The dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum, and their transmission by Anopheles stephensi, Anopheles gambiae and Aedes aegypti

• Published in: International journal for parasitology Vol. 33; no. 9; pp. 933 - 943
• Main Authors: Alavi, Y., Arai, M., Mendoza, J., Tufet-Bayona, M., Sinha, R., Fowler, K., Billker, O., Franke-Fayard, B., Janse, C.J., Waters, A., Sinden, R.E.
• Format: Journal Article
• Language: English
• Published: Oxford Elsevier Ltd 01-08-2003; Elsevier Science
• Subjects: Aedes; Aedes - parasitology; Aedes aegypti; Animals; Anopheles; Anopheles - parasitology; Anopheles gambiae; Anopheles stephensi; Biological and medical sciences; Disease Vectors; Female; Fundamental and applied biological sciences. Psychology; Host-Parasite Interactions; Humans; Life cycle. Host-agent relationship. Pathogenesis; Malaria; Malaria - parasitology; Malaria - transmission; Mosquitoes; Oocytes; Plasmodium - physiology; Plasmodium berghei; Plasmodium berghei - physiology; Plasmodium gallinaceum; Plasmodium gallinaceum - physiology; Protozoa; Salivary Glands - parasitology; Species Specificity; Mosquitoes; Plasmodium berghei; Anopheles; Malaria; Plasmodium gallinaceum; Aedes; Host parasite relation; Protozoal disease; Insecta; Anopheles gambiae; Transmission from animal to animal; Infectivity; Development; Vector; Protozoa; Apicomplexa; Life history; Parasite; Parasitosis; Infection; Anopheles stephensi; Arthropoda; Culicidae; Invertebrata; Diptera; Interspecific relation
• ISSN: 0020-7519; 1879-0135; 1879-0135
• DOI: 10.1016/S0020-7519(03)00112-7

Knowledge of parasite–mosquito interactions is essential to develop strategies that will reduce malaria transmission through the mosquito vector. In this study we investigated the development of two model malaria parasites,
Plasmodium berghei and
Plasmodium gallinaceum, in three mosquito species
Anopheles stephensi, Anopheles gambiae and
Aedes aegypti. New methods to study gamete production in vivo in combination with GFP-expressing ookinetes were employed to measure the large losses incurred by the parasites during infection of mosquitoes. All three mosquito species transmitted
P. gallinaceum;
P. berghei was only transmitted by
Anopheles spp.
Plasmodium gallinaceum initiates gamete production with high efficiency equally in the three mosquito species. By contrast
P. berghei is less efficiently activated to produce gametes, and in
Ae. aegypti microgamete formation is almost totally suppressed. In all parasite/vector combinations ookinete development is inefficient, 500–100,000-fold losses were encountered. Losses during ookinete-to-oocyst transformation range from fivefold in compatible vector parasite combinations (
P. berghei/
An. stephensi), through >100-fold in poor vector/parasite combinations (
P. gallinaceum/An. stephensi), to complete blockade (>1,500 fold) in others (
P. berghei/
Ae. aegypti).
Plasmodium berghei ookinetes survive poorly in the bloodmeal of
Ae. aegypti and are unable to invade the midgut epithelium. Cultured mature ookinetes of
P. berghei injected directly into the mosquito haemocoele produced salivary gland sporozoites in
An. stephensi, but not in
Ae. aegypti, suggesting that further species-specific incompatibilities occur downstream of the midgut epithelium in
Ae. aegypti. These results show that in these parasite–mosquito combinations the susceptibility to malarial infection is regulated at multiple steps during the development of the parasites. Understanding these at the molecular level may contribute to the development of rational strategies to reduce the vector competence of malarial vectors.