Modification of host social networks by manipulative parasites

Abstract

Social network models provide a powerful tool to estimate infection risk for individual hosts and track parasite transmission through host populations. Here, bringing together concepts from social network theory, animal personality, and parasite manipulation of host behaviour, I argue that not only are social networks shaping parasite transmission, but parasites in turn shape social networks through their effects on the behaviour of infected individuals. Firstly, I review five general categories of behaviour (mating behaviour, aggressiveness, activity levels, spatial distribution, and group formation) that are closely tied to social networks, and provide evidence that parasites can affect all of them. Secondly, I describe scenarios in which behaviour-altering parasites can modify either the role or position of individual hosts within their social network, or various structural properties (e.g., connectance, modularity) of the entire network. Experimental approaches allowing comparisons of social networks pre- versus post-infection are a promising avenue to explore the feedback loop between social networks and parasite infections.

The importance of individual‐to‐society feedbacks in animal ecology and evolution

“…Specifically, can pathogens change the dynamics of social interactions within a group by selecting for social connections based on specific health traits of potential associates, thus leading to a clustered structure driven by the host–pathogen dynamics? If pathogens manipulate host behaviour to their benefit (Poulin, 2018), or hosts respond to pathogens, such as by reducing social contacts when infected (Lopes, Block, & Konig, 2016), then host–parasite interactions could impact social structure dynamically. Black ants Lasius niger , for example, if challenged with a pathogenic fungus, individual‐level changes in the patterns of social contacts increase transmission‐inhibiting structural properties at the colony level (Adelman, Moyers, Farine, & Hawley, 2015).…”

“…Specifically, can pathogens change the dynamics of social interactions within a group by selecting for social connections based on specific health traits of potential associates, thus leading to a clustered structure driven by the host-pathogen dynamics? If pathogens manipulate host behaviour to their benefit(Poulin, 2018),Farine, & Hawley, 2015). However, individuals are not homogeneous; they can also vary in their infectiousness, in their contact rates, and in their infectious period(VanderWaal, Ezenwa, & Hawley, 2016).…”

Are British urban foxes (Vulpes vulpes) “bold”? The importance of understanding human–wildlife interactions in urban areas

“…We were unable to investigate all the factors that might influence a fox's personality, and future work should consider the effects of an animal's health on human–urban fox interactions (Koski, 2014). Disease, particularly the effects of novel parasites such as Toxoplasma gondii , can induce risk‐taking and other behaviors that influence an animal's social interactions with conspecifics, other species, and people (Johnson et al., 2018; Poulin, 2018).…”

“…Disease, particularly the effects of novel parasites such as Toxoplasma gondii, can induce risk-taking and other behaviors that influence an animal's social interactions with conspecifics, other species, and people (Johnson et al, 2018;Poulin, 2018).…”

Bidirectional interactions between host social behaviour and parasites arise through ecological and evolutionary processes

“…Some socially transmitted viruses, including rabies, can increase aggression and thereby physical contact, but whether this constitutes adaptive manipulation remains under review due to the variable manifestation of symptoms (Lefevre et al, 2009;Poulin, 2010). In fact, across parasites, it is far more common that parasitism leads to reduced activity and social isolation (Poulin, 2019). An exception are the microsporidia and cestode parasites of brine shrimp (Artemia franciscana and A. parthenogenetica): these parasites increase swarming of brine shrimp near the water surface, which may increase trophic transmission of the cestode to its avian host and direct transmission of microsporidia to nearby…”