Costs and drivers of helminth parasite infection in wild female baboons

Abstract

Helminth parasites can have wide-ranging, detrimental effects on host reproduction and survival. These effects are best documented in humans and domestic animals, while only a few studies in wild mammals have identified both the forces that drive helminth infection risk and their costs to individual fitness. Working in a well-studied population of wild baboons (Papio cynocephalus) in the Amboseli ecosystem in Kenya, we pursued two goals, to (a) examine the costs of helminth infections in terms of female fertility and glucocorticoid hormone levels and (b) test how processes operating at multiple scales-from individual hosts to social groups and the population at large-work together to predict variation in female infection risk. To accomplish these goals, we measured helminth parasite burdens in 745 faecal samples collected over 5 years from 122 female baboons. We combine these data with detailed observations of host environments, social behaviours, hormone levels and interbirth intervals (IBIs). We found that helminths are costly to female fertility: females infected with more diverse parasite communities (i.e., higher parasite richness) exhibited longer IBIs than females infected by fewer parasite taxa. We also found that females exhibiting high Trichuris trichiura egg counts also had high glucocorticoid levels. Female infection risk was best predicted by factors at the host, social group and population level: females facing the highest risk were old, socially isolated, living in dry conditions and infected with other helminths. Our results provide an unusually holistic understanding of the factors that contribute to inter-individual differences in parasite infection, and they contribute to just a handful of studies linking helminths to host fitness in wild mammals.

Keywords: Trichuris trichiura; baboons; female fertility; fitness costs; glucocorticoid hormones; helminth infection; primates.

Fig 1.

Processes proposed to drive inter-host variation in helminth infection risk in female savannah baboons. These processes operate at the level of the host population, host social groups, and individual hosts, as indicated by the concentric circles. See main text and Table S1 for key citations regarding these processes.

Fig. 2.

Plot showing the relationship between log-transformed Trichuris trichiura egg counts and log-transformed fecal glucocorticoid concentrations.

Figure 3.

Association between log T. trichiura egg counts and (A) presence/absence of strongyle infection; (B) female social connectedness to adult males; (C) age in years; (D) group size; (E) rainfall in the previous 3 months (cm); (F) average maximum temperature in the previous 3 months.