Social status, immune response and parasitism in males: a meta-analysis

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.

The sociality–health–fitness nexus: synthesis, conclusions and future directions

“…Habig & Archie [7] did provide a stronger and very interesting finding: in a second meta-analysis, dominant males exhibited higher levels of parasitism with protozoan blood parasites, gastrointestinal helminths and ectoparasites. Given their other results that demonstrate similar immune responses between subordinates and dominants, this suggests that other factors are influencing the difference in parasitism.…”

“…While we might expect that animals living in a group will experience some increased exposure to infectious disease [18,21], the same is not true of social stress, where heterogeneity in responses might be more marked (e.g. in relation to dominance rank, see [7], with possibilities for both positive and negative effects). The reasons for this difference in exposure and social stress effects are related to reasons given above: we only expect negative health consequences from chronic social stress in gregarious settings in which individuals have distinct social relationships [16].…”

“…This is to some extent a disappointment; it indicates that different studies are finding different patterns, yet we currently lack an understanding of the variability in the results. The authors [7] note that many other factors, such as mating system, may be needed to understand the links between social status and immunity. In addition, they note that many of the studies in the meta-analysis were conducted on captive animals, thus calling for more research on wild animal populations.…”

“…Other links involve effects of sociality on buffering the stressors of social life, including the intense competition that is observed in some species [5], with resulting effects on susceptibility to infectious and non-infectious diseases when these support networks are unavailable. Some papers in this theme issue provide examples of the mechanisms that underlie predicted interactions, such as the effects of dominance rank, sex and stress on hormone production [6], their effects on immune function and parasitism [7], and the role of the sympathetic nervous system in mediating effects of social instability on immune function [5]. Other papers in this issue have investigated the fitness consequences of sociality and parasitism, for example in Columbian ground squirrels [8].…”

“…Other papers in this issue have investigated the fitness consequences of sociality and parasitism, for example in Columbian ground squirrels [8]. The papers also take a wide range of approaches, including broad-scale comparative and meta-analysis [3,7,9], long-term field research on food availability, stress and population density [10], social networks and disease spread in wild animals [4], and experimental studies of behaviour in captive primates [5].…”