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Badolo, A.

Publications and source records attributed to Badolo, A..

14 recordsLinked to original sources

Rapid urban evolution of the dengue mosquito in West African cities

Aedes aegypti is an exceptionally effective global vector of human disease because of its strong specialization on human hosts and habitats. However, in its native range in Africa, many populations never specialized on humans and retained an ancestral generalist ecology. Now, in the rapidly growing cities of Kumasi, Ghana and Ouagadougou, Burkina Faso, we directly document genomic and behavioral evidence of a sudden shift towards greater specialization on humans over just five years. These changes are likely to enhance the ability of these urban mosquito populations to serve as effective vectors of human disease and may have played a role in unprecedented recent outbreaks of dengue fever in West African cities.

evolutionary biology↗

Ecological genomics of preference for human hosts in the native range of the dengue mosquito

The arbovirus transmitting mosquito Aedes aegypti has African origins where it maintains generalist and human specialist feeding forms, the latter of which has recently expanded their range worldwide. These two different forms appear to be directly linked to discrete genetic lineages, where the relative proportion of each ancestry dictates a mosquitos standing on the human specialist-generalist behavior spectrum. Here we take a population genomics approach to develop a predictive model for describing the distribution of human specialist behavior across Africa. We show genome-wide ancestry is predictive of human specialist behavior, but a subset of the genome offers even greater predictability. We also show that an ecological model incorporating precipitation, temperature and human density explains the geographic patterning of human specialist behavior in Africa.

evolutionary biology↗

Strong selection of Gammaproteobacteria across Aedes aegypti development suggests diagonal microbiome transmission

BackgroundAedes aegypti mosquitoes are the main vector of pathogens like dengue virus and chikungunya virus. The immature life stages of mosquitoes share the same habitat with a variety of microorganisms in aquatic environments. To better understand the microbial diversity in field-derived Ae. aegypti, we analysed simultaneously collected larvae, pupae, and freshly emerged adults from Burkina Faso together with their breeding water via 16S rRNA gene sequencing. ResultsWe observed a decrease in bacterial diversity and load across the mosquito life stages. At the phylum level, a strong increase in relative abundance of Proteobacteria was found along the mosquito stages. The same 40 amplicon sequence variants were consistently found as most abundant in the adults, regardless of the sample collection site, and all belonged to the Gammaproteobacteria. Our data suggest that these bacteria were not randomly derived by chance from the environment in the mosquito but rather deposited by a female mosquito during oviposition, a transmission route recently coined as "diagonal transmission". Indeed, our results indicated that there is a selection of Gammaproteobacteria from the breeding water and that these bacterial members are further maintained from larvae to adults. ConclusionThis study provided new data on the microbiome composition of field-collected Ae. aegypti, contributing to an enhanced understanding of the origin and colonization route of the mosquito microbiome, potentially via a diagonal transmission route.

microbiology↗

Morphological and genetic heterogeneity in Aedes aegypti (Diptera: Culicidae) populations across diverse landscapes in West Africa

Native to sub-Saharan Africa, Aedes aegypti has spread across the globe and is now one of the most significant vectors of arboviruses worldwide. However, data on the ranges of its populations remain sparse, and the genetic variability and ecological adaptability in West Africa are still poorly understood. In this study, we characterized the morphological and genetic diversity of Ae. aegypti across four landscape types (urban, peri-urban, rural, and sylvatic sites) in three West African countries (Burkina Faso, Cote dIvoire, and Ghana). Ae. aegypti exhibited significant variation in abdominal scaling patterns across countries and landscape types, with the sylvatic and urban populations in Burkina Faso displaying the highest proportions of white scales (>50% white scales), while black scales predominated among those from Cote dIvoire and Ghana (>80% black scales). Wing shape displayed limited differentiation between the countries, landscape types, and genetic clusters. Bayesian analysis indicated high gene flow among populations, with notable outliers observed in sylvatic sites from Burkina Faso and admixture patterns suggesting possible human-mediated dispersal. Additionally, two major mitochondrial lineages, clades A and B, were identified. Most samples were categorized under clade B, showing no evidence of clustering by country or landscape type. In contrast, clade A comprised primarily sylvatic specimens from Burkina Faso and a single urban individual from Cote dIvoire. These findings highlight the complex interplay of genetic, environmental, and ecological factors shaping the variations in Ae. aegypti populations in West Africa. They provide insights into the phenotypic and genetic diversity of Ae. aegypti, offering valuable implications for understanding arbovirus transmission dynamics and formulating targeted interventions against arboviral diseases.

