Multiple blood feeding in mosquitoes shortens the Plasmodium falciparum incubation period and increases malaria transmission potential

• Published in: PLoS pathogens Vol. 16; no. 12; p. e1009131
• Main Authors: Shaw, W Robert, Holmdahl, Inga E, Itoe, Maurice A, Werling, Kristine, Marquette, Meghan, Paton, Douglas G, Singh, Naresh, Buckee, Caroline O, Childs, Lauren M, Catteruccia, Flaminia
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 31-12-2020; Public Library of Science (PLoS)
• Subjects: Animals; Anopheles; Anopheles - parasitology; Antibodies; Behavior; Biology and Life Sciences; Blood; Blood meals; Chi-square test; Circumsporozoite protein; Deoxyribonucleic acid; Deprivation; Development and progression; Disease transmission; DNA; Egg laying; Feeding Behavior; Female; Females; Immunofluorescence; Incubation; Infectious Disease Incubation Period; Insect control; Insecticides; Life span; Lipids; Malaria; Malaria, Falciparum - transmission; Mathematical models; Meals; Medicine and Health Sciences; Midgut; Mosquito Vectors - parasitology; Mosquitoes; Nutrient cycles; Oocysts; Parasites; Parasitological research; Physiological aspects; Plasmodium falciparum; Plasmodium falciparum - growth & development; Reproductive cycle; Reproductive status; Risk factors; Salivary gland; Salivary glands; Sporozoites; Statistical analysis; Statistical models; Statistical tests; Time measurement; Vector-borne diseases; United States; Africa
• ISSN: 1553-7374; 1553-7366; 1553-7374
• DOI: 10.1371/journal.ppat.1009131

Many mosquito species, including the major malaria vector Anopheles gambiae, naturally undergo multiple reproductive cycles of blood feeding, egg development and egg laying in their lifespan. Such complex mosquito behavior is regularly overlooked when mosquitoes are experimentally infected with malaria parasites, limiting our ability to accurately describe potential effects on transmission. Here, we examine how Plasmodium falciparum development and transmission potential is impacted when infected mosquitoes feed an additional time. We measured P. falciparum oocyst size and performed sporozoite time course analyses to determine the parasite's extrinsic incubation period (EIP), i.e. the time required by parasites to reach infectious sporozoite stages, in An. gambiae females blood fed either once or twice. An additional blood feed at 3 days post infection drastically accelerates oocyst growth rates, causing earlier sporozoite accumulation in the salivary glands, thereby shortening the EIP (reduction of 2.3 ± 0.4 days). Moreover, parasite growth is further accelerated in transgenic mosquitoes with reduced reproductive capacity, which mimic genetic modifications currently proposed in population suppression gene drives. We incorporate our shortened EIP values into a measure of transmission potential, the basic reproduction number R0, and find the average R0 is higher (range: 10.1%-12.1% increase) across sub-Saharan Africa than when using traditional EIP measurements. These data suggest that malaria elimination may be substantially more challenging and that younger mosquitoes or those with reduced reproductive ability may provide a larger contribution to infection than currently believed. Our findings have profound implications for current and future mosquito control interventions.