Allometry and shared ancestry, rather than ecology, shapes the evolution of 3D eye size in temperate butterflies

Sridhar Halali, Stephen A Hall , Lars B Pettersson, Romain Carrié, Paul Caplat, Emily Baird, Niklas Wahlberg

Sensory traits shape animal lifestyles due to the central role they play in retrieving and processing environmental information. However, being some of the most energetically expensive tissues to build and maintain, ecological demands often modulate investment in these organs. Evidence that ecology shapes the evolution of sensory traits is plenty but is heavily biased towards vertebrates and has only recently begun to emerge in invertebrates. Here, we elucidate the macroevolution of a key sensory organ – eye size – using temperate butterflies as models. Using micro-CT X-ray imaging of pinned museum specimens, we quantified the eye size of 444 individuals comprising 59 species. Further, using 12 years of long-term monitoring data to quantify species habitat preferences, we tested the hypothesis that forest-associated species, likely experiencing dimmer light conditions, should have larger eyes
than those from open habitats. Our comparative analyses revealed tight allometric scaling between eye and wing size, and phylogeny alone explained 74% of eye size variation, with low heterogeneity in the evolutionary rates. Further, we found that habitat structure and a behavioural trait, male mate location strategy, had no association with eye size. Overall, allometry and shared ancestry, not ecology, shape the macroevolution of eye size in temperate butterflies and demonstrate how non-invasive microCT imaging can be used on pinned museum specimens for studying phenotypic evolution.