Mosquito–malaria interactions: a reappraisal of the concepts of susceptibility and refractoriness

Sinden, Robert E.; Alavi, Yasmene; Raine, J. Dale

doi:10.1016/j.ibmb.2004.03.015

Cited by 59 publications

(47 citation statements)

References 27 publications

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“…Even in susceptible mosquitoes, many parasites are killed, and thus some degree of resistance occurs (Al-Olayan et al 2002;Sinden et al 2004), probably as a result of the upregulation of genes involved in defense (Dimopoulos 2003;Levashina 2004). The mechanisms linking infection, immune effort, and reproductive effort have yet to be elucidated, but it is likely that this is where trade-offs will lie.…”

Section: Discussionmentioning

confidence: 99%

Evaluating the Costs of Mosquito Resistance to Malaria Parasites

Hurd

Taylor

Adams

et al. 2005

Evol

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Costly resistance mechanisms have been cited as an explanation for the widespread occurrence of parasitic infections, yet few studies have examined these costs in detail. A malaria-mosquito model has been used to test this concept by making a comparison of the fitness of highly susceptible lines of mosquitoes with lines that are resistant to infection. Malaria infection is known to cause a decrease in fecundity and fertility of mosquitoes; resistant mosquitoes were thus predicted to be fitter than susceptible ones. Anopheles gambiae were selected for refractoriness/resistance or for increased susceptibility to infection by Plasmodium yoelii nigeriensis. Additional lines that acted as controls for inbreeding depression were raised in parallel but not exposed to selection pressure. Selections were made in triplicate so that founder effects could be detected. Resistance mechanisms that were selected included melanotic encapsulation of parasites within 24 h postinfection and the complete disappearance of parasites from the gut. Costs of immune surveillance were assessed after an uninfected feed, and costs of immune deployment were assessed after exposure to infection and to infection and additional stresses. Mosquito survivorship was unaffected by either resistance to infection or by an increased burden of infection when compared with low levels of infection. In most cases reproductive fitness was equally affected by refractoriness or by infection. Resistant mosquitoes did not gain a fitness advantage by eliminating the parasites. Costs were consistently associated with larval production and egg hatch rate but rarely attributed to changes in blood feeding and never to changes in mosquito size. No advantages appeared to be gained by the offspring of resistant mosquitoes. Furthermore, we were unable to select for refractoriness in groups of mosquitoes in which 100% or 50% of the population were exposed to infection every generation for 22 generations. Under these selection pressures, no population had become completely refractory and only one became more resistant. Variations in fitness relative to control lines in different groups were attributed to founder effects. Our conclusion from these findings is that refractoriness to malaria is as costly as tolerance of infection. KeywordsAnopheles gambiae; fitness costs; innate immunity; malaria; mosquito; Plasmodium; refractoriness Despite their detrimental effects on the host, parasitic infections are extremely common (Esch and Fernandez 1993). This observation has led evolutionary ecologists to evoke life-history theories to explain why host traits for parasite resistance are not always selected. Immune defense is deemed to be costly, and thus supposed trade-offs exist with other fitness 2 E-mail: h.hurd@keele.ac.uk 3 E-mail: p.j.taylor@keele.ac.uk 4 E-mail: bia13@keele.ac.uk 5 E-mail: bia50@keele.ac.uk 6 E-mail: p.eggleston@keele.ac.uk UKPMC Funders Group Author Manuscript UKPMC Funders Group Author Manuscript UKPMC Funders Group Author Manuscriptcomponents. Th...

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Section: Discussionmentioning

confidence: 99%

Evaluating the Costs of Mosquito Resistance to Malaria Parasites

Hurd

Taylor

Adams

et al. 2005

Evol

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“…Sporogonic development during the oocyst stage may be critical for successful sporogony. There are data about encapsulation and melanization of oocysts in midguts of mosquitoes infected both with Plasmodium and Haemoproteus parasites (Collins et al, 1986;Schwartz and Koella, 2002;Dimopoulos, 2003;Sinden et al, 2004;Valkiūnas et al, 2013;Palinauskas et al, 2015). This defence mechanism is often recorded because it can be readily visualised in midgut preparations.…”

Section: Active Transmission Of Differentmentioning

confidence: 99%

Description, molecular characterisation, diagnostics and life cycle of Plasmodium elongatum (lineage pERIRUB01), the virulent avian malaria parasite

Palinauskas

Žiegytė

Iezhova

et al. 2016

International Journal for Parasitology

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“…High gametocyte production in response to sulphadoxine-pyrimethamine suggests that gametocyte production can respond to some cues within the host, and is not a fixed trait (Barnes and White, 2005). Incompatibility between parasite strains and various species and strains of Anopheles is now believed to reflect an interplay between polymorphic innate immune response genes of the mosquito that promote or retard parasite killing (melanization) and unknown melanization resistance genes of the parasite (Vlachou and Kafatos, 2005), hence current discussions often invoke evolutionary costs (Lambrechts et al, 2005;Sinden et al, 2004). Simultaneous propagation of multiple strains of malaria by a single mosquito has been confirmed by molecular genetic studies (Babiker et al, 1994;Huber et al, 1998;Ranford-Cartwright et al, 1993), but the high frequency of recombination during the sexual phase of the parasite life-cycle (confirming that 'male gametocytes of one strain' can indeed 'fertilize the females of a different strain') may mean that outcrossing, between strains, is as common as 'selfing' and thus, as predicted by Shute and Maryon (1954), that strains rapidly lose their identity in endemic areas.…”

Section: Infectivitymentioning

confidence: 99%

Chapter 1 Strain Theory of Malaria

McKenzie

Smith

O’Meara

et al. 2008

Advances in Parasitology Volume 66

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From the 1920s to the 1970s, a large body of principles and evidence accumulated about the existence and character of 'strains' among the Plasmodium species responsible for human malaria. An extensive research literature examined the degree to which strains were autonomous, stable biological entities, distinguishable by clinical, epidemiological or other features, and how this knowledge could be used to benefit medical and public health practice. Strain theory in this era was based largely on parasite phenotypes related to clinical virulence, reactions to anti-malarial drugs, infectivity to mosquitoes, antigenic properties and host immunity, latency and relapse. Here we review the search for a definition of 'strain', suggest how the data and discussion shaped current understandings of many aspects of malaria and sketch a number of specific connections with perspectives from the past 30 years.

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Mosquito–malaria interactions: a reappraisal of the concepts of susceptibility and refractoriness

Cited by 59 publications

References 27 publications

Evaluating the Costs of Mosquito Resistance to Malaria Parasites

Evaluating the Costs of Mosquito Resistance to Malaria Parasites

Description, molecular characterisation, diagnostics and life cycle of Plasmodium elongatum (lineage pERIRUB01), the virulent avian malaria parasite

Chapter 1 Strain Theory of Malaria

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