Abstract
Previous studies have shown that the central American mosquito vector, Anopheles albimanus, is generally refractory to oocyst infection with allopatric isolates of the human malaria parasite Plasmodium falciparum. However, the reasons for the refractoriness of A. albimanus to infection with such isolates of P. falciparum are unknown. In the current study, we investigated the infectivity of the P. falciparum clone 3D7A to laboratory-reared A. albimanus and another natural vector of human malaria, Anopheles stephensi. Plasmodium falciparum gametocytes grown in vitro were simultaneously fed to both mosquito species and the progress of malaria infection compared. In 22 independent paired experimental feeds, no mature oocysts were observed on the midguts of A. albimanus 10days after bloodfeeding. In contrast, high levels of oocyst infection were found on the midguts of simultaneously fed A. stephensi. Direct immunofluorescence microscopy and light microscopical examination of Giemsa-stained histological sections were used to identify when the P. falciparum clone 3D7A failed to establish mature oocyst infections in A. albimanus. Similar densities of macrogametes/zygotes, and immature retort-form and mature ookinetes were found within the bloodmeals of both mosquito species. However, in A. albimanus, ookinetes were seldom associated with the peritrophic matrix, and were neither observed in the ectoperitrophic space nor the midgut epithelium. In contrast, ookinetes were frequently observed in these midgut compartments in A. stephensi. Additionally, young oocysts were observed on the midguts of A. stephensi but not A. albimanus 2days after bloodfeeding. Vital staining of the immature retort-form and mature ookinetes found within the luminal bloodmeal, demonstrated that a significantly greater proportion of these malaria parasite stages were non-viable in A. albimanus compared with A. stephensi. Overall, our observations indicate that ookinetes of the P. falciparum clone 3D7A are destroyed within the bloodmeal of A. albimanus and that the midgut lumen, rather than the midgut epithelium, is the site of mosquito refractoriness in this particular malaria parasite-mosquito vector combination.
Highlights
Anopheles albimanus is an important vector of human malaria throughout central America (Pan American Health Organization, 1996)
512 of the 645 (79.1%) A. stephensi midguts examined at day 10 pbf were infected with at least one oocyst, demonstrating the infectivity of the gametocytes fed to A. albimanus
The central American mosquito vector A. albimanus is generally refractory to oocyst infection with allopatric isolates of the human malaria parasite P. falciparum (Boyd et al, 1938; Boyd and Jobbins, 1940; Eyles and Young, 1950; Jeffery et al, 1950), but the mechanism of refractoriness to this malaria parasite species is unknown
Summary
Anopheles albimanus is an important vector of human malaria throughout central America (Pan American Health Organization, 1996). With regard to the human malaria parasite species Plasmodium falciparum and Plasmodium vivax, A. albimanus tends to be susceptible only to infection with naturally-encountered (i.e. coindigenous or sympatric) malaria parasite species/strains, implying a relatively high degree of specificity in the relationship between malaria parasites and this mosquito species (Boyd et al, 1938; Boyd and Jobbins, 1940; Jeffery et al, 1950, 1954; Eyles, 1960; Warren and Collins, 1981; Teklehaimanot et al, 1987; Vaughan et al, 1994b; Gonzalez-Ceron et al, 1999, 2007; Rodriguez et al, 2000; Li et al, 2001; Joy et al, 2008). There are considerable differences in susceptibility to malaria infection between different strains of A. albimanus, indicating the existence of complex interactions determining parasite–vector compatibility
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