An elongated lifespan is associated with higher oxidative protection of flight tissue in Heliconiini butterflies

Abstract

Evolutionary theories of ageing often invoke trade-offs in resource allocation between somatic maintenance and other important physiological functions. One proposed mechanistic mediator of these trade-offs is oxidative stress, which arises from an imbalance between an organism's production of reactive oxygen species and its ability to detoxify them. Accordingly, many long-lived species across the animal kingdom show evidence for resistance to oxidative stress. However, it can be difficult to associate lifespan differences with oxidative phenotypes when comparing species across wide taxonomic distances, which may also show large differences in physiology. Butterflies in the long-lived Heliconius genus show a 3-fold lifespan extension and slowed ageing in comparison with their close relatives in the Heliconiini tribe, to whom they are phylogenetically, ecologically, and physiologically similar. However, proximate explanations for this extended longevity are currently lacking. Here, we leverage the neat comparative framework between Heliconius hecale and Dryas iulia, a shorter-lived Heliconiini outgroup, to test whether the observed lifespan differences between the two species are associated with differences in oxidative physiology. Our findings suggest superior oxidative protection of thoracic tissue in the longer-lived H. hecale compared to D. iulia, as evidenced by increased superoxide dismutase activity, increased total antioxidant capacity, and a corresponding reduction in lipid peroxidation in this tissue. Considering the metabolic demands of insect flight, we suggest that this oxidative phenotype may contribute to the extended longevity of Heliconius by enhancing protection of thoracic tissues against oxidative damage, representing a plausible proximate pro-longevity mechanism in this genus.