Sexual dimorphism in immunity across animals: a meta‐analysis

Abstract

In animals, sex differences in immunity are proposed to shape variation in infection prevalence and intensity among individuals in a population, with females typically expected to exhibit superior immunity due to life‐history trade‐offs. We performed a systematic meta‐analysis to investigate the magnitude and direction of sex differences in immunity and to identify factors that shape sex‐biased immunocompetence. In addition to considering taxonomic and methodological effects as moderators, we assessed age‐related effects, which are predicted to occur if sex differences in immunity are due to sex‐specific resource allocation trade‐offs with reproduction. In a meta‐analysis of 584 effects from 124 studies, we found that females exhibit a significantly stronger immune response than do males, but the effect size is relatively small, and became non‐significant after controlling for phylogeny. Female‐biased immunity was more pronounced in adult than immature animals. More recently published studies did not report significantly smaller effect sizes. Among taxonomic and methodological subsets of the data, some of the largest effect sizes were in insects, further supporting previous suggestions that testosterone is not the only potential driver of sex differences in immunity. Our findings challenge the notion of pervasive biases towards female‐biased immunity and the role of testosterone in driving these differences.

Dehydration enhances cellular and humoral immunity in a mesic snake community

“…The ability of an organism to mount a normal response to an antigen (i.e., immunocompetence) has been shown to fluctuate with environmental conditions and throughout ontogeny (Bakar et al, 2016; Love, Salvante, Dale, & Williams, 2008; Nelson & Demas, 1996; Sandland & Minchella, 2003). For example, empirical evidence suggests that season, sex, and hydration can all lead to inter‐ and intra‐individual variation in immunocompetence (Brusch, Christian, Brown, Shine, & DeNardo, 2019; Kelly, Stoehr, Nunn, Smyth, & Prokop, 2018; Walton, Weil, & Nelson, 2011; Zhang, Jin, Qu, & Caviedes‐Vidal, 2017). Despite previous research detailing the internal and external conditions which influence the immune system, there remain substantial gaps in our understanding of the biotic and abiotic factors that influence different components of the immune system in ecologically relevant contexts, including in free‐ranging animals (Viney, Riley, & Buchanan, 2005).…”

“…In addition to reproductive seasonality, the sex of an individual influences variation in key features of life history and physiology across animal taxa (Zuk, 2009). Recent work highlights the role of sex in immunological variation (reviewed in Klein and Flanagan, 2016; Foo, Nakagawa, Rhodes, & Simmons, 2017; Kelly et al, 2018). A meta‐analysis of 124 studies across vertebrates and invertebrates indicates that females tend to have higher measures of immunocompetence compared to males (Kelly et al, 2018).…”

“…Recent work highlights the role of sex in immunological variation (reviewed in Klein and Flanagan, 2016; Foo, Nakagawa, Rhodes, & Simmons, 2017; Kelly et al, 2018). A meta‐analysis of 124 studies across vertebrates and invertebrates indicates that females tend to have higher measures of immunocompetence compared to males (Kelly et al, 2018). However, the significance of this sex effect is highly sensitive to phylogeny, and this study exposes the taxonomical gaps in our understanding of sex‐specific variation in immune function.…”

Mating enhances immune function of Drosophila melanogaster populations against bacterial pathogens

“…Theory suggests that males will spend more resources in mating at the expense of immunity, making them more vulnerable to infections (Zuk and Stoehr, 2002). Meta-analysis on sex difference in invertebrate immunity, however, found no sexual dimorphism (Kelly et al, 2018; Letitia et al, 2000). While differences in post mating immunity between sexes has been observed in some cases, any trend generalising a sex biased immunocompetence remains elusive (Kelly et al, 2018; McKean and Nunney, 2005).…”

“…Meta-analysis on sex difference in invertebrate immunity, however, found no sexual dimorphism (Kelly et al, 2018; Letitia et al, 2000). While differences in post mating immunity between sexes has been observed in some cases, any trend generalising a sex biased immunocompetence remains elusive (Kelly et al, 2018; McKean and Nunney, 2005). In this study, we also test whether mated D. melanogaster females differ from mated males in their post mating immune function.…”