In male vertebrates, two conflicting paradigms—the energetic costs of high dominance rank and the chronic stress of low rank—have been proposed to explain patterns of immune function and parasitism. To date, neither paradigm has provided a complete explanation for status-related differences in male health. Here, we applied meta-analyses to test for correlations between male social status, immune responses and parasitism. We used an ecoimmunological framework, which proposes that males should re-allocate investment in different immune components depending on the costs of dominance or subordination. Spanning 297 analyses, from 77 studies on several vertebrate taxa, we found that most immune responses were similar between subordinate and dominant males, and neither dominant nor subordinate males consistently invested in predictable immune components. However, subordinate males displayed significantly lower delayed-type hypersensitivity and higher levels of some inflammatory cytokines than dominant males, while dominant males exhibited relatively lower immunoglobulin responses than subordinate males. Despite few differences in immunity, dominant males exhibited consistently higher parasitism than subordinate males, including protozoan blood parasites, ectoparasites and gastrointestinal helminths. We discuss our results in the context of the costs of dominance and subordination and advocate future work that measures both parasitism and immune responses in wild systems.
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.
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