ecology↗

From macro to micro: De novo genomes of Aedes mosquitoes enable comparative genomics among close and distant relatives

The yellow fever mosquito (Aedes aegypti) is an organism of high medical importance because it is the primary vector for diseases such as yellow fever, Zika, dengue, and chikungunya. Its medical importance has made it a subject of numerous efforts to understand their biology. One such effort, was the development of a high-quality reference genome (AaegL5). However, this reference genome was sourced from a highly inbred laboratory strain with unknown geographic origin. Thus, the reference is not representative of a wild mosquito, let alone one from its native range in sub-Saharan Africa. To better understand the genetic architecture of Ae. aegypti and their sister species, we developed two de novo chromosome-scale genomes with sequences sourced from single individuals: one of Ae. aegypti formosus (Aaf) from Burkina Faso and one of Ae. mascarensis (Am) from Mauritius. Both genomes exhibit high contiguity and gene completeness, comparable to AaegL5. While Aaf exhibits high degree of synteny to AaegL5, it also exhibits several large inversions. We further conducted comparative genomic analyses using our genomes and other publicly available culicid reference genomes to find extensive chromosomal rearrangements between major lineages. Overrepresentation analysis of expanded genes in Aaf, AaegL5, and Am revealed that while the overarching category of genes that have expanded are similar, the specific genes that have expanded differ. Our findings elucidate novel insights into chromosome evolution at both microevolutionary and macroevolutionary scales. The genomic resources we present are additions to the arsenal of biologists in understanding mosquito biology and genome evolution. SignificanceAedes aegypti is a major arboviral disease vector found throughout the tropics and sub-tropics. Its subspecies differ ecologically, as native sub-Saharan African form feeds on mammals generally and inhabit both sylvatic and domestic areas and the global invasive form preferentially feeds on humans and lives primarily domestic areas. Their medical importance has prompted the development of a high-quality reference genome, but it was sourced from an inbred laboratory strain of unknown origin. Here, we leveraged PacBio HiFi sequencing and HiC sequencing to develop the first de novo genome of Ae. aegypti sampled its native range in Burkina Faso. We also present a de novo genome of Ae. mascarensis, its sister species. Our genomes are comparably contiguous and complete to the reference genome. Comparative genomic analysis using our genomes and other culicid reference genomes reveal extensive chromosomal rearrangements.

genomics↗

Mosquito Wing Image Repository for Advancing Research on Geometric Morphometric- and AI-Based Identification

Accurate identification of mosquito species is essential for effective vector control and mitigation of mosquito-borne disease outbreaks. Traditional morphological identification requires highly specialized personnel and is time-consuming, while molecular techniques can be cost-effective and dependent on comprehensive genetic information. Wing geometric morphometry has emerged as a promising alternative, leveraging detailed geometric measurements of wing shapes and vein patterns to distinguish between species and detect intraspecies variations. This paper presents a curated dataset of 18,104 mosquito wing images, collected from 10,500 mosquito specimens, annotated with extensive meta-information, designed to support research in wing geometric morphometry and the development of machine learning models, ultimately supporting efforts in vector surveillance and research.

ecology↗

Sequencing 1206 genomes reveals origin and movement of Aedes aegypti driving increased dengue risk

