Host behaviour–parasite feedback: an essential link between animal behaviour and disease ecology

Abstract

Animal behaviour and the ecology and evolution of parasites are inextricably linked. For this reason, animal behaviourists and disease ecologists have been interested in the intersection of their respective fields for decades. Despite this interest, most research at the behaviour-disease interface focuses either on how host behaviour affects parasites or how parasites affect behaviour, with little overlap between the two. Yet, the majority of interactions between hosts and parasites are probably reciprocal, such that host behaviour feeds back on parasites and vice versa. Explicitly considering these feedbacks is essential for understanding the complex connections between animal behaviour and parasite ecology and evolution. To illustrate this point, we discuss how host behaviour-parasite feedbacks might operate and explore the consequences of feedback for studies of animal behaviour and parasites. For example, ignoring the feedback of host social structure on parasite dynamics can limit the accuracy of predictions about parasite spread. Likewise, considering feedback in studies of parasites and animal personalities may provide unique insight about the maintenance of variation in personality types. Finally, applying the feedback concept to links between host behaviour and beneficial, rather than pathogenic, microbes may shed new light on transitions between mutualism and parasitism. More generally, accounting for host behaviour-parasite feedbacks can help identify critical gaps in our understanding of how key host behaviours and parasite traits evolve and are maintained.

Dynamic, spatial models of parasite transmission in wildlife: Their structure, applications and remaining challenges

“…Waning immunity from maternal antibodies or prior exposure to an infectious agent may also contribute to temporal lags in the availability of susceptible individuals on different host patches depending on the local history of exposure (Fouchet et al., ; Garnier, Gandon, Harding, & Boulinier, ; Garnier et al., ; Plowright et al., ). Importantly, behavioural and physiological processes may be linked through host–parasite feedbacks (Ezenwa et al., ; Gudelj & White, ; VanderWaal & Ezenwa, ). An important next step for spatial, individual‐based models might be to incorporate feedbacks between behaviour and physiology, such as sickness‐induced behavioural changes or variable transmission efficiency between populations (Croft et al., ; Ezenwa et al., ; Quevillon, Hanks, Bansal, Hughes, & Gordon, ; Wilson et al., ).…”

“…Importantly, behavioural and physiological processes may be linked through host–parasite feedbacks (Ezenwa et al., ; Gudelj & White, ; VanderWaal & Ezenwa, ). An important next step for spatial, individual‐based models might be to incorporate feedbacks between behaviour and physiology, such as sickness‐induced behavioural changes or variable transmission efficiency between populations (Croft et al., ; Ezenwa et al., ; Quevillon, Hanks, Bansal, Hughes, & Gordon, ; Wilson et al., ). Advances in the field of ecoimmunology are making the data needed for such analyses ever more accessible (Adelman, Moyers, & Hawley, ).…”

The application of statistical network models in disease research

“…It may also be important to consider networks as dynamic, rather than static, structures, with changes affecting transmission over longer time‐scales, particularly in endemic diseases (Funk, Salathé & Jansen ; Ezenwa et al . ; Silk et al . ).…”

Can the behaviour of threespine stickleback parasitized with Schistocephalus solidus be replicated by manipulating host physiology?

“…Changes in behaviour following experimental infections have been shown in many animals (Ezenwa et al, 2016;Barber et al, 2000) and might reflect 'sickness behaviours' including lethargy, depression and a reduction in maintenance behaviours, such as grooming (Hart, 1988). During its pre-infective early growth phase within its fish host, S. solidus presence does not induce a host leucocyte immune response (Scharsack et al, 2004) and is associated with decreased monocyte proliferation (Scharsack et al, 2007).…”