SOCIAL CHANGE, PARASITE EXPOSURE, AND IMMUNE DYSREGULATION AMONG SHUAR FORAGER-HORTICULTURALISTS OF AMAZONIA: A BIOCULTURAL CASE-STUDY IN EVOLUTIONARY MEDICINE by TARA CEPON ROBINS A DISSERTATION Presented to the Department of Anthropology and the Graduate School of the University of Oregon in partial fulfillment of the requirements for the degree of Doctor of Philosophy June 2015 DISSERTATION APPROVAL PAGE Student: Tara Cepon Robins Title: Social Change, Parasite Exposure, and Immune Dysregulation among Shuar Forager-Horticulturalists of Amazonia: A Biocultural Case-Study in Evolutionary Medicine This dissertation has been accepted and approved in partial fulfillment of the requirements for the Doctor of Philosophy degree in the Department of Anthropology by: J. Josh Snodgrass Chairperson Lawrence S. Sugiyama Core Member Frances J. White Core Member Brendan J.M. Bohannan Institutional Representative and Scott L. Pratt Dean of the Graduate School Original approval signatures are on file with the University of Oregon Graduate School. Degree awarded June 2015 ii © 2015 Tara Cepon Robins iii DISSERTATION ABSTRACT Tara Cepon Robins Doctor of Philosophy Department of Anthropology June 2015 Title: Social Change, Parasite Exposure, and Immune Dysregulation among Shuar Forager-Horticulturalists of Amazonia: A Biocultural Case-Study in Evolutionary Medicine The Hygiene Hypothesis and Old Friends Hypothesis focus attention on the coevolutionary relationship between humans and pathogens, positing that reduced pathogen exposure in economically developed nations is responsible for immune dysregulation and associated increases in chronic inflammation, allergy, and autoimmunity. Despite progress in testing these ideas, few studies have examined these relationships among populations undergoing the transition from traditional to more market-based lifestyles. The present study tests relationships between economic development and social change, altered infectious disease exposure, and immune function among the Shuar forager- horticulturalists of Amazonian Ecuador, a population undergoing rapid economic change associated with increased market participation. Using stool samples to assess soil-transmitted helminth (STHs; parasitic intestinal worms) burden, dried blood spot measurement of the inflammatory marker C-reactive protein (CRP), and interviews to evaluate level of market integration (MI; the suite of social and cultural changes associated with rapid economic development) and disgust sensitivity, this dissertation tests the Hygiene and Old Friends Hypotheses. The first study tests relationships between STH exposure and MI, using geographic iv location in relation to the regional market center as a proxy for MI. This study documents lower rates of STHs in people living in more market integrated regions. The second study tests the coevolutionary role that STHs and other pathogens have played in shaping human psychology and behavior. Findings suggest that pathogen exposure has acted as a selective pressure, resulting in evolved disgust sensitivity toward pathogen related stimuli. This study provides evidence that disgust sensitivity is calibrated to local environments, acting to decrease STH exposure. The third study tests the role of STHs in immune function. CRP was positively related to age in uninfected individuals. No relationships existed for more traditionally living or infected individuals. These findings suggest that STH exposure may decrease the risk of developing chronic inflammation and associated diseases with advancing age. These studies provide support for the idea that STHs provide stimuli that decrease chronic inflammation, suggesting that altered intestinal microflora in developed nations may be partially responsible for the development of chronic inflammatory disorders like allergy and autoimmunity. This dissertation includes previously published and unpublished coauthored material. v CURRICULUM VITAE NAME OF AUTHOR: Tara Cepon Robins GRADUATE AND UNDERGRADUATE SCHOOLS ATTENDED: University of Oregon, Eugene, OR Marquette University, Milwaukee, WI DEGREES AWARDED: Doctor of Philosophy, Biological Anthropology, 2015, University of Oregon Master of Science, Biological Anthropology, 2009, University of Oregon Bachelor of Arts, Anthropology and History, 2007, University of Oregon AREAS OF SPECIAL INTEREST: Human health and biology Parasitology and coevolution Immune dysregulation PROFESSIONAL EXPERIENCE: Graduate Teaching Fellow, University of Oregon, 2007 to 2015 GRANTS, AWARDS, AND HONORS: Juda Memorial Endowment Travel Fund, University of Oregon, 2010, 2014 Doctoral Dissertation Improvement Grant, NSF, 2013 Stern/Barnett Award, University of Oregon, 2013 Health Education Award, University of Oregon, 2008, 2010, 