Distribution and habitat
Anopheles funestus is found in tropical sub-Saharan Africa, its range extending from Senegal to Ethiopia, Angola, South Africa and Madagascar. [4] Breeding takes place in water, any permanent or semi-permanent body of fresh water with some emergent vegetation being suitable, including swamps, lake verges, ponds and rice paddies. The larvae inhabit both sunlit and shaded locations, the vegetation probably being effective in reducing predation. [2] In the Sahel, increased aridity has moved the northern limit of its range southward by about 100 km (62 mi). Although it is considered to be a single species, part of a species complex, it shows some anomalies of behaviour across its range. It is present in the paddy fields of Madagascar but not in those of West Africa; it used to breed in fast-moving streams in South Africa before being largely eliminated by the use of insecticides, but when it became re-established there via Mozambique, it bred in swamps. [4] It is present in mountainous areas of East Africa at altitudes of up to 2,000 m (6,600 ft) but is largely absent from forests. [4]
Behaviour
The female mosquito lays a raft of eggs on the surface of water. The larval and pupal stages of the life cycle take place under water, but after metamorphosis, adults of both sexes leave the water and visit flowers to feed on nectar. Before it starts to breed, the female mosquito needs a meal of vertebrate blood to provide the protein it needs for egg production; the male does not bite. [5] The adult female Anopheles funestus is "anthropophilic", being attracted to people rather than to other animals; however this is not invariably the case, as in Senegal, the populations of this mosquito in the west of the country feed on human blood while those in the east favour that of other mammals (zoophilic). It is also "endophilic" in its behaviour; this means it is attracted to the inside of human habitations, both when feeding and when resting. It feeds at night, typically after 10 p.m. and usually between midnight and dawn, which gives it access to widely dispersed hosts in a non-alert state. [2]
Insecticide resistance
This is a highly adaptable species and many populations have developed resistance to pyrethroid insecticides, resulting in an upsurge of malarial infections in sub-Saharan Africa in the 1990s. [2] Since large scale deployment of insecticides began in the 1950s, An. funestus has rapidly evolved resistance throughout much of its range. [3] A. funestus has widespread resistance to DDT and pyrethroids in Southern and West Africa, and in the Tororo District of Uganda in the east of the continent. [7] The Tororo population was, however, entirely susceptible to bendiocarb, malathion, and dieldrin. [7]
A clearer genomic view on continental population structure is crucial for implementing strategic use of insecticides, taking into account the potential emergence and spread of insecticide resistance alleles. Additionally, with the implementation of gene drive release for vector control likely in the coming years, we need to be able to predict the spread of gene drive under different release scenarios, which is only possible if detailed knowledge of population connectivity across the continent, and how it varies along the genome, is in place. [3]
Recent Studies
In 2017, Bodee and his team put an open call to join the project through contributing wild An. funestus samples collected from 2014 onwards. They carried out short- read sequencing at ~35x coverage depth for >800 wild- caught specimens, of which 656 individuals from 13 African countries [Benin (BJ); Cameroon (CM); Central African Republic (CF); Democratic Republic of the Congo, Kinshasa (CD-K) and Haut-Uélé (CD-H); Gabon (GA); Ghana, Northern Region (GH-N) and Ashanti (GH-A); Kenya, Western Province (KE-W) and Nyanza (KE-N); Malawi (MW); Mozambique, Cabo Delgado (MZ-C) and Maputo (MZ-M); Nigeria (NG); Tanzania (TZ); Uganda (UG); and Zambia (ZM)], and 45 historic specimens (collected 1927 to 1967) from 16 African countries, and passed all quality control (QC) evaluations. [3]
Sequencing reads were aligned to a 251- Mbp high- quality chromosomal reference ge nome created from a wild- caught individual from Gabon, and each successfully sequenced sample was assigned to a geographic cohort based on its original collection location. Using a static-cutoff (sc) site filter, 73 million out of 162 million (45%) acces sible sites were segregating among the sequenced samples. Disregarding singletons, 49 million single- nucleotide polymorphisms (SNPs) were present on two or more chromosomes, 17.3% of which had more than two alleles. [3]
Discussion
Even if the Gambiae Complex disappeared today, malaria will still rage through Africa until An. funestus is also effectively targeted. The greater understanding of the high levels of genetic diversity and the complex population structure of An. funestus presented in this study will under pin smarter surveillance and targeted vector control More than 4000 km separates the sampling sites of the Equatorial cohort (from Ghana Ashanti to Western Kenya), yet populations from across that range are genetically connected, whereas much geographically closer popula tions, such as South Benin and North Ghana, are genetically distinc. [3]
Some of this structure may originate from geographic discon tinuities, such as the Congo basin rainforest and the Rift valley; some may originate from differences in climate and rainfall; and some may be due to local adaptation that we do not fully understand. [3]
The observations in this dataset regarding insecticide resistance further underscore the need to consider locally tailored control strategies. We identified strong selective sweeps centered on known insecticide resistance genes, where the same mutations tend to confer resistance and be under selection in a wide range of insects as well as in An. gambiae. However, these shared mutations clearly sometimes occur independently on multiple distinct haplotypic backgrounds, suggesting that An. funestus populations may not be mutation limited. [3]
This convergent evolution of resistance mechanisms highlights the adaptability of these vector populations and emphasizes the need for tailored interventions that consider local genetic backgrounds and resistance profiles. Insecticide resistance in An. funestus results from a complex interplay between convergent evolution, sharing of resistance alleles between populations, and changing selective pres sures in space and time and calls for the continued monitoring of resistance alleles alongside the development and deployment of newly identified insecticides or alternative control strategies. [3]
The existence of these ecotypes near the Equatorial population, which ranges across a vast area, highlights the complexity of population structure in An. funestus. This complexity together with the high genetic diversity of the species suggests that a one- size- fits- all approach to An. funestus vector control may be ineffective. [3]
Results
They found that the 17 geographic regions from which our samples originated form six population clusters with varying degrees of genome- wide differentiation. One of these populations, the Equatorial cohort, spans more than 4000 km and comprises individuals from seven countries. In close geographic proximity to this cohort, we found two genetically distinct ecotypes that appear to have a restricted range and distinct chromosomal karyotypes. Using a windowed principal components analysis (PCA) approach, we explored structure across the genome. We used this approach to identify segregating inversions and classify every individual into its specific inversion karyotype. We also identified genomic regions that have exceptional levels of divergence in comparison to other collinear parts of the genome. Some of these outlier regions are clearly driven by selection for insecticide resistance, as they contain loci with excessive haplo type sharing, often centered on genes known to play a role in insecticide resist ance in many insect species. We show that the Gste2 resistance allele has at least two independent origins and that, despite reports of DDT resistance emerging in the 1950s, none of the historic samples in this study carry DDT resistance alleles found in modern-day populations. [3]
Conclusions
Variable structure—such as that observed in this work, with some populations readily sharing alleles across the continent, and others clearly geographically proximal but geneti cally distinct—is a challenge for vector control. Even if the Gambiae Complex disappeared today, malaria would still rage through Africa until An. funestus is also effectively targeted. The greater understanding of the high levels of genetic diversity and the complex population structure of An. funestus presented in this study will underpin smarter surveillance and targeted vector control. [3]
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