was also shaped by interactions
between mitonuclear genotype and diet. Together, our findings demonstrate
that mitonuclear compatibility and the composition of the early
nutritional environment interact to shape developmental and behavioural
phenotypes. These results support a role for mitonuclear coadaptation in
mediating metabolic plasticity, highlighting the evolutionary and
physiological significance of genotype-specific mitonuclear coordination.