War and peace: social interactions in infections

Abstract

One of the most striking facts about parasites and microbial pathogens that has emerged in the fields of social evolution and disease ecology in the past few decades is that these simple organisms have complex social lives, indulging in a variety of cooperative, communicative and coordinated behaviours. These organisms have provided elegant experimental tests of the importance of relatedness, kin discrimination, cooperation and competition, in driving the evolution of social strategies. Here, we briefly review the social behaviours of parasites and microbial pathogens, including their contributions to virulence, and outline how inclusive fitness theory has helped to explain their evolution. We then take a mechanistically inspired 'bottom-up' approach, discussing how key aspects of the ways in which parasites and pathogens exploit hosts, namely public goods, mobile elements, phenotypic plasticity, spatial structure and multi-species interactions, contribute to the emergent properties of virulence and transmission. We argue that unravelling the complexities of within-host ecology is interesting in its own right, and also needs to be better incorporated into theoretical evolution studies if social behaviours are to be understood and used to control the spread and severity of infectious diseases.

Keywords: ecology; inclusive fitness; plasticity; relatedness; transmission; virulence.

Figure 1.

Examples of kin discrimination by: (a) direct recognition, e.g. cells of the slime mould Dictyostelium determine whether they are interacting with kin or non-relatives during slug and spore formation based on the sequence similarity of their surface adhesion proteins [66,67] (photo credit Owen Gilbert); (b) indirect cues based on familiarity with individuals, e.g. long-tailed tits learn the vocalization patterns of kin during the natal rearing period [68] (photo credit Sarah Reece) or (c) ‘armpits’ which are a mixture of direct and indirect cues, e.g. ground squirrels use olfactory cues which have a genetic component and are also learnt by self-referencing during development [69] (photo credit Alan Vernon). The malaria parasite, Plasmodium chabaudi (d), adjusts investment into male and female transmission stages according to how many other conspecific clones share the host, suggesting kin discrimination occurs [21] (photo credit Sarah Reece and Sinclair Stammers). The mechanism is unknown but indirect cues seems unlikely; an obvious candidate would be that parasites can infer the presence of other clones via the host immune response, but sex ratio adjustment is observed in infections before the required strain-specific responses develop.

Figure 2.

Theoretical relationships between virulence and relatedness under conditions of: (a) individual exploitation (virulence maximized at low relatedness) (b) collective exploitation (virulence maximized at high relatedness) (c) spiteful interactions, e.g. when harming competitors trades off against replication that causes virulence. (summarized by [16]).

Figure 3.

Phenotypic plasticity and reaction norms. In panel (a), phenotype does not vary with the environment and both genotypes have identical reaction norms. In panel (b) both genotypes are plastic and (c) there is also genetic variation. Panel (d) illustrates a genotype-by-environment interaction (G × E), where both genotypes are plastic but their phenotypic reaction norms vary. Genetic variation and G × E can complicate how much genetic variation is exposed to selection; in panel (e) the genotypes produce the same phenotype in environment (E) 1 but not in environment 2, so selection can only differentiate between the genotypes in environment 2.