Open AccessMultiple blood feeding in mosquitoes shortens the Plasmodium falciparum incubation period and increases malaria transmission potential
Author(s) -
W. Robert Shaw,
Inga Holmdahl,
Maurice A. Itoe,
Kristine Werling,
Meghan Marquette,
Douglas G. Paton,
Naresh Singh,
Caroline O. Buckee,
Lauren M. Childs,
Flaminia Catteruccia
Publication year - 2020
Publication title -
plos pathogens
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 3.719
H-Index - 206
eISSN - 1553-7374
pISSN - 1553-7366
DOI - 10.1371/journal.ppat.1009131
Subject(s) - anopheles gambiae , biology , malaria , plasmodium falciparum , anopheles , parasite hosting , transmission (telecommunications) , vector (molecular biology) , plasmodium (life cycle) , population , incubation period , basic reproduction number , gametocyte , virology , immunology , incubation , medicine , environmental health , gene , genetics , recombinant dna , biochemistry , world wide web , computer science , electrical engineering , engineering
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 R 0 , and find the average R 0 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.