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Compound eyes and retinal information processing in miniature dipteran species match their specific ecological demands

Gonzalez-Bellido, P.T., Wardill, T.J. and Juusola, M. (2011) Compound eyes and retinal information processing in miniature dipteran species match their specific ecological demands. Proceedings of the National Academy of Sciences of the United States of America, 108 (10). pp. 4224-4229. ISSN 0027-8424

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The compound eye of insects imposes a tradeoff between resolution and sensitivity, which should exacerbate with diminishing eye size. Tiny lenses are thought to deliver poor acuity because of diffraction; nevertheless, miniature insects have visual systems that allow a myriad of lifestyles. Here, we investigate whether size constraints result in an archetypal eye design shared between miniature dipterans by comparing the visual performance of the fruit fly Drosophila and the killer fly Coenosia. These closely related species have neural superposition eyes and similar body lengths (3 to 4 mm), but Coenosia is a diurnal aerial predator, whereas slow-flying Drosophila is most active at dawn and dusk. Using in vivo intracellular recordings and EM, we report unique adaptations in the form and function of their photoreceptors that are reflective of their distinct lifestyles. We find that although these species have similar lenses and optical properties, Coenosia photoreceptors have three-to fourfold higher spatial resolution and rate of information transfer than Drosophila. The higher performance in Coenosia mostly results from dramatically diminished light sensors, or rhabdomeres, which reduce pixel size and optical cross-talk between photoreceptors and incorporate accelerated phototransduction reactions. Furthermore, we identify local specializations in the Coenosia eye, consistent with an acute zone and its predatory lifestyle. These results demonstrate how the flexible architecture of miniature compound eyes can evolve to match information processing with ecological demands.

Item Type: Article
Copyright, Publisher and Additional Information: © 2011 National Academy of Science. This is an author produced version of a paper subsequently published in Proceedings of the National Academy of Science and the United States of America. Uploaded in accordance with the publisher's self-archiving policy.
Keywords: vision; predatory behavior; invertebrate; evolution
Institution: The University of Sheffield
Academic Units: The University of Sheffield > Faculty of Science (Sheffield) > School of Biological Sciences (Sheffield) > Department of Biomedical Science (Sheffield)
Depositing User: Miss Anthea Tucker
Date Deposited: 25 Mar 2011 11:47
Last Modified: 25 Mar 2011 11:47
Published Version: http://dx.doi.org/10.1073/pnas.1014438108
Status: Published
Publisher: National Academy of Sciences
Identification Number: 10.1073/pnas.1014438108
URI: http://eprints.whiterose.ac.uk/id/eprint/42916

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