Sociality, Sterility, and Poverty; Host-Pathogen Coevolution, with Implications for Human Ecology by Matthew H. Bonds (Under the direction of Pejman Rohani) Abstract Disease ecology constitutes a frontier of human ecology that is primed for integrated research between the natural and social sciences. Here, I present a framework for such inte- gration. Relying on game theory and optimization theory - techniques found in both the economics and evolutionary biology literatures - I ¯rst develop a theory of the coevolution of social behavior and infectious diseases for non-human social organisms, where I ¯nd that increases in pathogen virulence can surprisingly result in greater sociality. I then develop a model of pathogen-induced sterility that is integrated into the general evolution of viru- lence framework, and explains a well-known but poorly understood phenomenon: pathogen- induced gigantism. The model predicts that sterility could cause the host to invest more resources into maintenance versus reproduction. Under certain circumstances, the pathogen could therefore evolve to manipulate the host via castration, causing gigantism. Finally, I develop a formal ecological model of global health and economic development, where I ¯nd that fertility may play an even larger role in the persistence of poverty and disease than previously thought. Index words: ESS,CoESS, Evolution of Virulence, Pathogen Manipulation, Sociality, Infectious Disease, Poverty Trap Sociality, Sterility, and Poverty; Host-Pathogen Coevolution, with Implications for Human Ecology by Matthew H. Bonds B.A., Francis Marion University, 1998 Ph.D., University of Georgia, 2003 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Ful¯llment of the Requirements for the Degree Ph.D. Athens, Georgia 2006 °c 2006 Matthew H. Bonds All Rights Reserved Sociality, Sterility, and Poverty; Host-Pathogen Coevolution, with Implications for Human Ecology by Matthew H. Bonds Approved: Major Professor: Pejman Rohani Committee: Sonia Altizer Daniel E.L. Promislow H. Ronald Pulliam Arthur Snow Electronic Version Approved: Maureen Grasso Dean of the Graduate School The University of Georgia August 2006 Dedication This is dedicated to Adam, Meredith, Mom, and Gran'anne. iv Acknowledgments As for all graduate students, completing this dissertation has been as much of a personal process as it has been professional, and the line therefore becomes quite blurred between the personal and professional influences from a number of individuals. The most impor- tant early contribution came from my undergraduate biology professor, Travis Knowles, at Francis Marion University. He was a huge inspiration, and has become a close friend, who stimulated my interest in both natural history as well as public policy. Ron Pulliam has also played an extremely important role in my work. I was ¯rst exposed to disease-ecology in his graduate level population ecology class, and it was he who suggested disease ecology as a nexus between economics and ecology. With that impetus, while studying economics, I began serious dialogue with Don Keenan. Keenan has become a great friend, who has been a dedicated and constant source of ideas for me. It was through early conversations with both Keenan and Ron, that I eventually resolved to study infectious diseases of humans, and Ron put me in touch with Pej Rohani, with whom I eventually decided to undertake this project. The influence of each of the people mentioned above has been de¯nitive and this dissertation would not have been the same without them - indeed, it may not have been written at all. For each of them, my appreciation is also personal. But, for his sheer com- mitment to both the direct and indirect influences on my development as an ecologists and scholar, I owe a special thanks to Pej. He has not simply been an academic advisor. He has long recognized that true development comes in both direct and mysterious ways and has ensured that we in the lab have a community that is intellectually positive and constructive. Thus, through him, we are able to bene¯t from each other. With that in mind, I must thank the Rohani lab group, which evolved to become the Rohani-Altizer group. In a similar way, I owe Sonia Altizer for being not only supportive in her advisory role, but for joining Pej in v vi creating such an awesome place to work, and with such great scientists. Everybody among our research group deserves credit for contributing to a very fun, rich, intellectual culture, including Hanh Nguyen, Dan Vasco, Natalia Mantilla-Beniers, Yunxin Huang, Cat Bradley, Elizabeth Lindsey, Byron Ledbetter, and Andrew Leidner. But I must single a few out for having directly contributed to ideas for my work: Jaap de Roode, Amy Pederson, and Marc Choisy. I especially thank Helen Wearing, who has been an invaluable resource throughout the last three years. Finally, I thank my dissertation committee, which includes Art Snow, Daniel Promislow, Steve Hubbell, Mark Hunter, Pej and Sonia. This work was funded by an ARCS Fellowship, an Odum Fellowship and a grant from the National Science Foundation. Thanks to the donors, including the tax-paying public, for those causes. Table of Contents Page Acknowledgments . v Chapter 1 Introduction . 