Analogies in the evolution of individual and social immunity

Abstract

We compare anti-parasite defences at the level of multicellular organisms and insect societies, and find that selection by parasites at these two organisational levels is often very similar and has created a number of parallel evolutionary solutions in the host's immune response. The defence mechanisms of both individuals and insect colonies start with border defences to prevent parasite intake and are followed by soma defences that prevent the establishment and spread of the parasite between the body's cells or the social insect workers. Lastly, germ line defences are employed to inhibit infection of the reproductive tissue of organisms or the reproductive individuals in colonies. We further find sophisticated self/non-self-recognition systems operating at both levels, which appear to be vital in maintaining the integrity of the body or colony as a reproductive entity. We then expand on the regulation of immune responses and end with a contemplation of how evolution may shape the different immune components, both within and between levels. The aim of this review is to highlight common evolutionary principles acting in disease defence at the level of both individual organisms and societies, thereby linking the fields of physiological and ecological immunology.

Figure 1

Immune modules. The collective defence (pale grey, dotted line) of a group comprises all individual defences (medium grey, dashed line) of the group members and their interaction (arrows). Individual defences are composed of anti-parasite behaviours (B, dark grey ellipse) and physiological immune systems that can contain either only the innate (I) immune component (e.g. invertebrates) or also the acquired (A) immune component (e.g. vertebrates). The single immune modules interact with each other during anti-parasite defence and thus shape each other's evolution.

Figure 2

(a) Steps of infection and anti-parasite defence of individual organisms and (b) insect societies. (1) Border defence: parasites (black ovals) are prevented from entering the body or colony by avoidance behaviour and consolidated physiological defences in the epithelia or at nest entrances. (2) Soma defence: immune defence acts to prevent infection of somatic tissue (cells in the body and sterile workers in insect colonies). (3) Germ line and offspring defence: the reproductive tissue (ovaries) of organisms and the reproductive individuals (queens) of insect colonies are subject to specific immune privileges to prevent offspring infection.