An animal's social behaviour both influences and changes in response to its parasites. Here we consider these bidirectional links between host social behaviours and parasite infection, both those that occur from ecological vs evolutionary processes. First, we review how social behaviours of individuals and groups influence ecological patterns of parasite transmission. We then discuss how parasite infection, in turn, can alter host social interactions by changing the behaviour of both infected and uninfected individuals. Together, these ecological feedbacks between social behaviour and parasite infection can result in important epidemiological consequences. Next, we consider the ways in which host social behaviours evolve in response to parasites, highlighting constraints that arise from the need for hosts to maintain benefits of sociality while minimizing fitness costs of parasites. Finally, we consider how host social behaviours shape the population genetic structure of parasites and the evolution of key parasite traits, such as virulence. Overall, these bidirectional relationships between host social behaviours and parasites are an important yet often underappreciated component of population-level disease dynamics and host–parasite coevolution.

Hosts strongly influence parasite fitness. However, it is challenging to disentangle host effects on genetic vs plasticity-driven traits of parasites, since parasites can evolve quickly. It remains especially difficult to determine the causes and magnitude of parasite plasticity. In successive generations, parasites may respond plastically to better infect their current type of host, or hosts may produce generally ‘good’ or ‘bad’ quality parasites. Here, we characterized parasite plasticity by taking advantage of a system in which the parasite (the yeast Metschnikowia bicuspidata, which infects Daphnia) has no detectable heritable variation, preventing rapid evolution. In experimental infection assays, we found an effect of rearing host genotype on parasite infectivity, where host genotypes produced overall high or low quality parasite spores. Additionally, these plastically induced differences were gained or lost in just a single host generation. Together, these results demonstrate phenotypic plasticity in infectivity driven by the within-host rearing environment. Such plasticity is rarely investigated in parasites, but could shape epidemiologically important traits.

Many hermaphroditic parasites reproduce by both cross-fertilization and self-fertilization. To understand the maintenance of such mixed mating systems it is necessary to compare the fitness consequences of the two reproductive modes. This has, however, almost never been done in the context of host–parasite coevolution. Here we show the consequences of outcrossing and selfing in an advanced life-stage of the cestode Schistocephalus solidus, i.e. in its second intermediate host, the three-spined stickleback (Gasterosteus aculeatus). Each juvenile stickleback was simultaneously exposed to 2 experimentally infected copepods, one harbouring outcrossed the other selfed parasites. At 60 days p.i. parasites were removed from the fish's body cavity and, with microsatellite markers, assigned to either outcrossed or selfed origin. Prevalence was not significantly higher in outcrossed parasites. However, those fish that were infected contained significantly more outcrossed than selfed parasites. Thus the probability of a selfed parasite to progress in the life-cycle is reduced in the second intermediate host. Furthermore, we found that even the multiply infected fish increased in weight during the experiment. Nevertheless, total worm weight in multiply infected fish was significantly lower than in singly infected ones, which thus might be a parasite life-history strategy.

Parasites should be better at infecting hosts from sympatric populations than allopatric populations most of the time (parasite local adaptation). In a previous study of a population of snail parasites (Microphallus sp.) from Lake Alexandrina, New Zealand, we found that Microphallus was more infective to snails (Potamopyrgus antipodarum) in shallow water but not in deep water. Here, we repeated the original study and also monitored the development of the parasite. We found that parasites from shallow water were more infective to hosts from shallow water and developed more rapidly in these hosts. In contrast, parasites from deep water were not more infective to hosts from deep water and did not develop more rapidly in them. These results suggest clinal variation in the susceptibility of these snails, with shallow-water snails more susceptible than deep-water snails. We offer 2 possible explanations for these results. First, gene flow in the Microphallus population is primarily from shallow to deep water, leading to an asymmetric pattern of local adaptation. Alternatively, snails from shallow water may be more susceptible for reasons independent of gene flow, perhaps due to differences in host condition between habitats.