Complex interactions in the life cycle of a simple parasite shape the evolution of virulence

Abstract

Evolutionary expectations about the virulence of parasites (i.e., the parasite-induced mortality rate of the host) generally describe parasites which grow and are transmitted at the same time. Many parasites, however, go through an incubation period, that is they must grow before they can be transmitted. Moreover, the parasite incubation period and virulence are linked through its growth rate. We here suggest that such interactions make it difficult to predict how virulence will evolve. We illustrate our ideas with a parasite with a simple cycle, the microsporidianVavraia culicis, which infects the mosquitoAnopheles gambiae. We selected the parasite for six generations to kill their host and be transmitted early or late. Selecting for late transmission led to a stronger increasing its exploitation (i.e., cost due to growth), but not pathogenicity per parasite (i.e., cost independent of growth), than selection for early transmission. This was associated with higher virulence, and a shorter parasite life cycle, with the latter having a larger and more rapid production of the infective spores. In response, the host shortened its life cycle and shifted to early fecundity when infected with late-selected spores. Altogether, the results of this study reinforce the need for a reviewed and unified virulence theory and raise important questions for epidemiological and vector control strategies.

Dissecting transmission to understand parasite evolution

“…Note that bp' depends on the susceptibility of the new host 9 , which can be on factors such as life history 74,75 , the immune strategy employed 40,41 , the host's genotype 9,76,77 , and its overall fitness. It can also depend on the quality of the parasites, which depends on the previous two stages and is thus affected by, for example, the first host's nutrition, genotype and immune response 5,[78][79][80] and the interhost environment 81,82 . Finally, it can depend (non-linearly) on the number of parasites in the interhost stage.…”

“…The ongoing controversy between virulence and transmission is an expected result of the simplification of the components of infection. Recent work on decomposing 39,87 and extensively studying the components of infection 34,88 , and their relationship to each other 79,89,90 , is crucial and is marking a new era in infection biology. We believe the points mentioned and the framework designed here, will considerably push the field forward and help to better understand infection, namely the evolution of virulence.…”