Social immunity and the evolution of group living in insects

Abstract

One contribution of 14 to a theme issue 'The sociality-health -fitness nexus in animal societies'. The evolution of group living requires that individuals limit the inherent risks of parasite infection. To this end, group living insects have developed a unique capability of mounting collective anti-parasite defences, such as allogrooming and corpse removal from the nest. Over the last 20 years, this phenomenon (called social immunity) was mostly studied in eusocial insects, with results emphasizing its importance in derived social systems. However, the role of social immunity in the early evolution of group living remains unclear. Here, I investigate this topic by first presenting the definitions of social immunity and discussing their applications across social systems. I then provide an up-to-date appraisal of the collective and individual mechanisms of social immunity described in eusocial insects and show that they have counterparts in non-eusocial species and even solitary species. Finally, I review evidence demonstrating that the increased risks of parasite infection in group living species may both decrease and increase the level of personal immunity, and discuss how the expression of social immunity could drive these opposite effects. By highlighting similarities and differences of social immunity across social systems, this review emphasizes the potential importance of this phenomenon in the early evolution of the multiple forms of group living in insects.

Implications of the behavioural immune system for social behaviour and human health in the modern world

“…There exist many behavioural strategies of anti-parasite defence, observed across a wide range of species ( [1][2][3][4][5][6]; see also Meunier [7]). These strategies include specific behavioural tendencies that are stimulated by existing infections and that help to promote recovery from those infections (e.g.…”

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

“…Interesting new angles on this question were raised in this theme issue, including social immunity in insects [9] and the behavioural immune system in humans [12]. Yet other questions arise.…”

“…In that first chapter, the authors highlighted how transitions from a solitary lifestyle to group living resulted in new health-related costs and risks, and thus favoured the evolution of new counterstrategies to these costs that involve behaviour, physiology and immune responses. This evolutionary pattern is well illustrated by Meunier's [9] analysis of social immunity and group living in insects, where social immunity refers to collective anti-parasitic defences, such as systematic removal of dead animals from the nest. His review of the macroevolutionary patterns highlights the many diverse solutions that natural selection has discovered to control infection after group living evolves.…”

“…In group-living species, it is thought that many behavioural strategies to reduce parasite transmission have evolved [3,9,35]. The basic principles underlying these 'social immunity' strategies serve as the basis for hypotheses linking parasitism to cross-species variation in the structure of social groups [3,19,36].…”

“…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].…”