Abstract
BackgroundMalaria-infected mosquitoes have been reported to be more likely to take a blood meal when parasites are infectious than when non-infectious. This change in feeding behavior increases the likelihood of malaria transmission, and has been considered an example of parasite manipulation of host behavior. However, immune challenge with heat-killed Escherichia coli induces the same behavior, suggesting that altered feeding behavior may be driven by adaptive responses of hosts to cope with an immune response, rather than by parasite-specific factors. Here we tested the alternative hypothesis that down-regulated feeding behavior prior to infectiousness is a mosquito adaptation that increases fitness during infection.MethodsWe measured the impact of immune challenge and blood feeding on the fitness of individual mosquitoes. After an initial blood meal, Anopheles stephensi Liston mosquitoes were experimentally challenged with heat-killed E. coli at a dose known to mimic the same temporal changes in mosquito feeding behavior as active malaria infection. We then tracked daily egg production and survivorship of females maintained on blood-feeding regimes that either mimicked down-regulated feeding behaviors observed during early malaria infection, or were fed on a four-day feeding cycle typically associated with uninfected mosquitoes.ResultsRestricting access to blood meals enhanced mosquito survival but lowered lifetime reproduction. Immune-challenge did not impact either fitness component. Combining fecundity and survival to estimate the population-scale intrinsic rate of increase (r), we found that, contrary to the mosquito adaptation hypothesis, mosquito fitness decreased if blood feeding was delayed following an immune challenge.ConclusionsOur data provide no support for the idea that malaria-induced suppression of blood feeding is an adaptation by mosquitoes to reduce the impact of immune challenge. Alternatively, the behavioral alterations may be neither host nor parasite adaptations, but rather a consequence of constraints imposed on feeding by activation of the mosquito immune response, i.e. non-adaptive illness-induced anorexia. Future work incorporating field conditions and different immune challenges could further clarify the effect of altered feeding on mosquito and parasite fitness.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-016-1392-x) contains supplementary material, which is available to authorized users.
Highlights
Malaria-infected mosquitoes have been reported to be more likely to take a blood meal when parasites are infectious than when non-infectious
We propose that the altered feeding behavior of anophelines during malaria infection is another example of adaptive illnessinduced anorexia, and explains the same phenomenon previously attributed to parasite-manipulation [6]
When survivorship was compared at day 12 after the immune challenge, the time period corresponding to the extrinsic incubation period for P. falciparum at 27 °C [44,45,46,47], we found that restricting blood meals increased the probability that mosquitoes would survive long enough to transmit the parasite (Wald χ2 = 32.29, df = 5, p < 0.05), while immune-challenge had no effect on survival over this time period (p > 0.05) (Fig. 2)
Summary
Malaria-infected mosquitoes have been reported to be more likely to take a blood meal when parasites are infectious than when non-infectious This change in feeding behavior increases the likelihood of malaria transmission, and has been considered an example of parasite manipulation of host behavior. A behavior with high risk of mosquito mortality, has been reported to be suppressed during the non-infectious stage of parasite development and enhanced during the infectious stage [7]. These behavioral changes likely increase the probability of onward transmission and parasite fitness [8, 9], leading to the assumption that altered mosquito behavior is a classic case of parasite manipulation [6]. If the altered behaviors are adaptive, we expect that mosquitoes feeding on these altered regimes should have increased fitness following an immune-challenge compared to those that continue to feed normally
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