“Evolution and manipulation of vector host choice”

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Sylvain Gandon (July 2018)

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A new theoretical framework to study the epidemiology, the evolution and the manipulation of vector host choice behavior

In vector-borne diseases (e.g. avian malaria), both the insect vector (Culex mosquito) and the pathogen (avian Plasmodium) may have some ability to control the preference between an infected and an uninfected hosts (a bird). The optimal strategy depends on the actor (the mosquito vector or the malaria pathogen) but also the state of the actor (the mosquito may be infected or not, the pathogen may be in the mosquito or in the bird). This can yield multiple evolutionary conflicts over the control of the behavior of the vector.
(Credit: Sylvain Gandon, CC0)

Imagine you are a female mosquito. You are the vector of a pathogen that infects a vertebrate host you feed upon. You have the choice between feeding on an uninfected host or on a host infected by this pathogen. Which host should you pick for your next blood meal? Now, imagine that you are the pathogen. You have the potential to modify the preference of the female mosquito by modifying the scent of the infected host, but also, more directly, by modifying the decision of mosquitoes once they become infected. What should you do?

Answering these questions and understanding the evolution host preference is key for the epidemiology of vector-borne diseases. A growing number of experimental studies are revealing the diversity of behavioral preference of vector species from a broad range of pathosystems. In this paper, Sylvain Gandon develops a theoretical framework to study the evolution and the manipulation of vector behavior. This analysis shows that many factors are acting on the evolution of these traits: the fitness costs of the infection, the prevalence of the infection in the different hosts, whether or not the female mosquito is already infected, whether the pathogen manipulating the mosquito is currently infecting the mosquito or the vertebrate host. The model yields multiple evolutionary outcomes and explains the diversity of host choice behaviors observed in different vector-borne diseases. In particular, this analysis helps understand why several pathogens have evolved manipulation strategies that vary with the infectious status of their vector species, while other pathogens seem unable to evolve such complex conditional strategies.


Abstract

The transmission of many animal and plant diseases relies on the behavior of arthropod vectors. In particular, the specific preference for infected or uninfected hosts observed in many vector species is expected to affect the circulation of vector-borne diseases. Here I develop a theoretical framework to study the epidemiology and the evolution of the manipulation of host choice behavior of vectors. I show that vector preference strategies have dramatic epidemiological consequences. I also explore the evolution of vector host choice under different scenarios regarding the control of the vector behavior by the pathogen. This analysis yields multiple evolutionary outcomes and explains the diversity of host choice behaviors observed in a broad range of vector-borne diseases. In particular, this analysis helps understand why several pathogens have evolved manipulation strategies that vary with the infectious status of their vector species while other pathogens seem unable to evolve such complex conditional strategies. I argue that contrasting the behavior of infected and uninfected vectors is key to reveal mechanistic constraints acting on the evolution of the manipulation of vector behavior.