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University of Cincinnati UNIVERSITY OF CINCINNATI Date: 13-Aug-2010 I, Srdjan Maksimovic , hereby submit this original work as part of the requirements for the degree of: Doctor of Philosophy in Biological Sciences It is entitled: Unusual eye design: The compound-lens eyes of Strepsiptera and the scanning eyes of Sunburst Diving Beetle larvae Student Signature: Srdjan Maksimovic This work and its defense approved by: Committee Chair: Elke Buschbeck, PhD Elke Buschbeck, PhD 9/28/2010 1,046 Unusual eye design: The compound-lens eyes of Strepsiptera and the scanning eyes of Sunburst Diving Beetle larvae 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 2010 by Srdjan Maksimovic B.S., University of Belgrade, 2001 Committee Chair: Elke K. Buschbeck, Ph.D. Abstract The majority of investigated eyes describe specific variations of known eye types. But the eyes of two different insects, the compound-lens eyes of Strepsiptera and the scanning eyes of dytiscid diving beetle larvae, do not follow known design principles. Most adult insects possess a pair of large compound eyes, often occupying significant portion of their head. Compound eyes are typically composed of hundreds to thousands of ommatidia, each containing 8-10 photoreceptors. For the most part the receptors within each ommatidium act as a single sampling unit, averaging light intensities within all of them. Males of the insect order Strepsiptera are different: their eyes are composed of a smaller number of relatively large units (eyelets), each with an extended retina with often more than one hundred photoreceptors. In the strepsipteran species, Xenos peckii, each eye has about 50 eyelets. By using a behavioral paradigm based on the optomotor response, I have provided evidence that the eyelets in Xenos peckii eyes are image forming units. Each eyelet could sample up to 13 points, as opposed to one sampling point in an ommatidium. This unusual design has already inspired engineers to apply it into artificial optical solutions, such as a compact infra-red camera. Like strepsipteran eyes, the principal eyes of the Sunburst Diving Beetle (Thermonectus marmoratus) larvae are among the most bizarre in the animal kingdom. There are three different larval instars, all of which bear six eyes (stemmata) on each side of their head. The two frontal pairs, known as the principal eyes, are used to scan potential prey prior to capture. The principal eyes form long tubes, have bifocal lenses and are characterized by at least two one-dimensional retinas at their ends: a deep distal retina closer to the lens, and a proximal retina that lies directly underneath. The distal retina expresses long-wavelength iii opsin (TmLW) mRNA, whereas the proximal retina expresses ultraviolet opsin (TmUV II) mRNA. In contrast to third instars, the proximal retina of first instars shows a weak expression of the TmUV I mRNA limited only to its dorsal half. Third instars lack expression of TmUV I mRNA in their proximal retina. By using intracellular recordings from photoreceptor cells in third instars, I have shown that the distal retina has maximum sensitivity in green (LW), approximately 520-540 nm with an addition of a smaller peak in ultra-violet (UV), around 340-360 nm. The proximal retina is UV-sensitive with peak absorbance at 374 nm. This arrangement, to my knowledge, is the first example of a tiered system with the LW-sensitive cells distal to the UV-sensitive cells. Perhaps this unusual spectral arrangement creates a novel contrast enhancement mechanism. It is still unknown if these animals are capable of color and polarization sensitivity, and both of these visual modalities, including monochromatic vision, can be affected by the strange placement of the distal and proximal retina. Additional optical, physiological and behavioral studies will be necessary to answer these questions. iv Copyright and reproduction Articles in JEB are published under an exclusive, worldwide licence granted to the publisher by the authors, who retain copyright. 