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Toward Unraveling the Mystery of How the Unusual Principal Eyes of Thermonectus Marmoratus Larvae Work – Constructing a First Functional Model

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Toward Unraveling the Mystery of How the Unusual Principal Eyes of Thermonectus Marmoratus Larvae Work – Constructing a First Functional Model Toward unraveling the mystery of how the unusual principal eyes of Thermonectus marmoratus larvae work – constructing a first functional model. A dissertation submitted to the Division of Research and Advanced Studies of the University of Cincinnati In partial fulfillment of the requirements for the degree of Doctorate of Philosophy (Ph.D.) In the department of Biological Sciences of the College of Arts and Sciences 2013 by Annette Stowasser B.S., Xavier University, Cincinnati 2007 Committee Chair: Elke K. Buschbeck, Ph.D. 1 Abstract One might ask what one could possibly gain from exploring the function of tiny larval eyes? And one might answer that an exploration of the structure of such eyes and of the mechanical properties that evolved under their taxing size constraints has already served to inspire engineers in devising novel methods of navigation and visual task performance in robots. Moreover, an exploration of their specializations has also served to facilitate the study of very particular aspects of vision that can be found across many other species, including vertebrate animals and humans. Thus far, attention has been largely focused on adult compound eyes, but invertebrates also have chambered eyes, which should probably merit no less attention. Contrary to what is generally thought about these eyes, some of these visual systems are highly developed and complex. They too may result in the discovery of novel visual mechanisms, which may also serve to inspire engineers or to provide us with a more complete understanding of vision as well as of the evolution and development of eyes in general. Among the most interesting of these eyes are the principal eyes, E1 and E2, of Thermonectus marmoratus (Coleoptera:Dytiscidae) larvae. In previous studies of the behavior of these larvae, the anatomy of their eyes, the spectral sensitivity of their retinas and the ultrastructure of the retina of their principal eyes, their visual system have been shown to be unlike any other known eyes. They are unique in that they are tubular in shape and have a very complex layered retina in which the photoreceptor cells of the proximal retina (PR) are sensitive to UV light while those of the distal retina (DR) are sensitive to green light. The DR consists of many layers of photoreceptor cells 2 whose rhabdomeric portions are oriented perpendicular to the light path. Additionally, the retina is linear with a visual field that is a horizontal stripe. Due to the highly unusual construction of these eyes, some of the results were hard to interpret and raised additional questions as to how these eyes actually functioned in the context of both the behavior of the larvae and the visual challenges with which they were faced. For the purposes of this dissertation, a series of experiments was carried out to address the questions raised by the aforesaid past results and to elaborate a first conceptual model of how these eyes might function (Chapter 5). To that end, the optical properties of the lenses of these eyes were measured in order to ascertain where images are focused within these eyes, based on object distance and the spectral sensitivity of the retina (Chapter 2 and 4). The polarization sensitivity of the proximal retina was also measured (Chapter 3) for confirmation of its polarization sensitivity as suggested by the ultrastructure of its cells. 3 Copyright and Reproduction Articles in Current Biology (Chapter 2) Authors’ rights: “include the article in full or in part in a thesis or dissertation (provided that this is not to be published commercially)” Cell Press 600 Technology Square Cambridge, MA 02139 Phone: 1-617-661-7057 Fax: 1-617-661-7061 [email protected] Articles in The Journal of Experimental Biology (Chapter 3) Author rights: (these rights are retained when publishing an Open Access article) Authors remain the owners of the copyright to the article and retain the following non-exclusive rights (for further details, please refer to the licence agreement that accompanies article proofs): “(1) authors may reproduce the article, in whole or in part, in any printed book (including thesis) of which they are author, provided the original article is properly and fully attributed” The Journal of Experimental Biology The Company of Biologists Limited, Bidder Building, 140 Cowley Rd, Cambridge, CB4 0DL, UK Tel: +44 1223 425525 Fax: +44 1223 423520 [email protected] 4 Acknowledgements I very much wish to thank my advisor, Elke K. Buschbeck, and my committee members, Dr. Tiffany Cook, Dr. Edwin R. Griff, Dr. George W. Uetz and Dr. John E. Layne, for their academic support in this project, which was so perfectly suited to my passion for puzzles – especially those in which it is a wonder how the pieces ever fit together. I also wish to thank my advisors, Dr. Elke K. Buschbeck and Dr. John E. Layne, for their very special support in personal matters, support well in excess of anything that I had a right to expect. I thank the Buschbeck and the Layne lab groups as well as Dr. Ilya Vilinsky for helpful discussion; and, again, Dr. John E. Layne, for having lent me various lab equipment that included a rotating arm, camera, goniometer and still other things too numerous to mention. I thank Marisano J. James for his help in editing the polarization sensitivity manuscript. I thank Randy Morgan and the Cincinnati Zoo & Botanical Gardens for providing the original population of Sunburst Diving Beetles; Shannon Werner and Emily Jennings for their help in beetle care. I thank Doug J. Kohls, and Necati Kaval for providing technical assistance with scanning electron microscope imaging; Birgit Ehmer for her help with confocal and TEM imaging; and Peter Müller for helpful tips regarding the laser method. I also thank the anonymous reviewers who provided valuable comments that greatly improved the manuscripts. I offer a very special and heartfelt thanks to the families Wolfley, Hunt and Simerlink. This project would never have been completed without them as it would have been impossible for someone in my position—a single mother and graduate student with no extended family for support—to manage all my personal, professional 5 and academic obligations. They were there to help my children whenever I could not, knowing that I might never be able to repay them in kind. Another person who helped in invaluable ways was Rick Johnson. He took an enormous load off my shoulders when he undertook, of his own unprompted accord, to make sure that my son stayed on track at school during the last, busiest and most critical half-year of my project. Many thanks also go to Lauren Simerlink, Edwin Hunt, Nadja, and Heiko Stowasser (high school students or soon to be college freshmen) for having spent countless hours proofreading and participating in helpful discussions. Their expertise and keenness for a real taste of what awaits them in the future was most impressive. In this context I also would like to thank John Galvin very much for a final proofreading of this document. Finally, there is no way to thank my children Nadja and Heiko Stowasser enough for all their understanding, patience and help, and I apologize with all my heart for not having always been the mother I had originally so much wanted to be. All scientists—but biologists in particular—should probably stop, from time to time, and remark on how rare is life in the universe. In that spirit, I wish to thank my larvae for their sacrifice. However small and uncomprehending they were, they were precious life and little heroes to my cause. Funding This work was supported by the National Science Foundation under grants IOS0545978 and IOS1050754 and a University Research Council summer graduate fellowship to AS. 6 Contents List of Abbreviations ................................................................................................................ 10 Chapter 1: Introduction ............................................................................................................ 11 Introducing Sunburst diving beetles ..................................................................................... 14 What we need to know to understand how an eye works ..................................................... 15 The visual system of T. marmoratus – past results and the subjects of this dissertation .... 17 Anatomy .......................................................................................................................... 18 Spectral sensitivity ......................................................................................................... 20 Ultrastructure of the retina and polarization sensitivity .................................................... 23 Hunting behavior ............................................................................................................. 27 Range finding mechanisms ............................................................................................. 28 Optical properties of the lenses of E1 and E2 ................................................................. 29 Chapter 2: Biological bifocal lenses with image separation ................................................ 33 Summary .............................................................................................................................. 34 Results and Discussion ........................................................................................................ 35 Sunburst Diving Beetle Larvae Have Tubular Eyes with Two Retinas ........................... 35 Two
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