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Phylogenetic Patterns and Ecological Determinants of Adaptive Radiation

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Phylogenetic Patterns and Ecological Determinants of Adaptive Radiation PHYLOGENETIC PATTERNS AND ECOLOGICAL DETERMINANTS OF ADAPTIVE RADIATION A DISSERTATION SUBMITTED TO THE DEPARTMENT OF BIOLOGICAL SCIENCES AND THE COMMITTEE ON GRADUATE STUDIES OF STANFORD UNIVERSITY IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Matthew Leo Knope March 2012 © 2012 by Matthew Leo Knope. All Rights Reserved. Re-distributed by Stanford University under license with the author. This work is licensed under a Creative Commons Attribution- Noncommercial 3.0 United States License. http://creativecommons.org/licenses/by-nc/3.0/us/ This dissertation is online at: http://purl.stanford.edu/pc001rm2983 ii I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Tadashi Fukami, Primary Adviser I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Rodolfo Dirzo I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Elizabeth Hadly I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Ward Watt Approved for the Stanford University Committee on Graduate Studies. Patricia J. Gumport, Vice Provost Graduate Education This signature page was generated electronically upon submission of this dissertation in electronic format. An original signed hard copy of the signature page is on file in University Archives. iii Abstract It is well recognized that much of the biodiversity on Earth is the result of adaptive radiation, which is the process by which one biological lineage gives rise to many descendant lineages, all adapted to the various ecological roles they fill. However, it remains unclear why some lineages diversify greatly by adaptive radiation while others diversify little or not at all. The classic view is that “ecological opportunity” (where organisms find themselves in an area with abundant or under-utilized resources) allows the lineage to interact with the environment in novel ways and this promotes adaptive radiation. Here I utilize three taxonomically disparate systems (microbes, plants, and fishes) to examine patterns of diversification and identify possible ecological factors that promote or suppress adaptive radiation. In a laboratory experiment with bacteria and phage, I show that the prior evolutionary history of immigrants may determine their subsequent diversification dynamics after arrival to a new habitat. In another study, using molecular phylogenetics to investigate the rate of diversification of an adaptive radiation of flowering plants in Hawaii, I show that this radiation is among the most rapid yet studied in plants, on a per-unit-area basis, and suggest that the relative scale of habitable area available for the organisms under study is necessary to understand both the rate and the extent of diversification. Lastly, I utilize a radiation of marine fishes along the west coast of North America and show that morphological adaptations can facilitate habitat shifts leading to further evolutionary diversification not only in terrestrial and freshwater systems, but in marine systems as well, confirming the idea that general evolutionary principles apply across systems. One common theme that emerges from these studies is that the “ecological opportunity” hypothesis is supported, but that it may not fully explain diversification patterns. Overall, these studies suggest that explicit consideration of the prior evolution of immigrants, the relative scale of habitable area, and adaptive morphological shifts to novel habitats are necessary to fully understand patterns and drivers of adaptive radiation. iv Acknowledgments It has been said that it takes a village to raise a thesis, and while this is certainly true, in my case it has taken two villages and then some. I began my Ph.D. work at the University of Hawaii at Manoa in the fall of 2006 and transferred to Stanford University in the fall of 2008. Therefore, I may have at least double the typical number of people to thank for helping me through this journey. First and foremost, I would like to express my deepest gratitude to my principal advisor, Tadashi Fukami, who has is in every way exceeded my expectations for what it means to be an academic mentor. Tad is exactly the kind of scientist and mentor that I hope to be one day; he is exceptionally hard-working, enthusiastic, and encouraging. In addition, there is something intangible in Tad’s character that makes him a joy to work with. I have also been blessed by having a phenomenal Ph.D. committee. Liz Hadly, Rodolfo Dirzo, and Ward Watt define what it means to be excited about ecology and evolution. Their infectious enthusiasm, positive energy, and sharp analytical minds improved this thesis in innumerable ways. In addition, two of the best experiences of my time at Stanford were being a teaching assistant for Liz’s Evolutionary Paleobiology class and for Rodolfo’s Tropical Ecology and Conservation Biology class. They are both inspired and gifted educators dedicated to their craft and never satisfied with their lessons, no matter how refined. I am also very grateful to Jonathan Payne for serving as my outside committee member and for chairing my defense. I would also like to extend a very warm mahalo to all of the members of the Fukami lab both at Stanford and at the University of Hawaii. Melinda Belisle, Ben Callahan, Marie-Pierre Gauthier, Whitney Hoehn, Yolanda Madrid, Holly Moeller, Mifuyu Nakajima, Colin Olito, Kabir Peay, and Rachel Vannette made everyday at work a better place to be and I learned an incredible amount from each and every one of them. I would also like to thank all of the extended members of the Fukami lab and all other friends and colleagues (many to numerous to list here) in the Departments of Zoology and Botany at the University of Hawaii and in the Department of Biology at Stanford, for v their support and friendship. In addition, many people helped in a wide variety of ways to make each of the projects of this dissertation come to life and to avoid repeating myself, I acknowledge them individually at the end of the chapter that they contributed to. In the Biology Student Services Office at Stanford, Monica Bernal, Dan King, Jennifer Mason, Matt Pinheiro, and Valerie Kiszka exemplify what it means to be helpful, friendly, and professional. It seems no question is too small to not demand their full attention. In the Zoology Department Office at the University of Hawaii, Lynne Ogata, Audrey Shintani, and Jan Tatsuguchi truly made me feel like a part of their ‘ohana. I would also like to acknowledge both the chair of the Department of Zoology at the University of Hawaii, Sheila Conant, and the chair of the Department of Biology at Stanford University, Bob Simoni, for their generous support. During my first two years at the University of Hawaii, I had the best fellowship I could have possibly imagined. As an NSF GK-12 teaching fellow, I had the opportunity to work one day every week bringing ecology and evolution to the middle-school students at Assets School in Honolulu. These students work with a wide variety of learning challenges and I am positive that these students taught me far more than I ever taught them. I also had the priveldge to work with a number of truly gifted teachers at Assets that have dedicated their lives to service and make the world a better place everyday. Likewise, my GK-12 mentors, Erin Baumgartner and Kanesa Duncan, taught me a tremendous amount about how to teach science effectively. I am also blessed to have a family that is always incredibly supportive of all of my interests. I am forever grateful to my parents, Jeff Knope and Teri Katahara, for their continual encouragement and interest in the things that I find fascinating. Absolutely none of this work would have been possible without their hard work and many sacrifices on my behalf. I am also very fortunate to have the support and encouragement of my sister, Carrie Riley, my brother-in-law Shawn Riley, my nephew Sheamus Riley, and my niece Sophia Riley. Last, but certainly not least, I am a man blessed in love. Shama Hinard has not only been supportive of my dissertation work, she has been an integral part of it. From vi suspending me upside-down off a cliff on northern Molokai (and not dropping me) to collect a leaf tissue sample from an endangered species of Hawaiian Bidens, to reading my manuscripts and giving me insightful feedback, to putting up with too many evenings spent suffering through bad practice talks, I have run my tab high and am forever in her debt. vii Table of Contents Chapter 1. General introduction...................................................................................................................1 General introduction................................................................................................................................2 Analytical approaches .............................................................................................................................3 Overview of results..................................................................................................................................4 Author contributions................................................................................................................................6
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