Constraints on the development and evolution of compound eyes in insects

Constraints, whether developmental, phylogenetic, or energetic, may limit or bias the direction of evolution, although empirical evidence of their effects is limited. The development and evolution of compound eyes are often said to be constrained by limits on size imposed by energetic requirements or space restrictions, both a function of body size. Such constraints presumably counter benefits stemming from improvements in visual system performance that come with increased eye size. Presented here are three studies that test the hypothesis that body size constrains peripheral visual system evolution and development in insects. The first is a phylogenetically-controlled survey of 24 butterfly species examining how eye anatomy, including facet diameter and interommatidial angle, vary with body size. Large species had larger facet diameters and smaller interommatidial angles, which indicate superior vision. However, size- independent sexual dimorphism in eye structure was widespread, which may reflect sexual differences in selection pressures on eye morphology. The second study investigated phenotypic and genotypic variation in eye morphology of the Orange Sulphur butterfly (Colias eurytheme) when subjected to a dietary manipulation. Variation in eye morphology, even after adjustment for body size, was heritable, but was also sensitive to food stress. Intake of low quality food resulted in smaller eyes and facet diameters, although there was evidence that food stressed animals increased investment in eye development to partially mitigate these declines. The final study was a selection experiment that disrupted the relationship between eye size and body size in Drosophila melanogaster. Captive lines selected for proportionally large eyes were expected to show reduced responses to selection due to hypothesized countervailing selection against large eye size. Instead, eye size responded to selection favoring large eyes at the same rate as selection favoring small eyes, indicating that body size did not absolutely constrain eye size. Nevertheless, there were subtle effects that were consistent with weak relative constraints from body size. The view emerging from this work is that body size does constrain eye size, but that selection favoring large eyes can overcome this constraint when the demands on visual performance are strong.