Track 1: The ecology & evolution of social structure & 'social distancing'

In humans and other group-living animals, ‘social structure’ is the outcome of the patterning and distribution of social interactions among individuals to maximize the benefits of group-living (e.g. defense, cooperation) while minimizing its costs (e.g. competition, disease risk). Despite profound inter- and intra-species variation in social structure, the causal factors of such variation remain unclear, with explanations based on species’ evolutionary history, degrees of relatedness or kinship, and adaptations to current socio-ecological conditions like resource distribution, predation, and disease risk having all been proposed to play a role.

My past research, funded by the National Science Foundation (NSF DDIG #1231145), offered insights into the evolutionary and socio-ecological underpinnings of macaque social structure. Across 10 species of macaques, I established that some aspects of social structure related to macaques’ dominance hierarchies showed strong ‘phylogenetic signals’, i.e. were more similar among closely related compared to distantly related species. On the other hand, other aspects such as the patterning and disttibution of their affiliative grooming relationships, showed weak phylogenetic signals. Moreover, my research on both wild Tibetan macaques (M. thibetana) at Mt. Huangshan, China, and on free-ranging rhesus macaques (M. mulatta) at Cayo Santiago, revealed that the patterning and distribution of grooming relationships were strongly influenced by variation in the availability of food resources, which in turn governed the exchange of cooperative exchange of benefits (e.g. giving grooming for receiving support during conflicts, tolerance while feeding) in these primate groups based on economic laws such as ‘supply-and-demand’. Specifically, I revealed evidence for such ‘biological markets’. Together, these findings revealed that while some aspects of primate social structure seemed more evolutionarily stable strategies, others were more labile or flexible to variation in current socio-ecological conditions.

Current & future research: Aside from resource distribution, other ecological factors like disease pressure, through influencing animals’ decision-making in social contexts, may also influence the patterning and distribution of affiliative interactions. In this regard, group-living animals may show a range of different social responses to disease pressure, from care-giving, to passive self-isolation, to strategies like active self-isolation, avoidance, and exclusion that characterize ‘social distancing’. My current research, following the recent establishment of a collaboration with other research groups from the University of Ulm, University of Cambridge and University of Zurich conducting research at the Kalahari Research Centre (KRC: https://kalahariresearchcentre.org/ ), is aimed at assessing evidence for disease-coping social strategies among wild meerkat populations that have been repeatedly exposed to epidemics of tuberculosis (Tb) caused by an endemic Mycobacterium spp. After prolonged and unpredictable latent phases, Tb infection, characterized by disease symptoms of submandibular swellings and lesions on the cheeks, causes severe illness and mortality among meerkats. I am therefore currently examining evidence (or lack thereof) of longitudinal changes in meerkats’ social network connectedness across pre- versus post-infection periods that are suggestive of care-giving among closely-related individuals, versus ‘social distancing’ strategies among distant relatives or non-relatives. Future work will adopt cross-species phylogenetic comparative approaches, to disentangle the relative effects of social (e.g. degrees of relatedness among individuals, complexity of social organization) and pathogen-specific (mode of transmission, reproduction number or R0, host-specific virulence) characteristics on commonly used disease-coping strategies. The findings will provide key insights into the evolutionary and (mal)adaptive underpinnings of ‘social distancing’ in humans. 

Track 2: exposure and susceptibility as the ‘twin pillars’ of disease transmission 

The strength and diversity of animal social relationships strongly influences health outcomes, but not always in expected ways. A case in point is the adaptive relationship between social life and disease risk. Most epidemiological frameworks argue that disease risk is a major cost of group living in wildlife -- possessing more social connections makes individuals more susceptible to acquiring pathogens through social contact. Yet in strongly bonded animal societies like many wild primates (e.g. chimpanzees, macaques, humans), strong affiliative social connections may lower stress levels and enhance their immune function, and thereby socially buffer individuals against acquiring infectious agents.

