Networks of Indirect Contact Promote Spread of an Environmentally Transmitted Pathogen in a Highly Social Species

In group-living species, social behaviors, including non-contact territorial defense, may decrease the risk of pathogen transmission and spread by reducing contact among conspecifics, yet these strategies may paradoxically increase opportunities for transmission in some host-pathogen systems. We explore how social behaviors shape direct and indirect pathogen transmission of the emerging Mycobacterium tuberculosis complex (MTBC) pathogen M. mungi in banded mongooses (Mungos mungo). Using empirical behavioral data from a banded mongoose population in Uganda, we constructed social network models that incorporate observed intra-group contacts and simulated inter-group scent marking scenarios. These models show that indirect transmission can play a pivotal role, particularly when per-contact transmissibility is low. Simulations predicted increased population-level spread via socially directed, environmentally mediated pathways, while population-level invasion potential remained relatively unchanged. These results underscore the need to incorporate all transmission modes when modeling disease spread in social networks. We further emphasize the importance of considering the temporal dynamics of indirect transmission, including the persistence of both olfactory secretion and infecting pathogens deposited in the environment. For mixed transmission systems, fully accounting for both direct and indirect transmission mechanisms may be essential for characterizing disease spread, even when direct transmission pathways dominate. Our findings suggest that pathogens that exploit socially directed environmental transmission pathways may gain an evolutionary advantage, circumventing social barriers thought to have evolved to constrain pathogen spread.