Caitlin Barale, ID# 26907
LEAKEY FOUNDATION FINAL GRANT REPORT Summary of results My dissertation research focused on the juvenile period in geladas (Theropithecus gelada): the normative patterns of behavior and hormones during this understudied age group, the ontogeny of male-male bonds, and the overall effect of juvenile sociality and social development on dispersal and reproductive strategies. As expected, we documented an agerelated decrease in play but not grooming in both males and females, sex differences in the number of playmates and amount of time spent playing during the juvenile period, and a difference in grooming partner identity for males and females. We also found a U-shaped pattern in testosterone in juvenile males, analogous to that seen in juvenile male baboons. Our investigation into the formation of male-male bonds revealed a preference for same-age kin, although it is not clear that these bonds persist beyond the juvenile period as many males disperse alone. Importantly, we are finding a connection between dispersal strategy, dispersal timing and social integration, with more highly integrated males dispersing later and to bachelor groups and more isolated males dispersing earlier and to one-male units. Similarities between the gelada and human juvenile period make this project particularly relevant to humans. Like human children, and unlike most other primates, juvenile geladas interact socially with both relatives in their family unit and unrelated age-mates from outside their natal unit. Like human children, juvenile geladas return to their natal unit throughout the day and each night, and may behave differently with their peers and kin. Each natal unit has a unique combination of adults and juveniles, personalities and parenting styles. Thus, juveniles in the same peer group may experience very different social conditions. Our work examins the effects of these early social conditions on dispersal timing, dispersal strategy, and adult reproductive strategy, and will ultimately help provide a model for predictions about human development. Our work additionally provides a female-philopatric model for the development and function of male-male bonds, a valuable addition to a literature primarily focused on malephilopatric species. Publication plans We are currently writing up our results with the intent of publishing each chapter of the dissertation in a peer-reviewed journal in the coming year. Three papers (juvenile period patterns, utility of social networks, and patterns in juvenile gelada hormones) are in preparation, with at least three other papers being drafted. Detailed description of results First, we described sex differences and the normative trends in social behavior during the juvenile period for both male and female geladas. We also investigated play and grooming partner preferences for both males and females. We found that total social time does not vary with age or sex until age 5, at which point females socialize more than males (Figure 1). However, when the two components of gelada social behavior, play and grooming, are considered separately it become apparent that males and females differ in how they allocate their social time throughout the juvenile period. Play declines with age in both males and females, from a maximum at ages 0-1 to a minimum near zero by age 3 in females and age 6 in males (Figure 2). The decline is faster in females, and males play significantly more than females from ages 1-5. Grooming, in contrast, does not vary by sex until age 5, at which point females groom significantly more than males (Figure 3). The only age related difference in grooming rates is a significant increase in
Caitlin Barale, ID# 26907
grooming between ages 0-1 and all later age groups. The number of unique playmates an individual has declines with age in both males and females and stabilizes at 1-2 in females and 23 in males, approximately one year before maturity is reached (Figure 4). There is no difference in the number of grooming partners an individual has by sex or age, except for males age 0-1 who have significantly fewer grooming partners than all other age and sex groups (Figure 5). However, a sex difference does exist in type of grooming partner: males groom significantly more than females with extra-unit (unrelated) individuals beginning at age 1 (Figure 6, top panel). There is no sex difference in the fraction of time spent grooming with either mothers (which decreases with increasing age) or with unit individuals (with increases with increasing age) (Figure 6, bottom and middle panels). Sex differences are also present in juvenile partner preference in both play and grooming. In both social contexts, males prefer to play with other males of the same age. Females, on the other hand, show no preference for age or sex in play partners. Females prefer male grooming partners, and also are more likely to groom juveniles outside their age group. In particular, juvenile females choose infants as grooming partners. We are still waiting for genetic data to come back from the lab, but early results suggest a strong preference for relatives as partners for both males and females. The sex differences that exist in the juvenile period are indicative of sex-specific paths taken by adult male and female geladas. At the end of the juvenile period, male geladas disperse from their natal units and join either other one-male units or all-male bachelor groups. From there, they compete via physical fighting for control of and reproductive access to units of adult females. Consequently, we expect males to use their juvenile period for physical skill training, alliance building, and assessment of related and unrelated competitors (Bekoff, 1984; Caro, 1988; Pereira & Fairbanks, 2002). These hypotheses are confirmed in the trends in social behavior described above. Juvenile males exhibit high rates of play and grooming, a larger number of play partners than females, a preference for same-sex and same-age social partners (potential competitors), and an increasing interest in extra-unit/unrelated grooming partners as males approach dispersal. In contrast to males, female geladas remain in their natal unit for their entire life. They establish and maintain grooming bonds with a small