Search bioRxiv⌕ Search

Biology subjects

Gloria-Soria, A.

Publications and source records attributed to Gloria-Soria, A..

7 recordsLinked to original sources

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↗

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↗

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↗

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↗

Improved Aedes aegypti mosquito reference genome assembly enables biological discovery and vector control

Female Aedes aegypti mosquitoes infect hundreds of millions of people each year with dangerous viral pathogens including dengue, yellow fever, Zika, and chikungunya. Progress in understanding the biology of this insect, and developing tools to fight it, has been slowed by the lack of a high-quality genome assembly. Here we combine diverse genome technologies to produce AaegL5, a dramatically improved and annotated assembly, and demonstrate how it accelerates mosquito science and control. We anchored the physical and cytogenetic maps, resolved the size and composition of the elusive sex-determining \"M locus\", significantly increased the known members of the glutathione-S-transferase genes important for insecticide resistance, and doubled the number of chemosensory ionotropic receptors that guide mosquitoes to human hosts and egg-laying sites. Using high-resolution QTL and population genomic analyses, we mapped new candidates for dengue vector competence and insecticide resistance. We predict that AaegL5 will catalyse new biological insights and intervention strategies to fight this deadly arboviral vector.

genomics↗