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Download File Social Ties over the Life Cycle in Blue Monkeys Nicole A. Thompson Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy of the Graduate School of Arts and Sciences COLUMBIA UNIVERSITY 2018 © 2018 Nicole A. Thompson All rights reserved Abstract Social Ties over the Life Cycle in Blue Monkeys Nicole A. Thompson The ways that individuals socialize within groups have evolved to overcome challenges relevant to species-specific socioecology and individuals’ life history state. Studying the drivers, proximate benefits, and fitness consequences of social interaction across life stages therefore helps clarify why and how social behavior has evolved. To date, juvenility is one life stage that field researchers have largely overlooked; however, individual experiences during development are relevant to later behavior and ultimately to fitness. Juvenile animals are subject to unique challenges related to their small size and relative inexperience. They are likely to employ behavioral strategies to overcome these challenges, while developing adult-like behavioral competence according to their species and sex. The research presented in this dissertation draws from long-term behavioral records of adult females and shorter-term behavioral records of juveniles from a population of blue monkeys ( Cercopithecus mitis stuhlmanni ) in western Kenya. I combine data on social behavior, demography, and biomarkers related to energetic and metabolic status, to assess both short and long term corollaries of social strategies in this gregarious Old World primate. I first explored whether the quality of social ties predicted longevity among adult female blue monkeys. Controlling for any effects of dominance rank, group size, and life history strategy on survival, I used Cox proportional hazards regression to model the both the cumulative and current relationship of social ties and the hazard of mortality in 83 wild adult females of known age, observed 2-8 years each (437 subject-years) in 8 social groups. The strength of bonds with close partners increased mortality risk under certain conditions: females that had strong bonds with partners that were inconsistent over multiple years had a higher risk of mortality than females adopting any other social strategy. Within a single year, females had a higher risk of mortality if they were strongly bonded with partners that were inconsistent from the previous year vs. with partners that were consistent. Dominance rank, number of adult female group-mates, and age at first reproduction did not predict the risk of death. This study demonstrates that costs and benefits of strong social bonds during adulthood can be context-dependent, relating to the consistency of social partners over time. To understand the adaptive value of social behavior among juveniles, it was first necessary to understand the conditions under which their social behavior occurred and with which it co-varied. I examined the social behavior of 41 juvenile blue monkeys, using data collected over 8 consecutive months. I analyzed variation in social activity budgets and partner number related to life history characteristics, socio-demographic conditions, and seasonal environmental change. I examined partner preferences according to kinship, and relative age and rank. Lastly, I explored the stability of juvenile social tendencies over time. Males and females differed strongly in their social activity budgets and partner numbers: males spent more time playing with more partners than females, whereas females spent more time grooming and sitting close with more partners than males. Nevertheless, they were much more similar in terms of their partner preferences. Juveniles generally preferred to interact with partners with whom they were closely related and that were similar in age and maternal rank. Juveniles’ affiliative and aggressive behavior varied seasonally, suggesting that these two types of behavior were related. Rates of agonism given and received were the only types of social behavior to demonstrate repeatable inter-individual differences. This analysis provides a comprehensive examination of juvenile behavior in blue monkeys, synthesizing findings with those in other primate and non-primate species. I then explored the short-term costs and benefits of juveniles’ sociality in terms of their effects on allostatic load. I examined variation in energy balance (as measured by urinary C-peptide), social style, and their influences on allostatic load (as measured by fecal glucocorticoid metabolites, fGCs). Juvenile energy balance varied according to sex, availability of ripe fruit, and rainfall. Both energy balance and social style predicted fGC levels, such that juveniles that had a higher energy balance, groomed less, and played more had lower fGCs. Time spent grooming interacted with energy balance in their effect on fGCs, such that individuals with higher energy balance actually had higher fGCs the more time they groomed. Neither maternal rank nor involvement in agonism corresponded with juvenile fGC levels. These results suggest that juvenile blue monkeys experience energetic stressors and that navigating the social environment via overt affiliative behavior, namely grooming, is a potentially stress-inducing endeavor. Lastly, to further understand variation in social behavior during juvenility, I explored the role of mothers in shaping juveniles’ affiliative tendencies. I examined whether the social behavior of juvenile animals resembled that of their mothers and whether their social behavior was subject to maternal effects, using data from the 41 juveniles and their 29 mothers. Juveniles’ grooming time with peers corresponded with the amount of time they groomed with (primarily being groomed by) mothers as infants, and this relationship varied by sex. Females spent less time grooming with peers the more maternal grooming they received during infancy, whereas males groomed with peers more. The time juveniles spent in other types of association with partners did not correspond with the same behavior in mothers, nor were other types of association subject to maternal effects. This exploratory study suggests limited effects of maternal behavior during infancy, but also that females and males respond differently to maternal investment during the first year. The results of this dissertation emphasize the importance of long-term studies of natural populations in understanding the evolution of social behavior, particularly when examining the causes and consequences of social ties over the life cycle in a long-lived animal. Strategies of affiliation did indeed correspond with costs and benefits over the life cycle, as they were relevant both to mortality in female adults and metabolic hormones among juveniles. Further, individuals socialize during development according to their life trajectory as male or female, what seasonal changes in the physical environment require or allow, and early-life maternal effects. Table of Contents List of Tables and Figures ............................................................................................... iv Acknowledgments .......................................................................................................... viii Dedication ......................................................................................................................... xi Chapter 1: Understanding the fitness benefits of social connectionover the life cycle. ............................................................................................................................................. 1 Introduction ..................................................................................................................... 1 Issues Related to the Definition and Measurement of Social Connections .................... 3 Pathways of Connections’ Benefits .............................................................................. 13 The Physiological and Developmental Bases of Connections ...................................... 36 Summary and Future Directions ................................................................................... 41 Chapter 2: Stronger Social Bonds Do Not Always Predict Greater Longevity in A Gregarious Primate ........................................................................................................ 43 Abstract ......................................................................................................................... 45 Introduction ................................................................................................................... 46 Materials and methods .................................................................................................. 50 Results ........................................................................................................................... 59 Discussion ..................................................................................................................... 67 Conclusions ................................................................................................................... 71 Acknowledgments......................................................................................................... 72 Supplemental Information ............................................................................................ 74 Chapter 3: Socio-ecological drivers of social behavior during development in blue monkeys. .........................................................................................................................
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