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Patterning the insect eye: from stochastic to deterministic mechanisms

Ebadi, Haleh; Perry, Michael; Short, Keith; Klemm, Konstantin; Desplan, Claude; Stadler, Peter F.; Mehta, Anita
, (2017)

While most processes in biology are highly deterministic, stochastic mechanisms are sometimes used to increase cellular diversity, such as in the specification of sensory receptors. In the human and Drosophila eye, photoreceptors sensitive to various wavelengths of light are distributed randomly across the retina. Mechanisms that underlie stochastic cell fate specification have been analysed in detail in the Drosophila retina. In contrast, the retinas of another group of dipteran flies exhibit highly ordered patterns. Species in the Dolichopodidae, the "long-legged" flies, have regular alternating columns of two types of ommatidia (unit eyes), each producing corneal lenses of different colours. Individual flies sometimes exhibit perturbations of this orderly pattern, with "mistakes" producing changes in pattern that can propagate across the entire eye, suggesting that the underlying developmental mechanisms follow local, cellular-automaton-like rules. We hypothesize that the regulatory circuitry patterning the eye is largely conserved among flies such that the difference between the Drosophila and Dolichopodidae eyes should be explicable in terms of relative interaction strengths, rather than requiring a rewiring of the regulatory network. We present a simple stochastic model which, among its other predictions, is capable of explaining both the random Drosophila eye and the ordered, striped pattern of Dolichopodidae.