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CONQUERING THE COLD SHUDDER: THE ORIGIN AND EVOLUTION OF SNAKE EYES Dissertation Presented in Partial Fulfillment for the Requirements for the Degree of Doctor of Philosophy in the Graduate School of The Ohio State University By Christopher L. Caprette, B.S., M.S. **** The Ohio State University 2005 Dissertation Committee: Thomas E. Hetherington, Advisor Approved by Jerry F. Downhower David L. Stetson Advisor The graduate program in Evolution, John W. Wenzel Ecology, and Organismal Biology ABSTRACT I investigated the ecological origin and diversity of snakes by examining one complex structure, the eye. First, using light and transmission electron microscopy, I contrasted the anatomy of the eyes of diurnal northern pine snakes and nocturnal brown treesnakes. While brown treesnakes have eyes of similar size for their snout-vent length as northern pine snakes, their lenses are an average of 27% larger (Mann-Whitney U test, p = 0.042). Based upon the differences in the size and position of the lens relative to the retina in these two species, I estimate that the image projected will be smaller and brighter for brown treesnakes. Northern pine snakes have a simplex, all-cone retina, in keeping with a primarily diurnal animal, while brown treesnake retinas have mostly rods with a few, scattered cones. I found microdroplets in the cone ellipsoids of northern pine snakes. In pine snakes, these droplets act as light guides. I also found microdroplets in brown treesnake rods, although these were less densely distributed and their function is unknown. Based upon the density of photoreceptors and neural layers in their retinas, and the predicted image size, brown treesnakes probably have the same visual acuity under nocturnal conditions that northern pine snakes experience under diurnal conditions. Second, I quantified the orbital area, binocular overlap, eye size, lens size, and the refractive powers of the lens and spectacle within and among colubrid snakes and pit vipers. Among colubrid snakes, the size-adjusted orbital area fit preditions based upon ii ecology, with nocturnal arboreal species having the largest orbits (p < 0.001). My results on the distribution of binocular overlap among colubrid snakes, however, contradicted earlier studies. Diurnal arboreal species had the smallest angle of overlap, while terrestrial nocturnal species had the greatest degree of overlap (one-way ANOVA, p < 0.001). Among pit vipers, the eastern cottonmouth had a much greater average orbital area (one-way ANOVA, p < 0.001) for its body size than other species. This species is the only aquatic pit viper, and forages for a wide variety of food, including ectothermic prey under dim light, which may explain its relatively large eyes. Pit vipers had smaller orbital areas than colubrid snakes, but significantly greater binocular overlaps (Mann- Whitney U test, p < 0.001). The eyeballs of nine species were significantly subspherical, as were the lenses of four species. The lens contributed significantly more to the total refraction (paired t-tests, p < 0.05) than the spectacle in all but two species, the brown treesnake, in which the spectacle had greater refractive power (paired t-tests, p < 0.001), and the northern copperhead, in which the two elements did not differ in their refractive powers. Snakes evolved from lizards but have dramatically different eyes. These differences are cited widely as compelling evidence that snakes had fossorial and nocturnal ancestors. Snake eyes, however, also exhibit similarities to those of aquatic vertebrates. I used a comparative analysis of ophthalmic data among vertebrate taxa to evaluate alternative hypotheses concerning the ecological origin of the distinctive features of snake eyes. In parsimony and phenetic analyses, eye and orbital characters retrieved groupings more consistent with ecological adaptation rather than accepted phylogenetic relationships. Fossorial lizards and mammals cluster together, whereas iii snakes are widely separated from these taxa and instead cluster with primitively aquatic vertebrates. This indicates that snakes eyes most resemble those of aquatic vertebrates, and suggests that the early evolution of snakes occurred in aquatic environments. iv ACKNOWLEDGMENTS I am grateful to my committee for their patience, understanding, and substantial assistance in revising this document. I am particularly thankful to Tom Hetherington, my advisor, for his continued support well above and beyond any conceivable call of duty. Jerry Downhower provided frequent sparks to ignite the fire of curiosity about snake eyes. My discussions concerning phylogenetic analyses with John Wenzel were vital to the completion of the most significant chapter of my dissertation, and quite entertaining as well. Dave Stetson’s expertise