number of female relatives, and spend their adult lives raising offspring and interacting primarily with other females and the leader male of their unit. High grooming rates (particularly as young adults), low and rapidly declining play rates and a limited number of closely-related play partners, an emphasis on kinbased grooming relationships, and an attraction to infants all point to the common themes of adult female life. Next, we documented the pattern of testosterone levels in males across the juvenile period (Figure 7). We found that the highest levels of testosterone metabolites are seen during the first year of life. Metabolite concentrations decline from birth to age 3, when they reach their lowest levels. From age 3 to 7.5, testosterone concentrations gradually increase again, although they do not reach the levels seen during infancy. Sexual maturation in the form of testes, cheek tuft and canine development occurs during this time, as does dispersal, a behavioral maturational milestone. By age 7.5, gelada males are considered full adults – they have a full cape, welldeveloped cheek tufts, and have achieved their adult size and weight. From this age onwards, testosterone metabolite concentrations plateau and remain relatively stable. This pattern mirrors that seen in juvenile baboons (Gesquiere et al., 2005). Finally, we investigated the relationship between individual variation in juvenile social integration and the adoption of particular dispersal and reproductive strategies. This work is still
Caitlin Barale, ID# 26907
on-going, and we will finish the analyses in the next two months. Although it seems that specific pair bonds do not persist across the dispersal transition, as many individuals disperse alone or to distinct groups from their juvenile partners, the degree to which an individual is integrated into his juvenile networks is an important indicator of his dispersal and reproductive strategy. At this point, we have established that individual male geladas vary in the degree to which they are embedded in play and grooming networks, and that this variation is individually stable from one year to the next. Males who are highly integrated into the play network (have many unique play partners, are highly connected, connect subgroups, etc.) fill the same position as they mature. Males who are socially isolated remain socially isolated. From this knowledge, we are pursuing two lines of questioning. First, what factors of early life (group size, maternal dominance rank, maternal reproductive experience, sex ratio in group, etc.) could drive the development of individual variation in social integration? Second, is variation in social integration indicative of dispersal timing and strategy (as suggested by Bekoff’s social cohesion hypothesis (Bekoff, 1977)), and does it reveal the reproductive path males will ultimately take and thus give some indication of lifetime reproductive success? Preliminary results on a partial data set suggest that early social context is important and that maternal rank and group size are predictors of social integration, with sons of high ranking mothers and males in large groups being consistently more integrated than their counterparts. Additionally, it appears that socially isolated males disperse early and to one-male units while socially integrated males disperse at older ages and transfer to all-male bachelor groups. This result is in keeping with Bekoff’s original theory, as well as more recent work on individual variation and dispersal (Blumstein, Wey, & Tang, 2009; Cote, Clobert, Brodin, Fogarty, & Sih, 2010; Harcourt & Stewart, 1981; Harris & White, 1992). However, these results are preliminary and we are continuing to investigate them with a larger dataset and more dispersal data. Works Cited Bekoff, M. (1977). Mammalian dispersal and the ontogeny of individual behavioral phenotypes. The American Naturalist, 111(980), 715–732. Bekoff, M. (1984). Social play behavior. BioScience, 34(4), 228–233. Blumstein, D. T., Wey, T. W., & Tang, K. (2009). A test of the social cohesion hypothesis: interactive female marmots remain at home. Proceedings of the Royal Society B: Biological Sciences, 276(1669), 3007–3012. Caro, T. M. (1988). Adaptive significance of play: are we getting closer? Trends in Ecology and Evolution, 3(2), 50–54. Cote, J., Clobert, J., Brodin, T., Fogarty, S., & Sih, A. (2010). Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations. Philosophical Transactions of the Royal Society of London - Series B: Biological Sciences, 365(1560), 4065–4076. Gesquiere, L. R., Altmann, J., Khan, M. Z., Couret, J., Yu, J. C., Endres, C. S., … Wango, E. O. (2005). Coming of age: steroid hormones of wild immature baboons (Papio cynocephalus). American Journal of Primatology, 67(1), 83–100. Harcourt, A. H., & Stewart, K. J. (1981). Gorilla male relationships: Can differences during immaturity lead to contrasting reproductive tactics in adulthood? Animal Behaviour. Harris, S., & White, P. C. L. (1992). Is reduced affiliative rather than increased agonistic behaviour associated with dispersal in red foxes? Animal Behaviour, 44(6), 1085–1089. Pereira, M. E., & Fairbanks, L. A. (2002). Juvenile primates: life history, development, and behavior (2nd ed.). Chicago: University of Chicago Press.
Caitlin Barale, ID# 26907
Figures Figure 1: social behavior time budget by age and sex
Total social behavior by age and sex *"
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percent of time spent in social behavior
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Figure 2: play time budget by age and sex
Play time budget by age and sex 12
percent of time spent playing
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6 females males
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0 0
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age, years
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Caitlin Barale, ID# 26907
Figure 3: grooming time budget by age and sex
Figure 4: average number of unique playmates by age
Caitlin Barale, ID# 26907
Figure 5: Average number of unique grooming partners by age and sex
Figure 6: grooming partner type by age and sex
Caitlin Barale, ID# 26907
Figure 7: residual testosterone level by age class (sample size above each category)