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

Because an animal invests in an eye’s optics and photoreceptor array to meet behavioural needs at minimum cost, optics and photoreceptors compete for resources to maximise eye performance. This competition has not previously been investigated. Its outcome depends on the relative costs and benefits of investing space, materials and energy in optics and photoreceptors. We introduce a measure of cost, specific volume in µm³sr⁻¹, which relates to performance via optical, physiological and geometrical constraints. We model apposition compound eyes and simple (camera type) eyes to calculate the performance surface across the morphospace of eyes of given type and total cost. This surface identifies the allocation of resources that maximises efficiency and shows how efficiency reduces as eye morphology departs from optimum. Using published data, we calculate specific volumes to estimate the investments in optics and photoreceptors that insects make, and compare these with our models. We find that efficient allocation can explain three robust trends: fast flying diurnal insects allocate>50% of eye volume to photoreceptor arrays, their photoreceptors’ photosensitive waveguides (rhabdomeres, rhabdoms) are much longer than simple eyes’, and length increases systematically with spatial resolution. We conclude that photoreceptor costs often equal or exceed optical costs, therefore competition between optics and photoreceptors for resources is a major factor in eye design, and matching investments in optics and photoreceptors to maximise efficiency is a design principle. Our methodology can be developed to view the adaptive radiation of eyes through a cost:benefit lens.