Differential host responses to parasitism shape divergent fitness costs of infection

Abstract

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.

Context‐dependent costs and benefits of tuberculosis resistance traits in a wild mammalian host

“…We observed clear costs of infection resistance in the form of reduced condition and marginally reduced survival once infected in animals that converted to bTB positive later in life. In addition to our survival observations, poor body condition has been previously shown in this system to be a strong predictor of mortality (Budischak, O'Neal, Jolles, & Ezenwa, ; Gorsich, Ezenwa, Cross, Bengis, & Jolles, ). Therefore, the infection resistance phenotype appears to be advantageous only in terms of preventing or delaying bTB infection, but carries a survival cost if bTB does occur.…”

“…In contrast, we observed no fitness costs associated with higher levels of proliferation resistance, suggesting that this resistance phenotype associates with potentially higher energy stores and higher reproductive fitness in this population. This finding implies that at the onset of bTB, animals with higher initial fitness and condition suffer less pathology or can more effectively mitigate damage than animals in poor condition, which may lead to overall higher survival rates in this group, since condition is highly predictive of survival in buffalo (Budischak et al, ; Gorsich et al, ). It has been demonstrated across taxa that organisms in better condition have higher available resources to allocate to immune coping mechanisms or tolerate resource leaching by the pathogens themselves, especially in environments where resources are seasonally limited (Martin, Weil, & Nelson, ).…”

The contrasting hidden consequences of parasitism: Effects of a hematophagous nematode (Uncinaria sp.) in the development of a marine mammal swimming behavior

“…Therefore, it is possible that Uncinaria sp. induces “trade‐offs” in otariids between growth and the immune function, because the animals have to allocate more energy resources to clear the infection instead of growth (Budischak, O'Neal, Jolles, & Ezenwa, ). However, despite this decrease in growth rate, hookworm‐infected animals did not have a significantly different SMI compared to noninfected pups.…”

On the relationship between body condition and parasite infection in wildlife: a review and meta‐analysis

“…Hosts in good condition might better tolerate high pathogen loads, where tolerance is defined as the host's ability to maintain fitness in the presence of infection (Roy & Kirchner 2000). For example African buffalo infected by a mildly harmful intestinal worm showed no fitness costs of infection when hosts were otherwise in good condition (Budischak et al 2018). If hosts in poor condition suffer high mortality in the presence of infection, and hosts in good condition can better tolerate higher parasite loads, this could produce a positive infectioncondition relationship at the population level, despite negative effects of parasites on individuals.…”