Abstract
BackgroundBiological rhythms allow organisms to compartmentalise and coordinate behaviours, physiologies, and cellular processes with the predictable daily rhythms of their environment. There is increasing recognition that the biological rhythms of mosquitoes that vector parasites are important for global health. For example, whether perturbations in blood foraging rhythms as a consequence of vector control measures can undermine disease control. To address this, we explore the impacts of altered timing of blood-feeding on mosquito life history traits and malaria transmission.MethodsWe present three experiments in which Anopheles stephensi mosquitoes were fed in the morning or evening on blood that had different qualities, including: (i) chemical-induced or (ii) Plasmodium chabaudi infection-induced anaemia; (iii) Plasmodium berghei infection but no anaemia; or (iv) stemming from hosts at different times of day. We then compared whether time-of-day variation in blood meal characteristics influences mosquito fitness proxies relating to survival and reproduction, and malaria transmission proxies.ResultsMosquito lifespan is not influenced by the time-of-day they received a blood meal, but several reproductive metrics are affected, depending on other blood characteristics. Overall, our data suggest that receiving a blood meal in the morning makes mosquitoes more likely to lay eggs, lay slightly sooner and have a larger clutch size. In keeping with previous work, P. berghei infection reduces mosquito lifespan and the likelihood of laying eggs, but time-of-day of blood-feeding does not impact upon these metrics nor on transmission of this parasite.ConclusionThe time-of-day of blood-feeding does not appear to have major consequences for mosquito fitness or transmission of asynchronous malaria species. If our results from a laboratory colony of mosquitoes living in benign conditions hold for wild mosquitoes, it suggests that mosquitoes have sufficient flexibility in their physiology to cope with changes in biting time induced by evading insecticide-treated bed nets. Future work should consider the impact of multiple feeding cycles and the abiotic stresses imposed by the need to forage for blood during times of day when hosts are not protected by bed nets.
Highlights
Biological rhythms allow organisms to compartmentalise and coordinate behaviours, physiologies, and cellular processes with the predictable daily rhythms of their environment
We carried out three experiments to determine how the timing of receiving a blood meal affects aspects of mosquito survival and fecundity, and whether qualities of host blood or malaria infection modulate the effects of the time-of-day that mosquitoes feed
Reproduction: time to lay For mosquitoes that laid, those that were infected laid two days sooner than uninfected individuals and at any time point, were ~ 70% more likely to lay (mean ± SE days taken to lay since egg bowls were provided: uninfected = 6.88 ± 0.48, infected = 5.05 ± 0.35; infected:uninfected Hazard Ratio (HR) = 1.71 (± 0.171, z = 3.12, P = 0.002; Fig. 8a)
Summary
Biological rhythms allow organisms to compartmentalise and coordinate behaviours, physiologies, and cellular processes with the predictable daily rhythms of their environment. Whether they are clock-controlled or direct responses to rhythmic environmental cues, shape, and are shaped by interactions between organisms is poorly understood. We address this by examining the consequences of daily rhythms in the interactions between vectors, their hosts, and their parasites. Given reports that some mosquito populations have altered the time-of-day they bite (likely in response to the use of insecticide-treated bed nets) [6,7,8,9,10,11,12,13], exploring the consequences of perturbed blood foraging rhythms for mosquito fitness and malaria transmission is urgently required
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