Trends in Parasitology
Volume 28, Issue 11, November 2012, Pages 466-470
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Opinion
Breaking barriers: a leap ahead in Plasmodium biology
Do malaria parasites manipulate mosquitoes?

https://doi.org/10.1016/j.pt.2012.08.004Get rights and content

Malaria parasites have been suggested to alter the behavior of mosquito vectors to increase the likelihood of transmission. Some empirical evidence supports this hypothesis, yet the role of manipulation is ignored in most epidemiological models, and behavioral differences between infected and uninfected females are not considered in the development or implementation of control measures. We suggest that this disconnect exists because the link between behavioral alteration and actual transmission in the field has yet to be demonstrated or quantified fully. We review and discuss the current evidence for manipulation, explore its potential significance for malaria transmission, and suggest ways to move this hypothesis forward from theory to potential application in malaria control.

Section snippets

Manipulation by parasites

Transmission is a key determinant of parasite fitness. There are numerous examples of parasites altering the behavior of their host to increase the probability of transmission [1]. For example, ants infected with particular species of fungi ascend leaves at the appropriate moment before death to position themselves for prime dispersal of fungal spores [2]. Crab parasites castrate their crustacean hosts and manipulate them into caring for the parasite as they would their own offspring [3].

Malaria and mosquitoes

It is not difficult to imagine that natural selection might favor a malaria parasite that could stimulate its own transmission. According to the manipulation hypothesis, malaria parasites decrease mosquito blood-feeding and other risky behaviors during the pre-infectious phase, thereby decreasing the risk of host death during parasite development (oocyst stage). Parasites then increase vector feeding rate once they have become infectious (sporozoite stage) (reviewed in [5]).

There is evidence

Implications for transmission

The reproductive rate of the malaria parasite (which provides a measure of transmission intensity) is captured in the Ross–MacDonald framework, R0 = ma2bcpn/−rln(p) [20]. In this equation, ‘m’ is the ratio of vectors to humans, ‘a’ the mosquito biting frequency, ‘b’ the efficiency at which the parasite passes from mosquito to human, ‘c’ the efficiency with which the parasite passes from human to mosquito, ‘p’ the daily survival of the vector, ‘n’ the extrinsic incubation period of the parasite,

Research priorities to resolve the issues

Various lines of research would enable better characterization of the putative manipulation phenotype, a crucial step in assessing its effect on transmission (Box 1). Not least, the current evidence for manipulation needs to be greatly improved before we can understand the impact of parasite-induced behavior change on disease epidemiology.

Concluding remarks

Several studies suggest that malaria parasites manipulate mosquito behavior to facilitate transmission, but the nature and extent of the phenomenon remains unclear. Without transmission data, it is formally possible that these behavioral alterations could be side-effects of infection that do not increase transmission. Changes in mosquito behavior following parasite invasion could be a pathological consequence of infection, or a manifestation of the mosquito immune response to infection, or an

Acknowledgments

This work was supported by a National Institutes of Health (NIH)–National Institute of Allergy and Infectious Diseases (NIAID) International Centers of Excellence for Malaria Research (ICEMR) award (#U19AI089676).

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