Anopheles mosquitoes are the only arthropod vectors that transmit Plasmodium parasites that cause malaria in humans. The disease imposes a significant burden of mortality and morbidity, particularly in Sub-Saharan Africa (SSA) 1 where the most efficient mosquito vectors of malaria are found 2. Human malaria is mediated only by female Anopheles, and of the estimated 460 species, only 40 species or species complexes are considered to be important vectors in the wild 3, notably the Anopheles gambiae and Anopheles funestus species complexes that dominate malaria transmission throughout SSA4. In this paper, we focus on the three major East African vectors of human malaria: An. funestus sensu stricto, An. gambiae sensu stricto and An. arabiensis.
The successful transmission of Plasmodium parasites between humans requires intricate transformations within the mosquito vector 5, highlighting the key role of both vectorial capacity 6 and vector competence 7 in determining the local intensity of malaria transmission 7.
Vector competence refers to the ability of an arthropod vector to acquire, maintain and transmit a pathogen. This concept encompasses the inherent ability of a pathogen to effectively enter and reproduce within the vector and be released from the vector's salivary glands to initiate infection in another vertebrate host 7,8. Vectorial capacity describes the potential intensity of transmission by mosquitoes. It is defined as the total number of infectious mosquito bites on humans that will arise from a single infected person on a single day 9. This is influenced by a number of factors 6,10, most notably the probability of mosquitoes to feed on humans 11, daily vector survival 12, environmental factors that affect the time it takes for parasites to develop in the mosquito host 13, the availability of larval breeding sites 14, presence of vector control tools10 and vector competence15.
The vectoral capacity of a particular vector is strongly influenced by its ecology. The larval stage of mosquitoes takes place in water where biological factors greatly influence the habitat suitability and carrying capacity. These factors influence vector presence 3, fitness 16, longevity 17, which in turn affects the probability that a mosquito can acquire and maintain a parasite for long enough to become infectious 18. In East Africa, the three major vectors have different regional distribution due to ecology 19 and hydrology 14 and varying contributions to malaria transmission across different seasons 20–23. An. funestus mosquitoes have permanent breeding sites abundant with vegetation, making them likely to transmit malaria all year round 24,25. An. arabiensis and An. gambiae s.s. typically dominate in temporary sunlit pools and their presence is strongly dependent on rainfall or irrigation 26,27. An. gambiae s.s. requires high humidity to survive and occurs almost exclusively during humid and rainy periods 28. An. arabiensis and An. funestus, are more resistant to desiccation, are commonly found in abundance during the peak of the wet season and continue into the dry season; sustaining malaria transmission for several months after the end of the rains23,29.
Anopheles mosquitoes are dependent on vertebrate blood to provide proteins needed for egg development and undergo multiple cycles of feeding and egg development in their lifetime. Therefore, the preference of a vector for human blood has a direct impact on its efficiency as a vector by increasing its probability of acquiring and transmitting onward infection30. An. arabiensis have an opportunistic feeding behavior, targeting both human and animal hosts for its blood meals, so it may be a more or less important vector dependent on the relative proportion of cattle in an area 31. An. gambiae 32and An. funestus 33are more specialized blood feeders, feeding almost entirely on humans, although this does depend on host availability. In addition, there is evidence that multiple blood meals increase the likelihood of Plasmodium developing in the mosquito 34,35.
As well as environmental factors that affect vectors' susceptibility to infection and the interactions between the vector, pathogen, and host that impact probabilities of onward transmission, vector competence is influenced by a variety of internal factors, including the genetics of both the vector and the pathogen 5,36. Plasmodium takes resources from its definitive host that results in reduced fitness and reproductive output 37. Therefore, the mosquito innate immune system either modulates or resists infection 38, while the parasite counteracts mosquito defenses through host manipulation 39 and polyclonality40. Mosquito species show different levels of susceptibility to Plasmodium from refractory in the case of Anopheles quadriannulatus 41,42 to high susceptibility in Anopheles coluzzi 43,44.
In East Africa, there is evidence of higher proportions of infected An. funestus 45,46 relative to An. arabiensis and An. gambiae. This can be to an extent explained by the fact that An. funestus generally feeds almost exclusively on humans and has been shown to live longer than An. arabiensis 47. However, any differences in degree of vector competence among the three primary malaria vectors has not been evaluated. Understanding vector competence is crucial in understanding the risk of malaria transmission, informing effective malaria control strategies 36,48,49 and parameterizing mathematical models, where mosquito-parasite interactions are rarely considered 15,50.
Therefore, this study investigated whether vector competence towards Plasmodium falciparum differs between local East African strains of An. gambiae s.s., An. funestus and An. arabiensis mosquitoes. By experimentally infecting mosquitoes with field gametocytes using Direct Membrane Feeding Assays (DMFAs), we aim to compare the prevalence and intensity of P. falciparum infection between these Anopheles mosquito species.