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A Comparative Analysis of Morphological, Physiological, And AN ABSTRACT OF THE THESIS OF Jonathon Harris Stillman for the degree of Doctor of Philosophy in Zoology presented on December 4, 1998. Title: A Comparative Analysis of Morphological, Physiological, and Biochemical Adaptation to Abiotic Stress in Intertidal Porcelain Crabs, Genus Petrolisthes. Redacted for Privacy Abstract approved: George N. Somero Organismal tolerance to abiotic environmental stresses contributes significantly to setting the distribution limits of organisms, as demonstrated by vertical zonation patterns in the marine intertidal zone. In this thesis, the ultimate (evolutionary) and proximate (mechanistic) causes of tolerance to temperature and emersion stresses associated with the intertidal zone were examined using porcelain crabs, genus Petrolisthes. Species of Petrolisthes from intertidal and subtidal microhabitats of four biogeographic regions of the Eastern Pacific were used in phylogenetically-based comparative analyses of morphological, physiological, and biochemical adaptation to environmental stress. A phylogenetic tree based on the sequence of the 16sRNA gene was developed to facilitate these analyses. Organismal thermal tolerance limits are adapted to match maximal microhabitat temperatures. Acclimation of thermal tolerance limits suggests that temperate intertidal zone species are living close to their thermal maximum in nature. Respiratory responses to emersion vary among species from different vertical zones. Experimental examination of oxygen consumption rates and lactate accumulation during emersion suggests that intertidal species are able to respire in air using thin membranous regions on the ventral meral segments of their legs (leg membranes). Leg membrane size is positively correlated with body size across species, but not within a single species. Evolutionary analyses indicate that leg membranes may not have evolved for purposes of aerial respiration, but their presence may have allowed intertidal and subtidal species to achieve larger body sizes and higher metabolic rates. The thermal stabilities of an enzyme, lactate dehydrogenase (LDH), from 22 species of Petrolisthes varied widely, but were not correlated with maximal habitat temperatures. Comparative analyses did not indicate any evolutionary relationship between LDH thermal stability and microhabitat conditions. Experimental evidence suggests that interspecific differences in LDH stability are genetically based, and are due both to intrinsic properties of the LDH molecules and extrinsic protein stabilizers. Elucidation of the mechanism(s) of LDH stabilization in Petrolisthes may provide novel insight to the field of protein stabilization. These results studies suggest that individual traits may be subjected to differing levels of selection, and thus the analysis of environmental adaptation requires careful consideration of the biological significance of the traits being examined. © Copyright by Jonathon Harris Stillman December 4, 1998 All Rights Reserved A Comparative Analysis of Morphological, Physiological, and Biochemical Adaptation to Abiotic Stress in Intertidal Porcelain Crabs, Genus Petrolisthes by Jonathon Harris Stillman A Thesis Submitted to Oregon State University In partial fulfillment of the requirements for the degree of Doctor of Philosophy Presented December 4, 1998 Commencement June 1999 Doctor of Philosophy thesis of Jonathon Harris Stillman presented on December 4, 1998 Approved : Redacted for Privacy Major Profess , representing oology Redacted for Privacy Chair bf De a artment of Zoology Redacted for Privacy Dean of Graduat chool I understand that my thesis will become part of the permanent collection of Oregon State University libraries. My signature below authorizes release of my thesis to any reader upon request. Redacted for Privacy Jonathon Harris Stillman, Author I Acknowledgements I would like to thank my graduate thesis advisor, George Somero, for the many ways that he made my graduate student tenure a wonderful one. I thank him for providing me with continuous financial and research support, especially since my research projects focused on organisms, and sometimes problems that were far afield to his primary research foci. George offered me a lot of rope, allowing me to venture through the landscape of professional science, letting me learn to find my own way. I thank him for not letting go of his end while I wandered close to cliff edges and slippery slopes. I thank him for his role in making my years in graduate school some of the best of my life. I am proud and privileged to have worked with such a wonderful scientist and mentor. I thank Greg Jensen, who indirectly helped me to choose a thesis project by publishing his thesis project on porcelain crabs, and