One hand washes the other: cooperation and conflict in hygiene and immunity

Abstract

In humans and wild animals, pathogens impose costs on both the individual and the social group as a whole. To minimise these costs, group-living species have evolved many hygienic and immune traits that benefit from cooperation between individuals, thereby subjecting them to the laws of social evolution. Such social contracts include reciprocal grooming, altruistic self-isolation, spiteful treatment of infected individuals, and costly immune resistance responses. In highly social animals such as eusocial insects, these traits often present as complex “collective” or “social” immune systems. Even the expression of individual-level phenotypes such as sickness behaviours and immunological tolerance can depend heavily on social context, and understanding whether such responses present a benefit for the individual, the group, or both can be critical for understanding their functions and eco-evolutionary consequences. As yet, our consideration of these traits has mostly concerned individuals, or collective immunity in eusocial insect taxa. Consequently, their broader epidemiological consequences and implications for the evolution of sociality are relatively unclear. Here, I describe a wide number of socially evolved hygienic and immune traits in wild animals, both in social insects and in other taxa. I outline the problems that emerge when evolving and enforcing these anti-disease functions, discussing the conflicts that arise and their implications for evolutionary and cultural transitions in social complexity, and their potential analogues in human public health.

Behavioural defences against parasites across host social structures

“…helping behaviours, Stockmaier et al, 2021). Cooperative behaviours include individuals providing food (Loehle, 1995) or territory defence (Almberg et al, 2015) to support sick group members, all of which contribute to maintaining the fitness of parasitized individuals, with potential feedback benefits for the individual providing help if sick individuals reciprocate after they recover (Albery, 2022). Currently, these helping behaviours in stable groups are understudied, potentially because the physiological benefits and the clear link of helping behaviours to parasite tolerance are often challenging to quantify (Figure 1).…”

“…For less cooperative groups, behaviours likely evolved due to their direct benefits at the individual level but may still have some group‐level effects (i.e., increase fitness of other group members). For instance, even if individuals avoid or resist infection for selfish reasons, this might also reduce the likelihood of transmission to conspecifics (Albery, 2022). Ultimately, we hope to widen the diversity of study systems considered for the study of behavioural anti‐parasite responses, in a framework for understanding how axes of sociality should influence the expression and evolution of behavioural parasite avoidance, resistance and tolerance.…”

“…For less cooperative groups, behaviours likely evolved due to their direct benefits at the individual level but may still have some group-level effects (i.e., increase fitness of other group members). For instance, even if individuals avoid or resist infection for selfish reasons, this might also reduce the likelihood of transmission to conspecifics (Albery, 2022).…”