The manifestations and interdependence of social and physiological aging in wild female Assamese macaques (Macaca assamensis)
Dissertation
Datum der mündl. Prüfung:2023-05-09
Erschienen:2023-12-11
Betreuer:Prof. Dr. Julia Ostner
Gutachter:Dr. Oliver Schülke
Gutachter:Prof. Dr. Susann Boretius
Dateien
Name:Baptiste Sadoughi_Doctoral Thesis_2023_EDISS.pdf
Size:2.36Mb
Format:PDF
Description:Published doctoral thesis version
Zusammenfassung
Englisch
Aging is a multifaceted process which increases the probability of death, and although there can be only one outcome, the ways to get there are diverse. Accumulating evidence of aging in natural animal populations has shed light on this diversity, both across and within species, but we still have little knowledge of the opportunities, constraints and trade-offs faced by individuals as they go through this ultimate life-history stage. Specifically, it remains unclear which individual traits exhibit signs of aging, how individuals may adjust their behavior in response to physiological decay, and how, together, these changes may ultimately contribute to whole-organism aging. As such, investigating age-related changes in social behavior and physiological functions is imperative to reach a more holistic understanding of aging. A key issue in addressing social and physiological aging is the strong association between sociality and health. Social bonds, social integration, and exposure to social adversity are important predictors of health and lifespan across mammals. As some of the physiological mechanisms underlying the connections between sociality and health are uncovered, it becomes especially clear that aging of one component may influence aging in the other. Yet, the interdependences between sociality and physiology have seldom been addressed in the study of aging, due partly to a lack of detailed data on social behavior in natural populations of long-lived species. Another difficulty arises from the need to assess physiology via markers measured from non-invasively collected samples. Finally, although aging is an individual-level process, demographic and cohort effects can influence the patterns of aging uncovered in cross-sectional studies, which calls for a longitudinal approach. In this thesis, I investigate age-related changes in social and physiological traits in wild female Assamese macaques (Macaca assamensis) to address key questions at the crossroad of aging, sociality, and health in natural animal populations: Does social behavior exhibit age-related changes? Which physiological systems, at the interface with sociality, should be investigated for age-related changes? Does social aging influence the manifestations of aging in physiological traits, and vice versa? Can biomarkers of energetic state provide means of non-invasively investigating the physiological constraints on social behavior under field conditions? To investigate these issues in the female Assamese macaques, I use extensive behavioral data, and a review of the mechanisms linking sociality and health in non-human primates, after which I focus on the HPA axis and the gut microbiome as key physiological systems. Finally, I validated the non-invasive measurement of markers of metabolic activity in macaques to offer perspective to explore the causal path from physiology towards sociality. My results show that female Assamese macaques experience both social and physiological aging. Females decreased their social engagement and reduced the size of their grooming network with advancing age. This phenomenon could not be explained by a lack of opportunities to interact and was not associated with a greater tendency to focus on preferred partners with age. In addition to within-individual age effects, cross-sectional aging dynamics were influenced by demographic processes consistent with the selective disappearance of poorly socially connected individuals. Together, these results highlight the contribution of within-individual and demographic processes to group-level social aging and do not support increasing social selectivity as the primary driver of social disengagement in this population. For physiological traits, I find trait-specific aging patterns, across and within traits. HPA axis activity assessed from fecal glucocorticoid concentrations was not associated with age, neither before nor after accounting for the strength of individuals’ strong bonds. The taxonomic diversity of the gut bacterial community was not associated with age, and age was not a consistent predictor of gut bacterial composition across individuals. However, the gut bacterial composition exhibited a personal signature which became less stable and increasingly personalized with age. A decrease in the social transmission of gut bacteria may have contributed to, but was not sufficient to explain, the age-related patterns uncovered here. The validation of markers of metabolic activity was conducted via a food restriction experiment in captive macaques and assessed urinary concentrations of triiodothyronine and cortisol. Both hormones exhibited the predicted change with a decrease in triiodothyronine and an increase in cortisol during the restriction phase of the experiment. Furthermore, variation in urinary triiodothyronine concentrations correlated positively with variation in body mass. Concentrations of urinary triiodothyronine were reasonably robust to many issues associated with collection of samples under field conditions, making it a suitable non-invasive marker of energetic state in macaques. In conclusion, in female Assamese macaques, age is associated with progressive social disengagement and modifications in several aspects of the gut bacterial communities, whereas glucocorticoid concentrations appear constant over adulthood. The characterization of consistent aging patterns across individuals in a population is a necessary step in understanding the opportunities, constraints, and potential trade-offs that individuals face. As such, my thesis contributes to the growing field of biogerontology. Future research should investigate how individuals differ from the average trajectories and consider potential age-specific optima, in a diversity of systems, to advance our understanding of the links between sociality, health, and aging.
Keywords: senescence; functional aging; social aging; aging gut; primate; cercopithecines; Macaca assamensis; wild animal population; behavior; female-female bonds; social selectivity; gut microbiome; non-invasive metabolic markers; thyroid hormones; glucocorticoids