Evolution of frugivory across a large radiation of non-seed-dispersing animals

Sridhar Halali, Dheeraj Halali, Henry Barlow, Jessie Pereira Santos Pereira Santos, Oskar Brattström, Ullasa Kodandaramaiah, Freerk Molleman, Christopher Wheat , André VL Freitas, Niklas Wahlberg

The origin of Angiosperm fleshy fruits, a novel nutritious resource, has led to the evolution of frugivory in a wide range of animals. While the (co)evolutionary dynamics between fruits and seed dispersers has received much attention, the evolution of frugivory in non-seed-dispersing animals remains overlooked. Here, we elucidate the macroevolution of frugivory in a large radiation of an insect, butterflies, by combining macroevolutionary analyses and field experiments. Our comparative analyses spanning 80 million years of evolution across Nymphalidae butterflies, the only family which feed on fermenting fruits, revealed that frugivory has deep origins ~60 million years ago and has evolved convergently from nectar-feeding lineages. Notably, ancestral state estimations indicate that the evolution of frugivory roughly coincides with the evolution of larger fleshy fruit sizes in Angiosperms. Our field experiments across the tropics further showed that frugivorous butterflies from diverse lineages have convergently evolved a strong preference for fermenting over fresh fruit bait, suggesting that the evolution of frugivory is associated with behavioural specialization. Together, our study shows that fleshy fruits likely created a new ecological opportunity that butterflies exploited and required behavioural specialization to exploit this novel resource.