Timing malaria transmission with mosquito fluctuations

Abstract

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”, which states 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. We detect a periodic increase of parasitemia 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.

Adaptive periodicity in the infectivity of malaria gametocytes to mosquitoes

“…We reveal that: (i) gametocytes are less numerous in the host's blood at night but night time gametocytes are more likely to develop to oocysts; (ii) the greater infectivity of night time gametocytes does not increase the probability that mosquitoes become infected or result in more intense infection at the oocyst stage; (iii) independently of parasite time of day, mosquitoes fed at night are less likely to be infected with oocysts; and (iv) the greater infectivity of night time gametocytes does not alter the probability of mosquitoes harbouring sporozoites but does increase sporozoite burden in mosquitoes fed in their daytime. Our findings are broadly consistent with a recent study on the avian malaria Plasmodium relictum [ 16 ], which also reveals that transmission (to oocyst stage) is more efficient in the late afternoon and night (when vectors are active) than at noon or early morning. However, in this study, enhanced transmission is associated with elevated parasite density in the avian host's blood in the late afternoon.…”

Adaptive plasticity in the gametocyte conversion rate of malaria parasites

“…mosquito biting rate, host immunity, mosquito susceptibility) are equal [61]. Although time-of-day may affect transmission efficacy [81,82], host, parasite and mosquito time-of-day have been controlled for in our experiment thus allowing for comparison of transmission probability between groups. The proportional change in transmission probability resulting from changing vs. not changing conversion, is estimated as transmission probabilities of drug treated groups relative to that of the untreated groups.…”

“…From [61], and assuming all else equal with respect to other factors that could influence transmission (e.g. vector biting rates, host immunity, vector susceptibility, time-of-day of transmissions [61,81,82]), the probability of transmission for a given gametocyte density, G(t) is given by exp ½À 12:69 þ 3:6 log 10 GðtÞ� 1 þ exp½À 12:69 þ 3:6 log 10 GðtÞ� ð4Þ…”

The evolutionary ecology of circadian rhythms in infection

“…Given that rhythms of parasites and mosquitoes each affect malaria transmission in lab experiments 54,55 , what are the likely epidemiological consequences? Recent work suggests that mosquitoes are more susceptible to infection when they feed in the daytime and parasites are more infectious at night 54 .…”