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

Abstract

AbstractEvolutionary 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’s 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.Significance statementIn evolutionary medicine, we commonly refer to the severity or outcome of a parasitic infection as the parasite’s virulence. The evolution of virulence is shaped by the properties of both the host and parasite, such as the strength of the host’s immune response or the production of toxins by the parasite. A fundamental property of the parasite is the time at which it is transmitted from one host to the next. Here, using the mosquitoAnopheles gambiaeand the microsporidian parasiteVavraia culicis, we demonstrate that time to transmission directly affects the evolution of virulence and, therefore, the infection outcome in the new host. Our study highlights the importance of time to transmission in epidemiological models and decision-making in vector control strategies.