The number of dengue cases worldwide has increased ten-fold over the past decade as Aedes aegypti, the primary vector of this disease, thrives and expands its distribution, revealing limitations to current control methods. To better understand how Ae. aegypti evolved from a forest dwelling, generalist species to a highly anthropophilic urban species and the impact of contemporary gene flow on the future of dengue control, we sequenced 1,206 genomes from mosquitoes collected at 74 locations around the globe. Here we show that after evolving a preference for humans in the Sahel region of West Africa, the origin of the fully domesticated, anthropophilic subspecies Ae. aegypti aegypti (Aaa) occurred in the Americas during the Atlantic Slave Trade era and was followed by its explosive expansion around the globe. In recent decades, Aaa has invaded coastal Africa, the ancestral home range, introducing insecticide resistance mutations and an affinity for human hosts. Evidence of back-to-Africa migration is found in regions with recent dengue outbreaks, raising concern that global movement of Aaa could increase transmission risk of arboviruses including dengue in urban Africa. These data provide a platform to further study this important mosquito vector species and underscore developing complexity in the fight to limit the spread of dengue, Zika, and chikungunya diseases.

genomics↗

Global genomics of Aedes aegypti unveils widespread and novel persistent infectious viruses capable of triggering a small RNA response

The mosquito Aedes aegypti is a prominent vector for arboviruses, but the breadth of mosquito viruses that infects this specie is not fully understood. In the broadest global survey to date of over 200 Ae. aegypti small RNA samples, we detected viral small interfering RNAs (siRNAs) and Piwi interacting RNAs (piRNAs) arising from mosquito viruses. We confirmed that most academic laboratory colonies of Ae. aegypti lack persisting viruses, yet two commercial strains were infected by a novel tombus-like virus. Ae. aegypti from North to South American locations were also teeming with multiple insect viruses, with Anphevirus and a bunyavirus displaying geographical boundaries from the viral small RNA patterns. Asian Ae. aegypti small RNA patterns indicate infections by similar mosquito viruses from the Americas and reveal the first wild example of dengue virus infection generating viral small RNAs. African Ae. aegypti also contained various viral small RNAs including novel viruses only found in these African substrains. Intriguingly, viral long RNA patterns can differ from small RNA patterns, indicative of viral transcripts evading the mosquitoes RNA interference (RNAi) machinery. To determine whether the viruses we discovered via small RNA sequencing were replicating and transmissible, we infected C6/36 and Aag2 cells with Ae. aegypti homogenates. Through blind passaging, we generated cell lines stably infected by these mosquito viruses which then generated abundant viral siRNAs and piRNAs that resemble the native mosquito viral small RNA patterns. This mosquito small RNA genomics approach augments surveillance approaches for emerging infectious diseases.

genomics↗

Three years of insecticide resistance evolution and associated mechanisms in Aedes aegypti populations of Ouagadougou, Burkina Faso.

BackgroundResistance to insecticides is spreading among populations of Aedes aegypti, the primary vector of important human arboviruses. The escalating insecticide resistance poses a significant threat to dengue vector control, with an expanding number of countries affected by the disease. To gain a deeper insight into the evolution of insecticide resistance, it is essential to have longitudinal surveillance results, which are currently lacking, particularly from African Ae. aegypti populations. Here we report on three-years of surveillance of Ae. aegypti susceptibility to insecticide resistance phenotypes and associated kdr mutations in Burkina Faso, a country with regular dengue outbreaks. MethodsAe. aegypti susceptibility to insecticides and the V410L, V1016I, and F1534C kdr target site mutations linked to pyrethroid insecticide resistance were monitored in Ouagadougou from 2016 to 2018. Larvae were collected from artificial containers at two sites and reared to adulthood in an insectary. Bioassays were conducted on female adults, alongside with a laboratory-susceptible strain, following standard WHO protocols. Allele-specific PCR genotyping assays were utilized to identify the V410L, V1016I, and F1534C kdr pyrethroid target site mutations. ResultsBioassays revealed a high level of resistance to permethrin and deltamethrin that progressively increased over the three-year period in both localities. The 1534C mutation was nearly fixed throughout the three years at each locality, and while the closely related 410L and 1016I mutations did not vary between localities, their frequency notably increased from 2016 to 2018. Interestingly, Ae. aegypti populations in both areas remained susceptible to bendiocarb, fenitrothion, and malathion. Modeling the mortality data further confirmed the escalating resistance trend over the years and emphasized the significant role played by the three kdr mutations in conferring resistance to pyrethroids. ConclusionMortality rates indicate that Ae. aegypti populations from Ouagadougou are becoming increasingly resistant to pyrethroid insecticides, likely due to an increase in the frequencies of the 410L and 1016I kdr mutations. Organophosphate insecticides are likely to be better alternative options for control.

