Fitness costs of infection are fundamental to understanding the ecology and evolution of host–parasite interactions. However, these costs, and particularly their underlying mechanisms, are challenging to evaluate in wild populations.
Here, we quantified total and species‐specific costs of gastrointestinal worms on African buffalo, by combining the power of an anthelmintic treatment experiment that perturbed the entire worm community with a longitudinal study that tracked the two most dominant community members.
Reducing all worms improved buffalo body condition, which was strongly associated with increases in survival and reproduction. Species‐specific analyses revealed that condition‐mediated fitness costs of infection differed between parasite species. Hosts that gained the blood‐sucking worm Haemonchus, lost condition, and this loss may have been mediated by reductions in forage intake. Hosts that resisted Haemonchus by elevating IL‐4 and eosinophil immune defences were able to reduce their parasite loads and gain back condition.
Conversely, hosts that gained Cooperia, a less pathogenic worm, gained condition and had higher survival and reproductive success. Elevating immune defences had no effect on Cooperia abundance. Coupled with the positive relationship observed between Cooperia and host condition, our data suggest that hosts might benefit from tolerating Cooperia rather than incurring the costs of resistance.
Overall, our study reveals that differential host responses to parasites play a key role in mediating the costs of infection.
A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.12951/suppinfo is available for this article.
The ubiquity and importance of parasite co-infections in populations of free-living animals is beginning to be recognized, but few studies have demonstrated differential fitness effects of single infection versus co-infection in free-living populations. We investigated interactions between the emerging bacterial disease bovine tuberculosis (BTB) and the previously existing viral disease Rift Valley fever (RVF) in a competent reservoir host, African buffalo, combining data from a natural outbreak of RVF in captive buffalo at a buffalo breeding facility in 2008 with data collected from a neighbouring free-living herd of African buffalo in Kruger National Park. RVF infection was twice as likely in individual BTBþ buffalo as in BTB2 buffalo, which, according to a mathematical model, may increase RVF outbreak size at the population level. In addition, co-infection was associated with a far higher rate of fetal abortion than other infection states. Immune interactions between BTB and RVF may underlie both of these interactions, since animals with BTB had decreased innate immunity and increased pro-inflammatory immune responses. This study is one of the first to demonstrate how the consequences of emerging infections extend beyond direct effects on host health, potentially altering the dynamics and fitness effects of infectious diseases that had previously existed in the ecosystem on free-ranging wildlife populations.
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