Investments in photoreceptors compete with investments in optics to determine eye design.

Abstract

Eyes provide opportunities to understand the function, design, development, and evolution of elaborate sense organs. We take a new cost-benefit approach to understanding eye design by considering that optics and photoreceptors compete for the resources invested in an integrated system. We investigate this competition theoretically and empirically using a new measure of cost, specific volume. This common currency for optics and photoreceptors relates investments to image quality via geometrical, optical, and physiological constraints. By covering the morphospace of an eye of given type and cost, we model how trading optics against photoreceptors changes information capacity. In apposition compound eyes and simple eyes, an optimum configuration maximises efficiency. Efficiency requires heavy investment in photoreceptors and depends on photoreceptor energy consumption. Optimum information capacities and efficiencies scale non-linearly with total investment. Diurnal insects' apposition eyes follow trends that promote efficiency: photoreceptor arrays take 40-80% of total specific volume, photoreceptor length increases systematically with spatial resolution, and photoreceptors are exceptionally long. Thus, competition between optics and photoreceptors shapes eye design, and matching investments in optics and photoreceptors to improve efficiency is a design principle. Our new methodology can be developed to view the adaptive radiation of eyes through a cost-benefit lens.