1 1.1 The need for integrated ecological and economic research 1 1.2 Infectious Diseases as Frontier of Human Ecology . 6 1.3 Objectives . 6 1.4 Chapter 2: Coevolution of Sociality and Infectious Dis- eases . 7 1.5 Chapter 3: Host Life-History Strategy Explains Pathogen Induced Sterility . 10 1.6 Chapter 4: An Ecological Framework for Global Health and Economic Development . 13 2 Higher Disease Prevalence Can Induce Greater Sociality; a Game Theoretic Coevolutionary Model . 16 2.1 Introduction . 16 2.2 The Evolution of Social Contact in the Context of Infectious Diseases . 17 2.3 Model . 18 2.4 Evolutionarily Stable Contact and Disease Prevalence Respond to Each Other . 23 2.5 Coevolution of Host Sociality and Infectious Disease . 24 vii viii 2.6 Discussion . 28 3 Host Life History Strategy Explains Pathogen-Induced Sterility 33 3.1 Introduction . 33 3.2 Model . 35 3.3 Pathogen-Induced Sterility as Host Life-History Strategy 38 3.4 Coevolution of Pathogen Virulence . 44 3.5 Pathogen Manipulates Host Life-History Strategy, Causing Gigantism . 49 3.6 Discussion . 53 4 Reducing Fertility More Effective than Vaccinating for Improving Global Health and Economic Development; A Simple Ecological Framework . 57 4.1 Introduction . 57 4.2 Classic S-I-R Epidemiological Model . 60 4.3 Income Effect Creates Feedback Between Disease Preva- lence and the Transmission Rate . 61 4.4 Discussion . 69 5 Concluding Remarks and Future Research . 72 5.1 What has Been Accomplished . 72 5.2 Where to Go From Here . 75 Bibliography . 79 Appendix A Stochastic Simulation of Coevolving Contact and Virulence . 97 B The Optimal Contact Rate as a Function of Pathogen Preva- lence with Alternative Fitness Function . 98 ix C Solution to the Equilibrium levels of Protection and Disease Prevalence . 100 D Illustration of Feedback Between Protection and Disease Prevalence . 101 Chapter 1 Introduction \In October 1838, ¯fteen months after I had begun my systematic inquiry, I happened to read for amusement Malthus on Population, and being prepared to appreciate the struggle for existence which everywhere goes on, from long-continued observation of the habits of animals and plants, it at once struck me that under these circumstances favourable variations would tend to be preserved, and unfavourable ones to be destroyed. The result would be the formation of a new species." Charles Darwin (1887) \The enterprise within the social sciences best poised to bridge the gap to the natural sciences, the one that most resembles them in style and self-con¯dence, is economics." E.O. Wilson (1998) 1.1 The need for integrated ecological and economic research Among other things, human beings have been very successful reproducers. The world human population has grown from approximately ten million, before the agricultural revolution ten thousand years ago, to over six billion today, having added nearly four billion people in the last ¯fty years alone (Diamond, 1997). Such intense population growth seems almost natural. After all, the tendency to more-than-reproduce oneself is universally observed throughout the living world. Without \positive checks" such as \famine" and \disease" or perhaps \moral restraint", populations of any organism will experience exponential growth. This basic principle was laid out by the political economist Rev. Thomas Robert Malthus in his 1 2 landmark, \Essay on the Principle of Population," (Malthus, 1798), and constituted a key insight for Charles Darwin's explanation for the origin of species via evolution by natural selection (Darwin, 1879), which remains the primary over-arching paradigm in ecology today. Darwin's logic was relatively straightforward. A constant population level requires that the average individual produces exactly one reproductive o®spring in its lifetime. However, in reality, individuals of all species tend to reproduce many more times than once, with each o®spring often slightly di®erent from the rest. Because most natural populations are not growing exponentially, the vast majority of organisms in the world must be dying prema- turely. An ultimate consequence of all of this reproduction, variation, and death is evolution and diversity. And, like all of the other organisms that are part of the life-death evolutionary process, humans also tend to more-than-reproduce themselves... and we survive better. That the key paradigmatic theory of the natural sciences - evolution by natural selection - relies on principles ¯rst developed in the social sciences should be of no surprise. As humans, we are, after all, the most studied animals on earth. Since Darwin's theory was ¯rst presented, intellectual parallels between ecology and economics have remained, yet genuine synthesis is almost totally absent. This is a problem - the di®erences between humans and other organisms is more than just an intellectual curiosity.