2012, 2013 Anthropology Department Travel Award, University of Oregon, 2008, 2009, 2011, 2012, 2013 vi Dissertation Fieldwork Grant, Wenner-Gren Foundation, 2012 Sasakawa Young Leaders Fellowship, SYLLF, 2011 PUBLICATIONS: Madimenos FC, Liebert MA, Cepon TJ, Snodgrass JJ, Sugiyama LS. 2015. Osteoporosis prevalence in a Colono population from rural Amazonian Ecuador. Am J Hum Biol 27: 139-142. Cepon-Robins TJ, Gildner TE, Liebert MA, Colehour AM, Urlacher SS, Snodgrass JJ, Madimenos FC, Sugiyama LS. 2014. Soil-transmitted helminth prevalence and infection intensity among geographically and economically distinct Shuar communities in the Ecuadorian Amazon. J Parasitol 100(5): 598-607. Colehour A, Meadow JF, Cepon-Robins TJ, Gildner TE, Liebert MA, Urlacher SS, Bohannan BJM, Snodgrass JJ, Sugiyama LS. 2014. Local domestication of microbes via cassava beer fermentation. PeerJ 2: e479. Liebert MA, Snodgrass JJ, Madimenos FC, Cepon TJ, Blackwell AD, Sugiyama LS. 2013. Implications of market integration for cardiovascular and metabolic health among an indigenous Amazonian Ecuadorian population. Annals of Human Biology doi: 10.3109/03014460.2012.759621. McDade, TW, Tallman PS, Madimenos FC, Liebert MA, Cepon TJ, Sugiyama LS, Snodgrass JJ. 2012. Analysis of variability of high sensitivity C- reactive protein in lowland Ecuador reveals no evidence of chronic low- grade inflammation. Am J Hum Biol 24: 675-681. Madimenos FC, Snodgrass JJ, Liebert MA, Cepon TJ, Sugiyama LS. 2012. Reproductive effects on skeletal health in Shuar women of Amazonian Ecuador: A life history perspective. Am J Hum Biol doi: 10.1002/ajhb.22329. Cepon TJ, Snodgrass JJ, Leonard WR, Tarskaia LA, Klimova TM, Fedorova VI, Baltakhinova ME, Krivoshapkin VG. 2011. The effects of circumpolar adaptation and lifestyle on the development of autoimmune thyroid disorders among the Yakut of Siberia. Am J Hum Biol 23: 703-709. Madimenos FC, Snodgrass JJ, Blackwell AB, Liebert MA, Cepon TJ, Sugiyama LS. 2011. Normative calcaneal quantitative ultrasound data for the indigenous Shuar and non-Shuar colonos of the Ecuadorian Amazon. Archives of Osteoporosis 6: 39-49. vii ACKNOWLEDGMENTS I want to express my most profound gratitude for the Shuar who participated in these studies. I wish to thank our friends in Ecuador who helped facilitated this research and spent countless hours keeping us company, especially Bertha Fernandez, Marcia Salinas, and all of our friends in the Jempekat family. In addition, special thanks are due to my SHLHP teammates, my husband Kevin, my parents, and Higgins for their support and encouragement, and to my committee for their guidance and dedication over the last six years. The research in this dissertation was supported, in part, by the Wenner-Gren Foundation for Anthropological Research (Grant #8476, 7970), the National Science Foundation (Doctoral Dissertation Improvement Grant #BCS-1341165, BCS-0824602, BCS-0925910, GRF-2011109300), the Ryoichi Sasakawa Young Leaders Fellowship Fund, and the Anthropology Department and Institute of Cognitive and Decision Sciences at the University of Oregon. viii To my colleagues, friends and family for your support, encouragement, and love. And to the coho salmon, may they forever live on in all of their resplendent beauty. ix TABLE OF CONTENTS Chapter Page I. INTRODUCTION .................................................................................................... 1 Humans as Ecosystems .......................................................................................... 3 Human/Symbiont Coevolution .............................................................................. 6 Soil-transmitted Helminths: “Old Friends” or Foes? ............................................. 8 Selection for Pathogen Avoidance: The “Behavioral Immune System ................. 17 Epidemiological Transitions .................................................................................. 20 Evolutionary Medicine and Market Integration ..................................................... 24 Immune System Dysregulation and Inflammation ................................................ 29 The Hygiene and Old Friends Hypotheses ............................................................ 31 Study Population: The Shuar ................................................................................. 39 Traditional Shuar Subsistence and Health ....................................................... 39 Market Integration and Health among the Shuar ............................................. 46 The Shuar Health and Life History Project...................................................... 47 Dissertation Objectives .......................................................................................... 53 Bridge to