Timing malaria transmission with mosquito fluctuations

Temporal variations in the activity of arthropod vectors can dramatically affect the epidemiology and evolution of vector-borne pathogens. Here we explore the \"Hawking hypothesis\" stating that these pathogens may evolve the ability to time investment in transmission to match the activity of their vectors. First, we use a theoretical model to identify the conditions promoting the evolution of time-varying transmission strategies in pathogens. Second, we experimentally test the \"Hawking hypothesis\" by monitoring the within-host dynamics of Plasmodium relictum throughout the acute and the chronic phases of the bird infection. To explore the periodicity in the host parasite density, we develop a new methodology to correct for non-stationarities in the host parasitaemia. We detect a periodic increase of parasitaemia and mosquito infection in the late afternoon that coincides with an increase in the biting activity of its natural vector. We also detect a positive effect of mosquito bites on Plasmodium replication in the birds both in the acute and in the chronic phases of the infection. This study highlights that Plasmodium parasites use two different strategies to increase the match between transmission potential and vector availability. We discuss the adaptive nature of these unconditional and plastic transmission strategies with respect to the time-scale and the predictability of the fluctuations in the activity of the vector.\n\nImpact SummarySeasonal and daily fluctuations in the environment affect the abundance and the activity of vectors and may therefore have profound consequences on the transmission of infectious diseases. Here we show that, in accord with evolutionary theory, malaria parasites have evolved two different and complementary strategies to cope with fluctuations in mosquito availability. First, Plasmodium relictum adopts an unconditional strategy whereby within-host parasitaemia and mosquito infection increases in the afternoon and in the evening, when its vector, the Culex pipiens mosquito, is most active. Second, we find evidence for a plastic strategy allowing the parasitaemia to rapidly increase after exposure to mosquito bites.