Natural selection on a measure of parasite resistance varies across ages and environmental conditions in a wild mammal

Abstract

Parasites detrimentally affect host fitness, leading to expectations of positive selection on host parasite resistance. However, as immunity is costly, host fitness may be maximized at low, but nonzero, parasite infection intensities. These hypotheses are rarely tested on natural variation in free‐living populations. We investigated selection on a measure of host parasite resistance in a naturally regulated Soay sheep population using a longitudinal data set and found negative correlations between parasite infection intensity and annual fitness in lambs, male yearlings and adult females. However, having accounted for confounding effects of body weight, the effect was only significant in lambs. Associations between fitness and parasite resistance were environment‐dependent, being strong during low‐mortality winters, but negligible during harsher high‐mortality winters. There was no evidence for stabilizing selection. Our findings reveal processes that may shape variation in parasite resistance in natural populations and illustrate the importance of accounting for correlated traits in selection analysis.

Immune Profile Predicts Survival and Reflects Senescence in a Small, Long-Lived Mammal, the Greater Sac-Winged Bat (Saccopteryx bilineata)

“…Indeed, Soay sheep infected by nematodes may face high mortality risks during harsh winters [65], which may even lead to population crashes [66]. Furthermore, longitudinal studies on the same population found age-related changes in parasite resistance [67], [68]. These findings potentially indicate that endoparasite infections may involve higher costs in Soay sheep than in S. bilineata , especially when resources are limited.…”

Fecal antibody levels as a noninvasive method for measuring immunity to gastrointestinal nematodes in ecological studies

“…FEC has also been shown to be negatively related to body mass at the time of sampling and to subsequent survival, especially in young animals (Hayward et al. 2011). …”

“…2011, 2014). Teladorsagia circumcincta is a highly prevalent GIN parasite of the Soay sheep (Craig et al.…”

IL-17 and neutrophils: unexpected players in the type 2 immune response

“…Metazoan parasites are therefore likely to have been a central evolutionary force in the shaping of type 2 immune pathways. In a telling example from the unmanaged population of Soay sheep on St Kilda, parasitic nematodes especially in combination with malnutrition and severe weather, are the major determinants of failure to survive [8,12,13,14 ]. Thus, regulating energy metabolism and body temperature may be crucial to reproductive success in the face of helminth infection, providing a possible explanation for the association of type 2 immunity with these seemingly unrelated processes.…”

“…However, studying helminth infections will be a major route to enlightenment. From plants to fish, and from domesticated mammals to wild mammal populations, helminth burden is directly and negatively correlated with host fitness [8][9][10][11]. Metazoan parasites are therefore likely to have been a central evolutionary force in the shaping of type 2 immune pathways.…”