The costs and benefits of sociality in semi-free ranging Barbary macaques (Macaca sylvanus)
von Nadine Müller
Datum der mündl. Prüfung:2018-08-07
Betreuer:Prof. Dr. Julia Ostner
Gutachter:Dr. Oliver Schülke
Gutachter:Prof. Dr. Lars Penke
EnglischParasite infections are ubiquitous throughout the animal kingdom, and increased risk of parasite transmission has been suggested as one of the major costs of group living. With bigger group size and higher interaction frequencies, transmission is expected to increase due to higher pathogen exposure. In contrast, social integration and close affiliative relationships are known predictors of increased health, longevity and reproductive success in social animals. Sociality is thus hypothesized to offer fitness benefits by improving health, including reduced susceptibility to infectious diseases. The underlying mechanisms mediating the health benefits of social interactions are still largely unclear, particularly in wildlife. Recent methodological and theoretical advances in the fields of disease ecology and eco-immunology make studying the links between host sociality and parasites more feasible. Consequently, understanding host-parasite dynamics and the role of sociality for health has received increasing attention in behavioural ecology and evolutionary biology. Gastrointestinal (GI) helminths are a powerful tool to study the links between sociality and health, as they can be assessed noninvasively. However, host-parasite interactions are complex and can function as feedback loops: parasites alter their host’s physiology and behaviour, which in turn predict exposure and susceptibility to parasite infection. Often the directionality of the links between host behaviour, sociality and physiology and infection isn’t clear due to the correlational nature of conducted studies. Additionally, host behaviour can contribute to both exposure and susceptibility simultaneously and both factors can be intertwined, so understanding the role of sociality for parasite transmission is challenging. In this thesis I investigate the host-parasite dynamic between GI helminth infections and a social primate, the Barbary macaque (Macaca sylvanus), aiming at understanding the causes and consequences of GI helminth infection. Capitalizing on strongyle nematode clearance by routine anthelmintic treatment in a semi-free ranging population, I can take a step beyond correlational studies and draw more causal inferences about the direction of host-parasite interactions, placing a special focus on social behaviour. I combine behavioural observation data (~ 3500 hours) with analyses of molecular markers of immune regulation (urinary neopterin, uNEO), physical condition (urinary C-peptide, uCP) and hypothalamic-pituitary-adrenal (HPA) axis activation and parasite status assessment. This enables me to assess the consequences of parasite clearance and investigate the predictors of reinfection with GI helminths. To account for uncertainty of noninvasively assessed parasite status, I use patch occupancy modelling to estimate infection probabilities and individual reinfection risk. I test whether infection related behavioural changes are attributable to sickness behaviour or avoidance of infected conspecifics to extrapolate the impact of GI helminth infections on social behaviour and potentially evolution. With regard to parasite transmission, I test whether grooming predicts reinfection risk, indicating transmission due to social contact. Strongyle nematode infections, mostly caused by Oesophagostomum spp., were ubiquitous within the study population, with generally low egg shedding and large inter-individual variation in reinfection risk. Infections did not cause overt symptoms or affect physical condition. They nonetheless elicited sickness behaviour responses, namely increased HPA axis activation in combination with reduced activity. Anthelmintic treatment did not alter uNEO levels, but uNEO increased with age, implying immunosenescence. As coinfections with further GI helminths occurred mostly in old individuals, immunosenescence might influence an individual’s ability to cope with GI helminth infections in general. Individual frequency to initiate proximity to others was not predicted by an individual’s, but by the potential partner’s infection status, indicating avoidance of infected individuals. Reinfection was predicted by measures of both susceptibility and exposure. The strongest predictor of earlier reinfection was coinfection with further GI helminth taxa. I found no evidence for HPA axis activation and immune function as strong predictors of reinfection. Being in good physical condition tended to increase reinfection risk, indicating the presence of parasite tolerance strategies in Barbary macaques. Time spent in areas likely contaminated with faeces, a measure of exposure to infective parasite stages, emerged as a predictor of increased infection risk, confirming the direct environmental transmission route of strongyle nematodes. High social bond strength with opposite sex partners decreased reinfection probability, probably due to reduced susceptibility resulting from immunomodulatory effects of affiliative interactions. In contrast, grooming a high number of partners and strong bonds with same sex partners emerged as predictors of increased infection probability, implying a social component of transmission. Social interactions can thus have an ambivalent effect, contributing to both protection from and increased risk of GI helminth infections. The discrepancy between same and opposite sex bond effects is likely attributable to differences in interaction patterns, resulting in different relative contributions of same and opposite sex bonds to exposure and susceptibility. In conclusion, the results suggest that GI parasite infections can influence social behaviour in nonhuman primates. Given the dual role of social interactions for GI helminth transmission, a possible strategy to maximize benefits while limiting costs of sociality could be selective formation of strong bonds with a small number of partners, with the caveat that particular interaction patterns might be more beneficial than others. My results lead to a range of questions which need to be addressed by future research, particularly whether primates mitigate costs of infection by employing tolerance strategies. Causally linking components of social behaviour to exposure and susceptibility will be important for understanding individual variation in infection risk and contribution to transmission through a population. Investigating whether variation in responses to GI helminth infections predict long-term health and fitness outcomes will be vital to assess the impact of host-parasite dynamics on behaviour and potentially host social evolution.
Keywords: Macaques; Social relationships; Parasites; Physiology; Exposure; Susceptibility; anthelmintic treatment; Parasite transmission; Immunemarker; Wildlife health