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The Evolution of Extended Sexual Receptivity in Chimpanzees: Variation, Male-Female Associations, and Hormonal Correlates

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The Evolution of Extended Sexual Receptivity in Chimpanzees: Variation, Male-Female Associations, and Hormonal Correlates The Evolution of Extended Sexual Receptivity in Chimpanzees: Variation, Male-Female Associations, and Hormonal Correlates by Emily Elizabeth Blankinship Boehm Department of Evolutionary Anthropology Duke University Date:____________________ Approved: ___________________________ Anne E. Pusey, Supervisor ___________________________ Susan Alberts ___________________________ Christine Drea ___________________________ Stephen Nowicki ___________________________ Charles Nunn ___________________________ Christine Wall Dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Evolutionary Anthropology in the Graduate School of Duke University 2016 ABSTRACT The Evolution of Extended Sexual Receptivity in Chimpanzees: Variation, Male-Female Associations, and Hormonal Correlates by Emily Elizabeth Blankinship Boehm Department of Evolutionary Anthropology Duke University Date:____________________ Approved: ___________________________ Anne Pusey, Supervisor ___________________________ Susan Alberts ___________________________ Christine Drea ___________________________ Stephen Nowicki ___________________________ Charles Nunn ___________________________ Christine Wall An abstract of a dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Evolutionary Anthropology in the Graduate School of Duke University 2016 Copyright by Emily Elizabeth Blankinship Boehm 2016 Abstract Sexual conflict occurs when female and male fitness interests diverge. In a social system characterized by aggressive sexual coercion and the risk of infanticide, female chimpanzees (Pan troglodytes ) respond to this conflict by exhibiting an exaggerated sexual swelling that advertises sexual receptivity while concealing the exact timing of ovulation. Sexual swellings impose significant costs, yet can persist into pregnancy. Records from long-term studies of eastern chimpanzees (P. t. schweinfurthii ) in Gombe National Park, TZ, and Kibale National Park, UG, provide data on post-conception swellings, while data on group composition and behaviors such as mating, grooming, and aggression are drawn from the Gombe database only. Throughout, I use linear mixed models to simultaneously test multiple effects while controlling for repeated measures of individuals. In Chapter 1, I tested whether variation in females’ vulnerability to infanticide and aggression predicted the amount of swelling during pregnancy. In Chapter 2, I examined female-male relationships across reproductive states to ask whether females can better gain benefits and avoid costs by affiliating promiscuously with all males, or by investing in relationships with preferred males. Finally, I analyzed metabolites of reproductive hormones using enzyme immunoassay of urinary metabolites of reproductive hormones from pregnant females in both populations to build a hormonal profile of post-conception swellings. Swellings during pregnancy increase female-male association, and are caused by the same basic hormonal mechanism as preconception swellings, though they occur in a very different hormonal milieu. Females at greater risk iv of infanticide and intrasexual aggression swell more during pregnancy. Females mate promiscuously before conception, but during pregnancy and lactation, preferentially groom with males that are likely to protect them from aggression and infanticide. Based on these and other findings, I conclude that post-conception swellings in chimpanzees are an adaptive response to sexual conflict. v Dedication This dissertation is dedicated to Dr. Mary Ellen Newport, whose exuberance and awe for biology opened the door to my own; and to all my teachers at Maumee Valley Country Day School, who are also my family. vi Contents Abstract .............................................................................................................................. iv Dedication .......................................................................................................................... vi List of Tables ..................................................................................................................... xi List of Figures .................................................................................................................. xiii Acknowledgements ........................................................................................................... xv 1. Introduction: Deceptive signaling in mating and extended receptivity in primates ....... 1 1.1 Extended receptivity in primates ............................................................................ 3 1.2 Sexual swellings and extended receptivity in chimpanzees and bonobos .............. 7 1.3 Outline of chapters and hypotheses ........................................................................ 9 1.4 Field sites and general data collection methods ...................................................... 9 2. Variation in Post-conception Swellings Reflects Female Vulnerability to Infanticide and Aggression.................................................................................................................. 12 2.1 Introduction ........................................................................................................... 12 2.1.1 Infanticide in primates and the paternity confusion hypothesis ....................... 13 2.1.2. Intrasexual aggression in chimpanzees and the social passport hypothesis.... 15 2.1.3. Non-adaptive hypotheses for post-conception swellings ................................ 17 2.2 Methods................................................................................................................. 18 2.2.1 Assigning sexual swelling scores and conception dates .................................. 18 2.2.2 Defining trimesters ........................................................................................... 19 2.2.3 Determining immigrant status .......................................................................... 19 2.2.4 Calculating female dominance rank ................................................................. 20 2.2.5 Measures of post-conception swelling ............................................................. 20 vii 2.2.6 Estimating cycles to conception ....................................................................... 21 2.2.7 Data analysis .................................................................................................... 23 2.3 Results ................................................................................................................... 23 2.3.1 Correlation among measures of post-conception swelling .............................. 24 2.3.2 Cycles to conception ........................................................................................ 25 2.3.3 Healthy hormones hypothesis .......................................................................... 28 2.3.4 Seasonality and energetic constraints .............................................................. 32 2.3.5 Paternity confusion and social passport hypotheses ........................................ 33 2.4 Discussion ............................................................................................................. 40 2.4.1 Evaluating the paternity confusion hypothesis ................................................ 40 2.4.2 Evaluating the social passport hypothesis ........................................................ 42 2.4.3 Evaluating the healthy hormones hypothesis ................................................... 43 2.4.4 Evaluating the energetic constraints hypothesis .............................................. 44 2.4.5 Other potential explanations: The cost-of-sexual-attraction hypothesis .......... 45 3. Promiscuity or Partner Preference? Male-Female Interactions Across Reproductive States Reflect Female Strategies for Avoiding Aggression .............................................. 47 3.1 Introduction ........................................................................................................... 47 3.1.1 Costs to estrous females and the risk of infanticide ......................................... 48 3.1.2 Benefits of sociality and strategies for avoiding aggression ............................ 50 3.1.3 Kin recognition and paternal care in primates ................................................. 51 3.1.4 The promiscuity hypothesis ............................................................................. 52 3.1.5 The protection hypothesis ................................................................................ 53 3.2 Methods................................................................................................................. 55 viii 3.2.1 Determining paternities .................................................................................... 55 3.2.2 Defining time periods ...................................................................................... 56 3.2.3 Measures of Dyadic Association ..................................................................... 57 3.2.4 Calculating half-weight index of dyadic association ....................................... 57 3.2.5 Calculating grooming association index .......................................................... 58 3.2.6 Calculating rates of aggression ........................................................................ 59 3.2.7 Calculating rates of mating .............................................................................
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