evolutionary biology↗

Discovery and characterization of chromosomal inversions in the arboviral vector mosquito Aedes aegypti

Chromosomal inversions play a fundamental role in evolution and have been shown to regulate epidemiologically important traits in malaria mosquitoes. However, they have never been characterized in Aedes aegypti, the major vector of arboviruses, because of the poor structure of its polytene chromosomes. In this study, we applied a Hi-C proximity ligation approach to identify chromosomal inversions in 25 strains of Ae. aegypti, acquired from its worldwide distribution, as well as in one strain of Ae. mascarensis. The study identified 21 multi-megabase inversions with uneven distributions along the three chromosomes. All chromosomal inversions, including one specific for Ae. mascarensis, were polymorphic. Nevertheless, geographic origin separated the strains into two clusters carrying African and non-African inversions suggesting their potential association with Ae. aegypti subspecies. Some of the inversions colocalized with chemoreceptor genes and quantitative trait loci associated with pathogen infection, implicating the potential role of inversions in host choice and disease transmission.

evolutionary biology↗

Extensive variation and strain-specificity in dengue virus susceptibility among African Aedes aegypti populations

African populations of the mosquito Aedes aegypti are usually considered less susceptible to infection by human-pathogenic flaviviruses than globally invasive populations found outside Africa. Although this contrast has been well documented for Zika virus (ZIKV), it is unclear to what extent it is true for dengue virus (DENV), the most prevalent flavivirus of humans. Addressing this question is complicated by substantial genetic diversity among DENV strains, most notably in the form of four genetic types (DENV1 to DENV4), that can lead to genetically specific interactions with mosquito populations. Here, we carried out a continent-wide survey of DENV susceptibility using a panel of field-derived Ae. aegypti colonies from across the African range of the species and a colony from Guadeloupe, French West Indies as non-African reference. We found considerable variation in the ability of African Ae. aegypti populations to acquire and replicate a panel of six DENV strains spanning the four DENV types. Although African Ae. aegypti populations were generally less susceptible than the reference non-African population from Guadeloupe, in several instances some African populations were equally or more susceptible than the Guadeloupe population. Moreover, the relative level of susceptibility between African mosquito populations depended on the DENV strain, indicating genetically specific interactions. We conclude that unlike ZIKV susceptibility, there is no clear-cut dichotomy in DENV susceptibility between African and non-African Ae. aegypti. DENV susceptibility of African Ae. aegypti populations is highly heterogeneous and largely governed by the specific pairing of mosquito population and DENV strain. Author summaryAfrican populations of the mosquito Aedes aegypti are usually thought to be less likely to get infected by flaviviruses compared to Ae. aegypti mosquitoes found outside Africa. While this has been well-demonstrated for Zika virus, it is not clear if the same is true for dengue virus, which is the most common flavivirus in humans. Studying this is complicated by the strain diversity of dengue virus, including four main genetic types, potentially causing different interactions. In this study, we compared several mosquito populations and found that, in general, African mosquitoes were less likely to get infected by dengue virus compared to mosquitoes from outside Africa. However, in some cases, African mosquitoes were just as or even more likely to get infected. The specific strain of dengue virus also influenced how likely African mosquitoes were to get infected, showing that the relationship between African mosquitoes and dengue virus is complex.

