Evolutionary consequences of vector-borne transmission: how using vectors shapes host, vector and pathogen evolution

Abstract

Transmission mode is a key factor that influences host–parasite coevolution. Vector-borne pathogens are among the most important disease agents for humans and wildlife due to their broad distribution, high diversity, prevalence and lethality. They comprise some of the most important and widespread human pathogens, such as yellow fever, leishmania and malaria. Vector-borne parasites (in this review, those transmitted by blood-feeding Diptera) follow unique transmission routes towards their vertebrate hosts. Consequently, each part of this tri-partite (i.e. parasite, vector and host) interaction can influence co- and counter-evolutionary pressures among antagonists. This mode of transmission may favour the evolution of greater virulence to the vertebrate host; however, pathogen–vector interactions can also have a broad spectrum of fitness costs to the insect vector. To complete their life cycle, vector-borne pathogens must overcome immune responses from 2 unrelated organisms, since they can activate responses in both vertebrate and invertebrate hosts, possibly creating a trade-off between investments against both types of immunity. Here, we assess how dipteran vector-borne transmission shapes the evolution of hosts, vectors and the pathogens themselves. Hosts, vectors and pathogens co-evolve together in a constant antagonistic arms race with each participant's primary goal being to maximize its performance and fitness.

Keywords: Coevolution; evolution; parasite–host interaction; vector ecology; vector-borne diseases; virulence.

Graphical abstract

Fig. 1.

Illustration of the main selective pressures acting on hosts (A), vectors (B) and parasites (C), and examples of research questions that still lack answers (D). Figure created with BioRender.com.

Fig. 2.

Vector-borne pathogens and their vertebrate hosts and dipteran vectors transmitted in human-modified habitat. (1) Leishmania spp. infects humans via sandfly bites in (a) zoonotic cycles (using domestic dogs as the main reservoirs) and in (b) anthroponotic cycles (i.e. human-to-human transmission). (2) Dengue virus infects mostly humans and is vectored by the mosquito Aedes aegypti. (3) Human malaria parasites are transmitted among humans by Anopheles mosquitoes in residential and agricultural areas. (4) West Nile virus circulates among birds and is vectored by Culex mosquitoes and infects humans mainly in residential and in agricultural areas. (5) Spillover of pathogen from domestic to wildlife animals, here illustrated by the spillover of Plasmodium juxtanucleare from domestic chickens to wild birds (Ferreira-Junior et al., 2018). (6) Avian haemosporidian prevalence has been positively and/or negatively associated with anthropization depending on the parasite genera (e.g. Plasmodium or Haemoproteus), the type of anthropic impact (e.g. farming, urbanization, pollution, etc.) and the geographic region of the study (e.g. Neotropics, Europe, etc.). Urbanization and landscape modifications driven by human activities can have several environmental effects, such as increases in (A) temperature and (B) environmental pollution. Figure created with BioRender.com.