Patterning the insect eye

From stochastic to deterministic mechanisms

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

Research output: Contribution to journalArticle

Abstract

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.

Original languageEnglish
Article numbere1006363
JournalPLoS Computational Biology
Volume14
Issue number11
DOIs
Publication statusPublished - Nov 1 2018

Fingerprint

Patterning
Insects
eyes
Drosophilidae
insect
insects
Cellular automata
Stochastic models
Drosophila
Lenses
Dolichopodidae
Color
Specifications
Wavelength
Diptera
Retina
Unordered
Regulatory Networks
ommatidia
Cellular Automata

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Modelling and Simulation
  • Ecology
  • Molecular Biology
  • Genetics
  • Cellular and Molecular Neuroscience
  • Computational Theory and Mathematics

Cite this

Ebadi, H., Perry, M., Short, K., Klemm, K., Desplan, C., Stadler, P. F., & Mehta, A. (2018). Patterning the insect eye: From stochastic to deterministic mechanisms. PLoS Computational Biology, 14(11), [e1006363]. https://doi.org/10.1371/journal.pcbi.1006363

Patterning the insect eye : From stochastic to deterministic mechanisms. / Ebadi, Haleh; Perry, Michael; Short, Keith; Klemm, Konstantin; Desplan, Claude; Stadler, Peter F.; Mehta, Anita.

In: PLoS Computational Biology, Vol. 14, No. 11, e1006363, 01.11.2018.

Research output: Contribution to journalArticle

Ebadi, H, Perry, M, Short, K, Klemm, K, Desplan, C, Stadler, PF & Mehta, A 2018, 'Patterning the insect eye: From stochastic to deterministic mechanisms', PLoS Computational Biology, vol. 14, no. 11, e1006363. https://doi.org/10.1371/journal.pcbi.1006363
Ebadi H, Perry M, Short K, Klemm K, Desplan C, Stadler PF et al. Patterning the insect eye: From stochastic to deterministic mechanisms. PLoS Computational Biology. 2018 Nov 1;14(11). e1006363. https://doi.org/10.1371/journal.pcbi.1006363
Ebadi, Haleh ; Perry, Michael ; Short, Keith ; Klemm, Konstantin ; Desplan, Claude ; Stadler, Peter F. ; Mehta, Anita. / Patterning the insect eye : From stochastic to deterministic mechanisms. In: PLoS Computational Biology. 2018 ; Vol. 14, No. 11.
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