Patterning the insect eye: From stochastic to deterministic mechanisms

While most processes in biology are highly deterministic, stochastic mechanisms are sometimes used to increase cellular diversity. In human and Drosophila eyes, photoreceptors sensitive to different wavelengths of light are distributed in stochastic patterns, and one such patterning system has been analyzed in detail in the Drosophila retina. Interestingly, some species in the dipteran family Dolichopodidae (the “long legged” flies, or “Doli”) instead exhibit highly orderly deterministic eye patterns. In these species, alternating columns of ommatidia (unit eyes) produce corneal lenses of different colors. Occasional perturbations in some individuals disrupt the regular columns in a way that suggests that patterning occurs via a posterior-to-anterior signaling relay during development, and that specification follows a local, cellular-automaton-like rule. We hypothesize that the regulatory mechanisms that pattern the eye are largely conserved among flies and that the difference between unordered Drosophila and ordered dolichopodid eyes can be explained in terms of relative strengths of signaling interactions rather than a rewiring of the regulatory network itself. We present a simple stochastic model that is capable of explaining both the stochastic Drosophila eye and the striped pattern of Dolichopodidae eyes and thereby characterize the least number of underlying developmental rules necessary to produce both stochastic and deterministic patterns. We show that only small changes to model parameters are needed to also reproduce intermediate, semi-random patterns observed in another Doli species, and quantification of ommatidial distributions in these eyes suggests that their patterning follows similar rules.[Author summary] A simple model is able to account for a diversity of photoreceptor patterns in different fly species, ranging from highly deterministic to fully random.This work was supported in part by German research foundation STA 850/15-1 to PFS, NIH (grant R01 EY13010) to CD, NIH grant K99 EY027016 to MP Ministerio de Economía, Industria y Competitividad http://www.mineco.gob.es/ through the Ramón y Cajal program and through project SPASIMM, FIS2016-80067-P (AEI/FEDER, EU) to KK.Peer reviewe