in light and electron microscopy were invaluable to the completion of two of my dissertation chapters. The Borror Laboratory of Bioacoustics (BLB) was most generous in “employing” me throughout a number of quarters, despite my dissertation research having no bearing on animal communication whatsoever. I want to thank Abbott Gaunt for bringing me to OSU in the first place, Sandra L.L. Gaunt for first providing me with an RA at the BLB, and Doug Nelson and Jill Soha for going so far as to letting me manage the digital project during its final year. My experiences at the BLB were some of the best of my graduate career. Cathy Drake and the EEOB (Zoology) office staff, despite overwhelming responsibilities, remain outstanding examples of efficiency to which every bureaucratic organization should aspire. I am grateful to José Diaz for taking time out of his busy days v to assist me in preparing specimens for TEM and training me in the finer points of said preparation. Kathy Wolken and Brian Kemmenoe of the Campus Imaging and Microscopy Facility trained me in using the TEM. The staff of the Biological Sciences and Pharmacy Library, under the superb leadership of Bruce Leach, were always helpful, considerate, and reliable. I thank the California Academy of Sciences for funding my visit to their herpetological collections, their helpful staff, Jens Vindum, Rhonda Lucas, and Ricka Stoelting, in particular; the National Museum of Natural History for granting me access to their herpetolocical collections, Addison Wynn and Roy McDiarmid, in particular; John Condit for helping me locate specimens in the OSU Museum; and the USGS BRD for funding the work on brown treesnakes through the former Ohio Cooperative Fish and Wildlife Research Unit. People too numerous to count contributed to many discussions, criticisms, and witticisms concerning my dissertation research. They are responsible for much of the good and none of the bad in this document. The late Garth Underwood provided my earliest exposure to snake eyes through his chapter in Biology of Reptilia. Al Savitsky encouraged me in my work and got me thinking seriously about snake eye development. Brady Porter, Brad Coupe, Nancy Anderson, Chris Shulse, Hitesh Khanna, Earl Campbell, Robin Taylor, Kurt Pickett, and Karen Hallberg represent some of the more significant friends that contributed to my thinking in this effort. Science Club provided a wealth of relief after each week of frustration, and for that (and the great beer) I am most grateful. Lastly, but certainly not least, I thank my wife, Heather Caprette, for her love and support throughout most of this endeavor. vi VITA 1966................................................................................................................................ Born 1988..................................................................... B.S., Biology, Cleveland State University 1993.................................................................... M.S., Biology, Cleveland State University 1999 – present...............................................................................................Ph.D Candidacy Department of Evolution, Ecology, and Organismal Biology The Ohio State University PUBLICATIONS Caprette, C.L., Lee, M.S.Y., Mokany, A., Shine, R.A. and Downhower, J.F. 2004.The origin of snakes (Serpentes) from the perspective of vertebrate eye anatomy. Biological Journal of the Linean Society, 81: 469-482. Caprette, C.L. and Gates, M.A. 1994. Quantitative analyses of interbreeding in populations of vannus-morphotype Euplotes, with special attention to the nominal species E. vannus and E. crassus. Journal of Eukaryotic Microbiology, 4: 316-324. FIELDS OF STUDY Evolution, Ecology and Organismal Biology vii TABLE OF CONTENTS Page: Abstract.............................................................................................................................ii Acknowledgments............................................................................................................ v Vita................................................................................................................................... vii List of Tables.................................................................................................................... x List of Figures...................................................................................................................xi Chapters: 1. Introduction................................................................................................................ 1 What are snakes?............................................................................................ 2 The origin of snakes......................................................................................
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