Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence

Abstract

Interactions involving several parasite species (multi-parasitized hosts) or several host species (multi-host parasites) are the rule in nature. Only a few studies have investigated these realistic, but complex, situations from an evolutionary perspective. Consequently, their impact on the evolution of parasite virulence and transmission remains poorly understood. The mechanisms by which multiple infections may influence virulence and transmission include the dynamics of intrahost competition, mediation by the host immune system and an increase in parasite genetic recombination. Theoretical investigations have yet to be conducted to determine which of these mechanisms are likely to be key factors in the evolution of virulence and transmission. In contrast, the relationship between multi-host parasites and parasite virulence and transmission has seen some theoretical investigation. The key factors in these models are the trade-off between virulence across different host species, variation in host species quality and patterns of transmission. The empirical studies on multi-host parasites suggest that interspecies transmission plays a central role in the evolution of virulence, but as yet no complete picture of the phenomena involved is available. Ultimately, determining how complex host-parasite interactions impact the evolution of host-parasite relationships will require the development of cross-disciplinary studies linking the ecology of quantitative networks with the evolution of virulence.

Figure 1.

Increasing levels of complexity in the study of host–parasite associations. (a,b) Traditional investigations focus on species–species interactions; (c,d) an increasing number of studies have begun to investigate species–assemblage relationships, but (e) the full complexity (i.e. assemblage–assemblage relationships) is currently unstudied. P and H are parasites or hosts, respectively. This is a fictive illustration of three butterfly species interacting with nematodes, microsporidia and fungi. The different shadings denote different genotypes. For simplicity, the different genotypes of the different host and parasite species are not noted in (c), (d) and (e).