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; (2) authors and any academic institution where they are employed may reproduce the article, in whole or in part, for the purpose of teaching students; (3) authors may post a copy of the article on their website, provided that it has already been published by the journal and is linked to the journal’s website at http://jeb.biologists.org; (4) authors may use data contained in the article in other works they create; 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] v Acknowledgements There are many people, without whom, this research would not be possible. First, I would like to thank my research advisor, Dr. Elke Buschbeck, who has been a wonderful and understanding mentor. Many thanks for her generous support and interest in my work, yet hands-off approach to overseeing my research. With her friendship and accessibility to her students, she serves as an example of a great advisor. I also would like to thank my committee members: Dr. John Layne, for helping me with the complex computational world of visual processing; Dr. Tiffany Cook, for introducing me to the remarkable molecular techniques used in vision science; Drs. Bruce Jayne and Ali Minai, who paid critical attention and helped me determine the course of my research. Special thanks to Dr. Stephanie Rollmann for letting me use her lab and equipment, and for her help and advice whenever I needed one. I also would like to thank Drs. Ilya Vilinsky and Edwin Griff , for showing a deep interest and understanding of my research. My thanks also extend to people who have become my friends and colleagues as we worked side by side, trying to make the best of our time. Special thanks go to Nadine Stecher, Premraj Rajkumar, Annette Stowsser, Sri Pratima Nandamuri, Shannon Werner, Jessie Ebie, Karunyakanth Mandapaka and many others who made graduate school more interesting and at times very amusing. My deepest love and appreciation go to my parents, Slavko and Cvijeta Maksimovic, and my brother, Dejan, for their infinite love and support. Without them I would not be the person I am today. vi Most of all, I would like to thank my wife, Irena, from the bottom of my heart for all her patience and support. She is my best friend and has been for the past 15 years. Thank you for all your love, support and encouragement. vii Table of Contents Introduction……….…………………………………….…………………………………1 References…………………………………………………………………………………6 Chapter 1 Behavioral evidence for within-eyelet resolution in twisted-winged insects (Strepsiptera) Abstract…………………………………………………………………………………..10 Introduction………………………………………………………………………………11 Materials and methods……………………………………………………………….…..16 Animals…………………………………………………………………………….16 Histology and Scanning electron microscopy (SEM)……………………………...16 Experimental setup…………………………………………………………………17 Quantifying the optomotor response…………………………………….................19 EMD model………………………………………………………………………...20 Results……………………………………………………………………………………24 Discussion………………………………………………………………………………..28 Acknowledgements………………………………………………………………………38 References………………………………………………………………………………..38 Chapter 2 Spatial distribution of opsin encoding mRNAs in the tiered larval retinas of the Sunburst Diving Beetle Thermonectus marmoratus (Coleoptera: Dytiscidae) Abstract…………………………………………………………………………………..43 Introduction………………………………………………………………………………44 Materials and methods…………………………………………………………………...49 Animals……………………………………………………………………….……49 mRNA extraction, cDNA synthesis, PCR, and cloning……………………….…...49 Sequencing and phylogenetic analysis……………………………………….…….51 Histology, environmental scanning electron microscopy (ESEM)………….……..52 Single fluorescence in situ hybridization…………………………………….…….52 Double chromogenic in situ hybridization…………………………………………55 Results……………………………………………………………………………………56 Opsin sequences and phylogenetic analysis……………………………………….56 Spatial expression of TmLW, TmUV I and TmUV II mRNAs...…………………59 Opsin mRNA expression in the distal and proximal retinas of Eyes 1 & 2....….....59 Opsin mRNA expression in the E1 medial retina.…………………………………62 Opsin mRNA expression in Eyes 3 – 6……………………………………………64 Opsin mRNA expression in the eye patch…………………………………………66 Discussion………………………………………………………………………………..66 Distribution of opsin mRNAs in the larval eyes of Thermonectus marmoratus…...66 Comparison of T. marmoratus opsin subclasses with those of other invertebrates..68 Presence of two UV-sensitive opsins in T. marmoratus…………………………...72 Functional implications…………………………………………………………….73 viii Acknowledgements………………………………………………………………………75 References………………………………………………………………………………..76 Chapter 3 The spectral sensitivity of the principal eyes of the Sunburst Diving Beetle Thermonectus marmoratus (Coleoptera: Dytiscidae) larva Abstract…………………………………………………………………………………..84 Introduction………………………………………………………………………………86 Materials and methods…………………………………………………………………...90 Animals…………………………………………………………………………….90
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