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Systematic variations in microvilli banding patterns along fiddler crab rhabdoms

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Abstract

Polarisation sensitivity is based on the regular alignment of dichroic photopigment molecules within photoreceptor cells. In crustaceans, this is achieved by regularly stacking photopigment-rich microvilli in alternating orthogonal bands within fused rhabdoms. Despite being critical for the efficient detection of polarised light, very little research has focused on the detailed arrangement of these microvilli bands. We report here a number of hitherto undescribed, but functionally relevant changes in the organisation of microvilli banding patterns, both within receptors, and across the compound eye of fiddler crabs. In all ommatidia, microvilli bands increase in length from the distal to the proximal ends of the rhabdom. In equatorial rhabdoms, horizontal bands increase gradually from 3 rows of microvilli distally to 20 rows proximally. In contrast, vertical equatorial microvilli bands contain 15–20 rows of microvilli in the distal 30 µm of the rhabdom, shortening to 10 rows over the next 30 µm and then increase in length to 20 rows in parallel with horizontal bands. In the dorsal eye, horizontal microvilli occupy only half the cross-sectional area as vertical microvilli bands. Modelling absorption along the length of fiddler crab rhabdoms suggests that (1) increasing band length assures that photon absorption probability per band remains constant along the length of photoreceptors, indicating that individual bands may act as units of transduction or adaptation; (2) the different organisation of microvilli bands in equatorial and dorsal rhabdoms tune receptors to the degree and the information content of polarised light in the environment.

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Acknowledgments

We are grateful to Peter McIntyre, Sally Stowe, the ANU Electron Microscopy Unit and Willi Ribi for histological help and advice, and to Justin Marshall for comments on the manuscript. We thank Eric Warrant and a very constructive referee for their time to discuss absorption modelling and their help with designing it. The work was supported by a PhD scholarship from the Saudi Arabia Ministry of Education and a King Abdulaziz University travel grant for A.A., by an Asian Office of Aerospace Research and Development and Air Force Office of Scientific Research grant for M.J.H., and by the Australian Research Council Centre of Excellence in Vision Science for A.A. and J.Z.

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  1. Ali Alkaladi

    Present address: Department of Biological Sciences, Faculty of Science, King Abdulaziz University, North Campus, PO Box 11508, Jeddah, 21463, Saudi Arabia

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  1. ARC Centre of Excellence in Vision Science, Research School of Biology, Bld 46, The Australian National University, Canberra, ACT, 0200, Australia

    Ali Alkaladi & Jochen Zeil

  2. Queensland Brain Institute, University of Queensland, St Lucia, QLD, 4072, Australia

    Martin J. How

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Correspondence to Ali Alkaladi.

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Alkaladi, A., How, M.J. & Zeil, J. Systematic variations in microvilli banding patterns along fiddler crab rhabdoms. J Comp Physiol A 199, 99–113 (2013). https://doi.org/10.1007/s00359-012-0771-9

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