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Expression of UV-, blue-, long-wavelength-sensitive opsins and melatonin in extraretinal photoreceptors of the optic lobes of hawkmoths

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Abstract

Lepidopterans display biological rhythms associated with egg laying, eclosion and flight activity but the photoreceptors that mediate these behavioural patterns are largely unknown. To further our progress in identifying candidate light-input channels for the lepidopteran circadian system, we have developed polyclonal antibodies against ultraviolet (UV)-, blue- and extraretinal long-wavelength (LW)-sensitive opsins and examined opsin immunoreactivity in the adult optic lobes of four hawkmoths, Manduca sexta, Acherontia atropos, Agrius convolvuli and Hippotion celerio. Outside the retina, UV and blue opsin protein expression is restricted to the adult stemmata, with no apparent expression elsewhere in the brain. Melatonin, which is known to have a seasonal influence on reproduction and behaviour, is expressed with opsins in adult stemmata together with visual arrestin and chaoptin. By contrast, the LW opsin protein is not expressed in the retina or stemmata but rather exhibits a distinct and widespread distribution in dorsal and ventral neurons of the optic lobes. The lamina, medulla, lobula and lobula plate, accessory medulla and adjacent neurons innervating this structure also exhibit strong LW opsin immunoreactivity. Together with the adult stemmata, these neurons appear to be functional photoreceptors, as visual arrestin, chaoptin and melatonin are also co-expressed with LW opsin. These findings are the first to suggest a role for three spectrally distinct classes of opsin in the extraretinal detection of changes in ambient light and to show melatonin-mediated neuroendocrine output in the entrainment of sphingid moth circadian and/or photoperiodic rhythms.

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Acknowledgements

We are grateful to Dr. Larry A. Donoso for the generous gift of a set of arrestin antibodies and peptides, to Dr. Joachim Schachtner for his gift of eggs of Manduca sexta, to Dr. Carol Gregorio for help with the antibody immunoaffinity purification and to Dr. Lisa Nagy for sponsoring us while the antibodies were being made. We also thank Angela Bruns and Claudia Obermeier for excellent rearing of our hawkmoth stocks. The monoclonal antibody 24B10 developed by Seymour Benzer was obtained from the Developmental Studies Hybridoma Bank developed under the auspices of the NICHD and maintained by the Department of Biological Sciences, University of Iowa, Iowa City, USA.

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  1. Institut für Zoologie 1, Universität Erlangen-Nürnberg, Staudtstr. 5, 91058, Erlangen, Germany

    Jochen Lampel & Lutz T. Wasserthal

  2. Comparative and Evolutionary Physiology Group, Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA

    Adriana D. Briscoe

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  1. Jochen Lampel
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Correspondence to Jochen Lampel.

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This work was partially supported by the Canadian Institute for Advanced Research (A.D.B.) and the National Science Foundation (grant nos. IBN-0082700 and IBN-0346765; A.D.B.).

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Lampel, J., Briscoe, A.D. & Wasserthal, L.T. Expression of UV-, blue-, long-wavelength-sensitive opsins and melatonin in extraretinal photoreceptors of the optic lobes of hawkmoths. Cell Tissue Res 321, 443–458 (2005). https://doi.org/10.1007/s00441-004-1069-1

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