Track 3: Understanding the hidden dimensions of human-wildlife interfaces as 'Coupled Natural & Human Systems' 

The global expansion of human populations and the consequential ‘carbon footprint’ during the Anthropocene has increased wildlife exposure to anthropogenic factors such as climate change, land-use change, and contact with humans and livestock. Given the now well-established evidence for human-wildlife interfaces to function as hotspots for disease risk, assessing such risk and its behavioral and environmental underpinnings is one of the most pressing conservation and public health concerns of the 21st century. Yet one major challenge facing such research pertains to the implementation of a consensual theoretical framework to understand human-wildlife juxtaposition and interactions, and in turn their long-term effects on wildlife and people. 

One approach to address the above gaps involves implementing conceptual frameworks of Coupled Natural and Human Systems (or CNHS). Per these frameworks, research on human-wildlife interactions can aim to reach beyond the interface, by considering and evaluating the feedback mechanisms and effects of interactions on long-term stability and homeostasis of both humans and wildlife. 

In 2016 I successfully applied to (as co-PI) an NSF Dynamics of Coupled Human-Natural Systems Grant (NSF#151855), to conduct long-term, comparative assessments of interactions between anthropogenic factors and macaque populations and species across South and South-East Asia, specifically rhesus macaques in Northern India, long-tailed macaques (M. fascicularis) in Malaysia, and bonnet macaques (M. radiata) in Southern India. Over the past five years this research has implemented a CNHS framework to assess the impact of interactions with humans on aspects of macaque ecology and social behavior, and reciprocally on the impact of macaque-specific demographic characteristics and social status on their propensities to take risks by engaging with humans. Currently I am also using approaches of ‘conservation psychology’, to assess the impact of human-macaque interactions on human behavior, specifically on inter-individual differences in implicit and explicit attitudes, beliefs and experiences towards wildlife.

Current and future directions: Tp pursue new trajectories of research stemming from the CNHS project, I have established external collaborations independent of my postdoctoral work - specifically with the EcoHealth Alliance in New York and Bangladesh, the Kalahari Research Centre in South Africa, and other independent researchers at UC Davis, University of Cambridge, University of Ulm, and the University of Zurich. These efforts are currently focusing on examining the impact of behavioral and environmental aspects of human-wildlife CNHS, on the co-occurrence and community ecology of pathogenic and commensal microbes.

Specifically I am implementing the principles of community ecology to disentangle the relative effects of anthropogenic, socio-ecological, and microbe-specific factors on the co-occurrence and community structure of microbes among hosts. Among wild rhesus macaques in Bangladesh, my recent work implementing a combination of cutting-edge SNA tools and macroecological Joint Species Distributions Models (JSDMs) revealed a strong impact of anthropogenic factors (human and livestock densities), social organization (individuals’ group membership, and inter-population geographic distances) on the co-occurrence and assemblages of Enteroviruses. In doing so the work is providing crucial insights into a changing perspective of viruses as being embedded components of human-natural systems, rather than as external agents that merely cause disease within such systems.

I am also currently conducting similar research on wild meerkats at the KRC, but to disentangle the relative effects of exposure to climate change (longitudinal changes to temperature, rainfall), land-use changes, and aspects of individual animals’ life-history (body-weight, diet) and social life (dominance status, connectedness in kinship and social networks), on the co-occurrence of pathogenic MTBC bacteria with commensal gut microbiota. The work is providing a holistic picture of the deterministic factors that influence the prevalence and progression of endemic Tb in a group-living animal society, and thereby should naturally inform similar assessments in human systems.

In the longer-term, my work will build on these on-going projects, by focusing more on ecosystem-level effects. For instance, projects will be aimed at understanding the inter-relationships between microbial co-occurrence and host social and ecological interactions, using multi-level or multiplex network approaches that capture animals’ social interactions with their conspecifics, and their ecological interactions and overlap with other biotic environmental components such as humans, other wildlife, livestock, and feral mammals. A key aspect of this research would also involve the inclusion of a human social component, i.e. understand how socio-economic factors in (peri)urban environments such as income inequality, red-lining and other divisive constructs in countries such as South Africa and Bangladesh, may impact human-wildlife interactions and disproportional vulnerability. From ‘One Health’ perspectives, these efforts would inform interventions that move the outcomes of human-wildlife interactions from conflict towards co-existence, at these and other locations.