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Learning from the Extraordinary: How the Highly Derived Larval Eyes of the Sunburst Diving Beetle Can Give Insights Into Aspects Of

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Learning from the Extraordinary: How the Highly Derived Larval Eyes of the Sunburst Diving Beetle Can Give Insights Into Aspects Of Learning from the extraordinary: How the highly derived larval eyes of the Sunburst Diving Beetle can give insights into aspects of holometabolous insect visual systems 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 2011 by Nadine Stecher B.S., University of Rostock, 2001 M.S., University of Rostock, 2005 Committee Chair: Elke K. Buschbeck, Ph.D. Abstract Stemmata, the eyes of holometabolous insect larvae, vary greatly in number, structure and task. The stemmata of the Sunburst Diving Beetle, Thermonectus marmoratus, are among the most sophisticated. The predatory larvae have six eyes and a potentially light-sensitive spot (eye spot) adjacent to the stemmata. The forward-pointing tubular eyes Eye 1 (E1) and Eye 2 (E2) are involved in prey capture, and possess a biconvex lens, a cellular crystalline cone-like structure, and tiered retinal tissue. A distal and a proximal retina can be distinguished, which differ not only in morphology but possibly also in function. E1 has an additional retina which runs medially alongside the crystalline cone-like structure. Using transmission electron microscopic preparations, I described the ultrastructure of the retinas of the principal eyes E1 and E2. The proximal retinas are composed of photoreceptors with predominantly parallel microvilli, and neighboring rhabdomeres are oriented approximately orthogonally to each another. This rhabdomeric arrangement is typical for eyes that are polarization sensitive. A similar organization is observed in a portion of the medial retina of E1, but not in either of the distal retinas. Since Thermonectus marmoratus larvae are visually-guided predators, polarization sensitivity would perhaps improve their ability to detect prey with polarization features. Measuring hunting performance of larvae under polarized or unpolarized illumination conditions, I have shown that polarized illumination decreased the latency to prey detection and improves capturing success. Although polarization-sensitivity is expected to be common among holometabolous insect larvae due to the rhabdomeric nature of their stemmata, no larvae have been named that possess polarization sensitivity that is involved in prey capture. Moreover, while many invertebrates that are polarization sensitive have polarization-specific regions in ii their visual system, the eyes of Thermonectus marmoratus larvae potentially have a division of labor within the same stemma. The interesting question arises as to how these stemmata develop. Although they are structurally very unlike each other, stemmata are considered to be homologous to adult compound eyes. It is perhaps in their development that one can find evidence for a common ancestry. Using basic histological methods, I observed stemmatal development in Thermonectus marmoratus embryos, and contrasted my finding to structural changes during compound eye development. The latter is described best in Drosophila. Similar to Drosophila ommatidia, the stemmata originate from a proliferative, pseudostratified epithelium. The photoreceptor cells differentiate in sequence, and they appear before the accessory cells differentiate. In Thermonectus marmoratus, the photoreceptor cells that are located in the proximal layer in the fully-developed stemma assume their position earlier than the prospective distal photoreceptors. In contrast to the Drosophila compound eye, which is characterized by distinct periods of high mitotic activity, cell proliferation in T. marmoratus stemmatal development appears to be a continuous but low-level process. Moreover, I did not observe a morphogenetic furrow-like differentiation process such as it is typical for Drosophila ommatidial development. Based on the morphological study, it will be possible to investigate molecular similarities between the development of compound eyes in Drosophila and the stemmata in Thermonectus marmoratus. iii Copyright transfer statement The copyright to th article entitled “Retinal ultrastructure may mediate polarization sensitivity in larvae of the Sunburst diving beetle, Thermonectus marmoratus (Coleoptera: Dytiscidae)” is transferred to Springer-Verlag (respective to owner if other than Springer and for U.S. government employees: to the extent transferable) effective if and when the article is accepted for publication. The author warrants that his/her contribution is original and that he/she has full power to make this grant. The author signs for and accepts responsibility for releasing this material on behalf of any and all co-authors. The copyright transfer covers the exclusive right to reproduce and distribute the article, including reprints, translations, photographic reproductions, microform, electronic form (offline, online) or any other reproductions of similar nature. An author may self-archive an author-created version of his/her article on his/her own website and or in his/her institutional repository. He/she may also deposit this version on his/her funder’s or funder’s designated repository at the funder’s request or as a result of a legal obligation, provided it is not made publicly available until 12 months after official publication. He/ she may not use the publisher’s PDF version, which is posted on www.springerlink.com, for the purpose of self- archiving or deposit. Furthermore, the author may only post his/her version provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer’s website. The link must be accompanied by the following text: “The final publication is available at www.springerlink.com”. Prior versions of the article published on non-commercial pre-print servers like arXiv. gov can remain on these servers and/or can be updated with the author’s accepted version. The final published version (in pdf or html/xml format) cannot be used for this purpose. Acknowledgement needs to be given to the final publication and a link should be inserted to the published article on Springer’s website, accompanied by the text “The final publication is available at springerlink.com”. The author retains the right to use his/her article for his/her further scientific career by including the final published journal article in other publications such as dissertations and postdoctoral qualifications provided acknowledgement is given to the original source of publication. The author is requested to use the appropriate DOI for the article. Articles disseminated via www.springerlink.com are indexed, abstracted and referenced by many abstracting and information services, bibliographic networks, subscription agencies, library networks, and consortia. The copyright of the chapters entitled “The influence of polarized light illumination on the hunting success in the first instar larvae of the Sunburst Diving Beetle, Thermonectus marmoratus (Insecta, Dytiscidae)” and “Development of the larval eyes of the Sunburst Diving Beetle, Thermonectus marmoratus (Insecta: Dytiscidae)” belongs to the author, Nadine Stecher. iv Acknowledgements I would like to thank my advisor Elke Buschbeck for her generous support and interest in my projects, on which I was able to work under her supervision but still independently. Elke always manages to give each single student special attention in their time of need. I would like to thank my committee members: George Uetz for his help with my statisctics. Ed Griff for asking those questions I never would have have thought of asking, and also for the mentoring I received being his TA. Tiffany Cook for sharing her expertise on eye development, and John Layne for his help with computational analyses. Thanks to Guy Cameron for giving me a UGS for the home stretch of my thesis work when I was really no longer elibible for funding. Randy Morgan and the Insectarium of the Cincinnati Zoo & Botanical Garden provided the initial culture of Sunburst diving beetles. This research was funded by the National Science Foundation (IOB-545978). Special thank you hugs go out to my friends and emotional support group, featuring Prem Rajkumar, Sri Pratima Nandamuri, Shannon Werner, Jessie Ebie, Shira Gordon, K Marie Hoefer, and Srdjan Maksimovic. Having these guys in my life really helped me through grad school and my personal life as they would always pick me up when I was feeling low. They also shared many happy days with me, of which there were plenty, and always let me believe that my jokes were funny. We talked a lot about science, too. I am eternally grateful to my parents, who have always believed in me and helped me out of any bad situation. I know I am very lucky having a family that is as caring and supportive as mine. And most of all, my love Suman, who has been my anchor for the past few years. v Contents Introduction ................................................................................................................................... 1 Chapter 1 Retinal ultrastructure may mediate polarization sensitivity in larvae of the Sunburst diving beetle, Thermonectus marmoratus (Coleoptera: Dytiscidae). .................................................... 6 Abstract ....................................................................................................................................... 7 Introduction ................................................................................................................................
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