Abstract
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.
Highlights
Social hierarchies are a fundamental feature of many human and non-human animal societies [1]
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
Subordinate males exhibited relatively greater baseline levels of IFN-g (d 1⁄4 0.610, p 1⁄4 0.042; n 1⁄4 4; figure 3c) and higher IL-6 and TNF-a responses to immune stimulants than dominant males (IL-6: d 1⁄4 0.387; p 1⁄4 0.025, n 1⁄4 13; figure 3d; TNF-a: d 1⁄4 0.476; p 1⁄4 0.007; n 1⁄4 7; figure 3e). These results indicate that subordinate males may exhibit dysregulated inflammatory responses relative to dominant males, and probably should not be taken as evidence for stronger immune function in subordinate than dominant males
Summary
Social hierarchies are a fundamental feature of many human and non-human animal societies [1]. Organisms are not expected to experience broad immunosuppression in the face of energetic or hormonal challenges; rather they should reallocate their investment in different types of immune defence depending on their energetic and disease-related costs [31,54,57,58] To date, two such hypotheses have been proposed that make specific predictions about how males should allocate investment in immune defence as a function of reproductive effort or stress. For studies that included multiple time points for a given test of immune hypothesis: immune defences are shaped by patterns of chronic and acute stress higher social status lower social status rstb.royalsocietypublishing.org Phil. To test the links between social status and individual disease risk, we conducted a meta-analysis of the relationships between dominance rank and measures of parasitism (electronic supplementary material, tables S3 and S6). We assessed publication bias visually via funnel plot analyses and quantitatively using Egger’s tests [81]
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