Do malaria parasites manipulate mosquitoes?

Abstract

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 fully demonstrated or quantified. 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.

Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

“…It is likely that the existing literature contains both false negative and false positive reports, and unbiased screenings of a broad number of parasite species are very difficult, due to the broad diversity of possible manipulation effects that would have to be considered. Negative reports are rare (but see, for example; Cator et al, 2012Cator et al, , 2013Cator et al, , 2015Soh et al, 2013;Berret and Voordouw, 2015;Vantaux et al, 2015) and many cases of manipulating parasites might as yet remain undiscovered, either because they lead to inconspicuous or no alterations in the phenotype of the host, or because certain classes of parasites are seldom studied for host manipulation. By contrast, false positive reports can arise because alternative explanations for the observed phenotypic alterations are usually not excluded.…”

“…As a possible explanation, he suggested publication bias, that is, an initial euphoria concerning the intensity of manipulation effects became replaced by more realistic estimates over time (Poulin, 2000). More recently, other authors have stressed that alternative explanations need to be considered-and excluded-to provide conclusive empirical support for an assumed case of manipulation (Klein, 2005;Thomas et al, 2005;James, 2010;Cator et al, 2012Cator et al, , 2015Lafferty and Kuris, 2012;Worth et al, 2013). Alternatively, such alterations can: (1) represent mere side-effects of the pathology that is associated with infection; (2) form part of the successful immune response of the host to parasitization; or (3) represent traits that were inherited from ancestors but represent maladaptations in the present host-parasite combination (Klein, 2005;Thomas et al, 2005).…”

Climate, environmental and socio-economic change: weighing up the balance in vector-borne disease transmission

“…Combining data for these two species to estimate vital rates would not necessarily generate realistic inference. Furthermore, data and research are particularly needed to better understand the influence of environmental factors on key parameters such as the EIP [89], vector competence [94,113], biting behaviour and interactions with infection [118,119], because these have been very under-researched to date.…”

Microorganism-mediated behaviour of malaria mosquitoes

“…To optimize Plasmodium transmission, malaria-infected mosquito vectors carrying transmissible stages (sporozoites) should preferentially bite non-infected hosts, while infected hosts carrying transmissible stages (gametocytes) should be more attractive to healthy vectors than hosts without transmissible stages. Various studies in non-human systems indeed demonstrated altered mosquito feeding behaviour such as probing, persistence and engorgement rate upon Plasmodium infection (Hurd, 2003), suggesting manipulation of mosquito vectors by Plasmodium (Cator et al, 2012). Anopheles gambiae mosquitoes infected with sporozoites also showed increased attraction to the odour of healthy humans compared to non-infected mosquitoes .…”

“…Other examples of manipulation are seen in Trypanosome-infected tsetse flies, which probe more frequently on vertebrate hosts than their non-infected counterparts (Roberts, 1981), thus increasing parasite transmission. Manipulation of mosquitoes by Plasmodium parasites, through direct effects in the mosquito, has been reviewed in detail (Koella et al, 1998;Lefèvre & Thomas, 2008;Cator et al, 2012) and will be briefly introduced below.…”