Social interaction, and not group size, predicts parasite burden in mammals

Abstract

Although parasitism is often considered a cost of sociality, the evidence is mixed, possibly because sociality is multivariate. Here we contrast the dependence of parasitism costs on major social variables such as group size and social structure, as measured by network metrics. We conduct two robust phylogenetic meta-analyses, comprising 43 published results for studies with group size and 32 results with social structure metrics. This is the first meta-analytical test of this hypothesis for mammals as a whole. Contrarily to theoretical expectations and previous meta-analyses, there is no relationship between group size and parasitism, but we find conflicting results when analysing different aspects of sociality. Our analysis reveals that social structure is connected to parasite load, possibly because contact between group members, and not group size, is linked to parasite transmission. While more intensely interconnected groups facilitate parasite transmission, large groups are frequently fragmented into smaller, weakly connected subgroups. Strong social modularisation should thus be favoured by natural selection to hamper parasite overload. Future empirical studies should focus on specific parameters of social network structure and on parasite transmissibility. If social structure can evolve fast, even culturally, then host/parasites evolutionary games enter into a whole new fast dynamics, and animal conservation studies should take advantage of this possibility.

Linking parasitism to network centrality and the impact of sampling bias in its interpretation

“…By whatever mechanism, our results support those of review studies and meta-analyses showing that, across many different sociality measures and parasites with different life histories and modes of transmission, the relationship between sociality and parasitism is generally positive (Altizer et al, 2003;Rushmore et al, 2017;Briard and Ezenwa, 2021;Lucatelli et al, 2021).…”

“…It therefore seems important to consider what these various centrality measures represent in terms of host socio-biology and in terms of social or ecological processes. Exposure and transmission risk of fast and directly spread parasites such as lice or certain viruses and bacteria might depend simply on the number of associations individuals have (degree), whereas slower-spreading/developing parasites or those requiring additional developmental stages in the environment may be more dependent on the actual time hosts spend in contact or in spatial proximity with one another (strength), or the overall degree of social integration they have (eigenvector centrality) (Silk et al, 2017; Briard and Ezenwa, 2021; Lucatelli et al, 2021). By whatever mechanism, our results support those of review studies and meta-analyses showing that, across many different sociality measures and parasites with different life histories and modes of transmission, the relationship between sociality and parasitism is generally positive (Altizer et al, 2003; Rushmore et al, 2017; Briard and Ezenwa, 2021; Lucatelli et al, 2021).…”

“…It therefore seems important to consider what these various centrality measures represent in terms of host socio-biology and in terms of social or ecological processes. Exposure and transmission risk of fast and directly spread parasites such as lice or certain viruses and bacteria might depend simply on the number of associations individuals have (degree), whereas slower-spreading/developing parasites or those requiring additional developmental stages in the environment may be more dependent on the actual time hosts spend in contact or in spatial proximity with one another (strength), or the overall degree of social integration they have (eigenvector centrality) (Silk et al, 2017;Briard and Ezenwa, 2021;Lucatelli et al, 2021).…”

Density dependence and disease dynamics: moving towards a predictive framework

“…Ultimately, if density drives greater social connectedness, the findings of these studies may be indicative of density dependent transmission; in fact, in species whose inhabited area grows in step with population size, social connectedness may be a more informative measure of transmission than density (Elliot & Hart 2010). While most earlier analyses mention density, at least to some extent (Cote & Poulin 1995;Rifkin et al 2012;Patterson & Ruckstuhl 2013;Nunn et al 2015b), the more recent social network structure meta-analyses do not (Lucatelli et al 2020;Briard & Ezenwa 2021). This may imply that social drivers of disease are increasingly being distinguished from density dependence.…”

“…Earlier examples either compared across multiple species and correlated their social structures with parasitism (Ezenwa 2004;, simulated (Nunn et al 2015b), or meta-analysed within-species estimates of group size effects (Cote & Poulin 1995;Rifkin et al 2012;Patterson & Ruckstuhl 2013). More recently, with the growing popularity of network analysis in disease ecology (Craft 2015;White et al 2017;Albery et al 2021a), meta-analyses have targeted social network studies to examine how individual-level sociality drives infection across a range of different systems (Lucatelli et al 2020;Briard & Ezenwa 2021).…”