Limited impact of within-vector ecology on the evolution of malaria parasite transmission investment

Abstract

Malaria parasites spend part of their life in a vertebrate host and the rest in an arthropod vector and must successfully navigate both environments to gain fitness. In vertebrate hosts, malaria parasites infect red blood cells and can either replicate asexually or develop into the sexual form required for transmission to the vector. Despite the clear fitness benefits of onward transmission, only a small proportion of malaria parasites convert to sexual development. Mathematical models seeking to test the plausibility of various hypotheses to explain these low “conversion rates” have focused almost exclusively on the vertebrate/host half of the parasite life cycle. Here, we examined how processes occurring in the vector, including density-dependent parasite development and parasite-induced vector mortality, influence the evolution of parasite conversion rate in the host by developing a multi-scale model of within-host infection dynamics and parasite within-vector developmental processes for rodent malaria. We found that, regardless of model specifications (e.g., definitions of fitness, magnitude of parasite-induced vector mortality), considering processes within the vector had only a weak influence on the optimal conversion rate, but substantially diminished the fitness returns for all strategies and resulted in a sharper declines off the optima. Our approach allowed us to derive new metrics of parasite fitness (which we call “infectivity functions”) that link within-host gametocyte density to the probability of transmission to new hosts after passing through the vector, and that prevent overestimation of parasite transmission potential.