Host-pathogen interactions on the move: migratory waterfowl and avian influenza viruses

Abstract

Pathogens may impose substantial costs on their hosts, yet, simultaneously, pathogen populations are influenced by the condition and behaviour of these hosts. Migratory hosts and their pathogens are particularly fascinating as migrants connect disparate habitats; are exposed to a greater diversity of pathogens; and, concomitantly, must perform long-distance movement. Focusing on Arctic-breeding waterfowl and low-pathogenic avian influenza virus (AIV) I investigated: the role of host migration in the temporal and spatial dynamics of the pathogen; the potential for these non-lethal viruses to affect host behaviour and fitness; and the ramifications of such behavioural modifications for viral dynamics. Physiological and behavioural observations from free-living populations, paired with long-term surveillance and epidemiological models were used to address these questions. Across species, AIV infection risk was related to species’ life history and environmental conditions, particularly the use of aquatic habitats, and geographic location. Also at the level of individual hosts the risk of acquiring AIV infection was higher for individuals foraging in aquatic habitats. Once infected, susceptibility to AIV differed between individuals on the basis of their age. Moreover, long-distance migrants were found to maintain a detectable immune response over many months, in contrast to previous expectations. I also found that individuals that were naturally infected with AIV had reduced fitness compared to their non-infected counterparts, in terms of reduced survival and impaired reproductive success. However, these effects were not seen in individuals experimentally inoculated with AIV in a unique experiment in free-living birds, suggesting that naturally-occurring infection with AIV may be accompanied by other infections that together have a greater impact on host fitness than each pathogen in isolation. Epidemiological models suggest that the behavioural differences seen in naturally-infected individuals are sufficient to modify the timing and location of epidemics. Together, the findings from this project underscore the importance of host ecology to pathogen dynamics, and the potential for pathogens to shape ecological trade-offs facing the host.