microbiology↗

Molecular signature of domestication in the arboviral vector Aedes aegypti

BackgroundDomestication is a complex, multi-stage and species-specific process that results in organisms living close to humans. In the arboviral vector Aedes aegypti adaptation to living in proximity with anthropogenic environments has been recognized as a major evolutionary shift, separating a generalist form, Aedes aegypti formosus (Aaf), from the domestic form Aedes aegypti aegypti (Aaa), which tends to deposit eggs artificial containers and bite humans for a blood meal. These behaviors enhance the mosquito vectorial capacity. The extent to which domestication has impacted the Ae. aegypti genome has not been thoroughly investigated yet. ResultsTaking advantage of two forms distinct and historically documented geographic distributions, we analyzed the genomes of 634 worldwide Ae. aegypti mosquitoes. Using more than 300 million high-confidence SNPs, we found a unique origin for all out-of-Africa Ae. aegypti mosquitoes, with no evidence of admixture events in Africa, apart from Kenya. A group of genes were under positive selection only in out-of-Africa mosquitoes and 236 genes had nonsynonymous mutations, occurring at statistically different frequencies in Aaa and Aaf mosquitoes. ConclusionWe identified a clear signal of genetic differentiation between Aaa and Aaf, circumscribed to a catalogue of candidate genes. These "Aaa molecular signature" genes extend beyond chemosensory genes to genes linked to neuronal and hormonal functions. This suggests that the behavioral shift to domestication may rely on the fine regulation of metabolic and neuronal functions, more than the role of a few significant genes. Our results also provide the foundation to investigate new targets for the control of Ae. aegypti populations.

evolutionary biology↗

Dating the origin and spread of specialization on human hosts in Aedes aegypti mosquitoes

The globally invasive mosquito subspecies Aedes aegypti aegypti is a highly effective vector of human arboviruses because it specializes in biting humans and breeding in human habitats. Recent work suggests that specialization first arose as an adaptation to long, hot dry seasons in the West African Sahel, where Ae. aegypti is forced to rely on human-stored water for breeding. However, rainfall patterns in this region have changed dramatically over the past 10-20 thousand years, and we do not yet know exactly when specialization occurred. Here we use whole-genome cross-coalescent analysis to date the emergence of human specialist populations in the Sahel and thus further probe the climate hypothesis. Importantly, we take advantage of the known migration of human-specialist populations out of Africa during the Atlantic Slave Trade to calibrate the coalescent clock and thus obtain a more precise estimate of the older evolutionary event than would otherwise be possible. We find that human-specialist mosquitoes diverged rapidly from ecological generalists approximately 5,000 years ago, which corresponds to the end of the African Humid Period--a time when the Sahara dried and water stored by humans became a uniquely stable, aquatic niche in the Sahel. We also use population genomic analyses to date a previously observed influx of human-specialist alleles into major West African cities, where mosquitoes tend to be more attracted to humans than in nearby rural populations regardless of climate. In this case, the characteristic length of tracts of human-specialist ancestry present on a generalist genetic background in Kumasi, Ghana and Ouagadougou, Burkina Faso suggests the change in behavior occurred during rapid urbanization over the last 20-40 years. Taken together, we show that the timing and ecological context of two previously observed shifts towards human biting in Ae. aegypti differ; climate was likely the original driver, but urbanization has become increasingly important in recent decades. Understanding the changing relationship between mosquitoes and humans over time is critical for predicting and managing burdens of mosquito-borne disease.

evolutionary biology↗

Climate and urbanization drive mosquito preference for humans

The majority of mosquito-borne illness is spread by a few mosquito species that have evolved to specialize in biting humans, yet the precise causes of this behavioral shift are poorly understood. We address this gap in the arboviral vector Aedes aegypti. We first characterize the behaviour of mosquitoes from 27 sites scattered across the species ancestral range in sub-Saharan Africa, revealing previously unrecognized diversity in female preference for human versus animal odor. We then use modelling to show that this diversity can be almost fully predicted by two ecological factors - dry season intensity and human population density. Finally we integrate this information with whole genome sequence data from 345 individual mosquitoes to identify a single underlying ancestry component linked to human preference, with genetic changes concentrated in a few key chromosomal regions. Our findings strongly suggest that human-biting in this important disease vector originally evolved as a by-product of breeding in human-stored water in areas where doing so provided the only means to survive the long, hot dry season. Our model also predicts that changes in human population density are likely to drive future mosquito evolution. Rapid urbanization may drive a shift to human-biting in many cities across Africa by 2050.

evolutionary biology↗