Nicole Thompson
Ph.D. 2018
Social ties over the life cycle in blue monkeys
Dissertation Abstract:
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.
Publications based on dissertation work:
Thompson, N.A. & Cords, M. 2018. Stronger social bonds do not always predict greater longevity in a gregarious primate. Ecology and Evolution 8:1604–1614.
doi: 10.1002/ece3.3781
Cords, M. & Thompson, N.A. 2017. Friendships, coalitions, and alliances. In: American Psychological Association Handbook of Comparative Psychology,
Call, J., Burghardt, G.M., Pepperberg, I., Snowdon, C. & Zentall,
T. eds. Washington, D.C.: American Psychological Association, pp.
899-914.
Thompson, N.A.,
Higham, J.P., Heisterman, M., Vogel, E., Cords, M. 2019. Energy balance
but not competitive environment corresponds with allostatic load during
development in an Old World monkey. Hormones and Behavior 108: 30-41. doi.org/10.1016/j.yhbeh.2018.12.014
After graduation, Nicole became a post-doc at the University of New Mexico.
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