Variation in mitochondrial DNA affects locomotor activity and sleep in Drosophila melanogaster

Abstract

Mitochondria are organelles that produce cellular energy in the form of ATP through oxidative phosphorylation, and this primary function is conserved among many taxa. Locomotion is a trait that is highly reliant on metabolic function and expected to be greatly affected by disruptions to mitochondrial performance. To this end, we aimed to examine how activity and sleep vary between Drosophila melanogaster strains with different geographic origins, how these patterns are affected by mitochondrial DNA (mtDNA) variation, and how breaking up co-evolved mito-nuclear gene combinations affect the studied activity traits. Our results demonstrate that Drosophila strains from different locations differ in sleep and activity, and that females are generally more active than males. By comparing activity and sleep of mtDNA variants introgressed onto a common nuclear background in cytoplasmic hybrid (cybrid) strains, we were able to quantify the among-line variance attributable to mitochondrial DNA, and we establish that mtDNA variation affects both activity and sleep, in a sex-specific manner. Altogether our study highlights the important role that mitochondrial genome variation plays on organismal physiology and behaviour.

Fig. 1. Locomotor activity and sleep in females and males of the coevolved and cybrid lines.

The total number of activity events recorded over three days in original (A) and cybrid (D) lines. The total number of activity events recorded when the flies were awake in original (B) and cybrid (E) lines. The proportion of time that flies were asleep, defined as 5 min of inactivity in original (C) and cybrid (F) lines. See Figs S1-S4 for individual actograms and boxplots for each line. See Table 1 for details of each line. See Table 2 for outputs of statistical models and Table S1 for random effect variance components.

Fig. 2. Haplogroup effect.

Locomotor activities and sleep in coevolved and cybrid females and males based on the mtDNA haplogroup division. A Total activity counts over three days. B Activity of the flies when awake. C The proportion of time the flies spent sleeping.

Fig. 3. A comparison of Coevolved and Novel Mito-nuclear associations.

A total number of activity events recorded over 3 days. B the total number of activity events recorded when flies were not asleep. C The proportion of time that flies were determined to be asleep, defined as 5 min of inactivity, See Table 2 for outputs of statistical models.