then directly helped me by taking the time to show me what a porcelain crab looked like and where I could find them. I value the time that we spent together in the intertidal zone of Panama, and look forward to our next porcelain crab adventure. I thank those people who helped me with specimen and data collection, especially those who sacrificed their bodies helping me in the intertidal zone collecting crabs, and those who sacrificed their minds helping me in the laboratory. I thank crab-grabbers: Barbara Byrne, Stacey Dillon, Gail Turk, Greg Jensen, Amy Moran, and Pam Jensen, and lab-lubbers: Seran Kim (LDH T50 measurements), Rebekah Harrison (LDH stability acclimation), Michelle Wilke (leg membrane measurements) and Sarah Banyard (lactate measurements). II For helping me access field research sites and use their laboratory space, I thank the following people: Penny Barnes and her associates at the Smithsonian Tropical Research Institute in Panama, Sergio Navarrete and his associates at the EstaciOn Costera del Investigaciones, Pontifica Universidad de Cat Mica, Las Cruces, Chile, the staff at the Centro Intercultural de Estudios de Desiertos y Oceanos, in Puerto Peiiasco, Mexico, Craig Marshall at the University of Otago in Dunedin, New Zealand, the staff at the Leigh Marine Lab in Leigh, New Zealand, and Nora Terwilliger and the staff at the Oregon Institute of Marine Biology, University of Oregon. I thank those people who facilitated my access to museum collections, including Gary Pettit, Jody Martin and George Davis at the Los Angeles County Museum of Natural History, and Ray Manning at the National Museum of Natural History. I thank Austin Pritchard and the physiology teaching laboratory at Oregon State University for allowing me to borrow the respirometers and impedance conversion equipment. I thank Bruce Menge, Jane Lubchenco, Barbara Block, Paul Levine, William Gil ly, Jennifer Nielsen, David Epel, and Dennis Powers for allowing me to use equipment and supplies from their laboratories. For offering their wisdom and experience, for occasionally adding a bit of levity to the laboratory setting, and for staying out of my way when I asked them to, I thank the following people who have been my colleagues during parts of the past six and a half years: (in no particular order) Gene Williams, Tom Dietz, Gretchen Hofmann, Dietmar Kultz, Elizabeth Dahlhoff, Jose Torres, Peter Fields, Tzung-Horng Yang, Jen-Jen Lin, Robert Podolsky, Andy Gracey, Deirdre Roberts, Lars Tomanek, Rachael Ream, Patricia Schulte, Jens Franck, John Keen, Eric Sanford, Gary Allison, Carol Blanchette, Jeff Harding, Dwayne Meadows, Mark Carr, Tony Kaltenberg, Jason Podrabsky, Brad Buckley, Sergio Navarrete, Marta Gomez Chiarri, and Zora Lebaric. III I owe a special thanks to Carol Reeb, who sacrificed her time to teach me some of the analytical methods involved in molecular phylogenetics. I thank Janice Blum, and the staffs of the Immunology Department and the Virginia Mason Research Center at the University of Washington, for making me feel at home, and for their interest and tolerance of my crazy research on wild animals. For being there to offer me peace of mind, great advice, and her friendship, I express deep appreciation and life-long friendship to Karina Nielsen, who when I found myself alone at the outset of graduate school let me join as an honorary member of her family. Doing so provided me with the cultural connectivity that was so essential to my mental happiness. The days and nights of discussion of science, art, culture and past lives, all the great food, and all the time spent together, were as much a part of my first few years in graduate school as was anything else. I offer my deepest thanks for the enduring support of Carol Fang, my wonderful wife. Thank you for your words of encouragement, support, patience and warmth. Believe it or not, as I hunkered over my research in intense concentration, I did actually listen to what you were saying. To our dog Jasmine, I offer a big juicy bone and an ear scritchin's for her wonderful companionship during trips to the intertidal zone, and her patience and loyalty during the time I spent pipetting and typing, and generally ignored her. One could ask for no better a dog. To my parents, Marilyn and Jerry, and my brother Scott, thanks for putting up with my eccentricities and non-traditional career choice. Take solace in knowing that although we never finish our life's education, I have finally finished graduate school. Finally, I thank the National Science Foundation for supporting this research with grants IBN 9206660 to George Somero, and IBN 9700701 to myself and George Somero. IV TABLE OF CONTENTS Page Chapter 1: Introduction 1 Conceptual framework of comparative organismal biology 2 Study system: porcelain
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