Parasitic gut infection causes functional and molecular resemblance of Libellula pulchella dragonfly flight muscle to skeletal muscle of obese vertebrates

Abstract

We previously demonstrated the existence of a naturally occurring, metabolic disease phenotype in Libellula pulchella dragonflies, that shows high similarity to vertebrate obesity and type II diabetes, and is caused by a protozoan gut parasite. To further mechanistic understanding of how this metabolic disease phenotype affects male L. pulchella fitness in vivo, we examined infection effects on in situ muscle performance- and molecular traits relevant to L. pulchella flight performance in nature. Importantly, these traits were previously shown to be affected in obese vertebrates. Similar to obesity effects in rat skeletal muscle, dragonfly gut infection caused a disruption of relationships between body mass, flight muscle power output and alternative pre-mRNA splicing of troponin T, a trait known to affect muscle calcium sensitivity and performance in insects and vertebrates. In addition, when simulated in situ to contract at cycle frequencies ranging from 20-45Hz, infected individuals' flight muscles displayed a left-shift in the power-cycle frequency curves, i.e., their optimal cycle frequency was significantly reduced. Interestingly, this left-shift resulted in power-cycle frequency curves that were similar to those produced by flight muscles of non-infected, teneral (i.e., physiologically immature) adult L. pulchella males. Overall, our results indicate that effects of metabolic disease on skeletal muscle physiology in natural insect systems are similar to those observed in vertebrates maintained in laboratory settings. More generally, they indicate that study of natural, host-parasite interactions can contribute important insight into how environmental factors other than diet and exercise may contribute to the development of metabolic disease phenotypes.