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Biology subjects

Rose, N. H.

Publications and source records attributed to Rose, N. H..

12 recordsLinked to original sources

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↗

Olfactory receptor coexpression and co-option in the dengue mosquito

The olfactory sensory neurons of vinegar flies and mice tend to express a single ligand-specific receptor. While this one neuron-one receptor motif has long been expected to apply broadly across insects, recent evidence suggests it may not extend to mosquitoes. We sequenced and analyzed the transcriptomes of 46,000 neurons from antennae of the dengue mosquito Aedes aegypti to resolve all olfactory, thermosensory, and hygrosensory neuron subtypes and identify the receptors expressed therein. We find that half of all olfactory subtypes coexpress multiple receptors. However, coexpression occurs almost exclusively among genes from the same family--among odorant receptors (ORs) or among ionotropic receptors (IRs). Coexpression of ORs with IRs is exceedingly rare. Many coexpressed receptors are recent duplicates. In other cases, the recruitment or co-option of single receptors by multiple neuron subtypes has placed these genes together in the same cells with distant paralogs. Close examination of data from Drosophila reveal rare cases of both phenomena, indicating that the olfactory systems of these two species are not fundamentally different, but instead fall at different locations along a continuum likely to encompass diverse insects.

neuroscience↗

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↗

Thermal tolerance of mosquito eggs is associated with urban adaptation and human interactions

Climate change is expected to profoundly affect mosquito distributions and their ability to serve as vectors for disease, specifically with the anticipated increase in heat waves. The rising temperature and frequent heat waves can accelerate mosquito life cycles, facilitating higher disease transmission. Conversely, higher temperatures could increase mosquito mortality as a negative consequence. Warmer temperatures are associated with increased human density, suggesting a need for anthropophilic mosquitoes to adapt to be more hardy to heat stress. Mosquito eggs provide an opportunity to study the biological impact of climate warming as this stage is stationary and must tolerate temperatures at the site of female oviposition. As such, egg thermotolerance is critical for survival in a specific habitat. In nature, Aedes mosquitoes exhibit different behavioral phenotypes, where specific populations prefer depositing eggs in tree holes and prefer feeding non-human vertebrates. In contrast, others, particularly human-biting specialists, favor laying eggs in artificial containers near human dwellings. This study examined the thermotolerance of eggs, along with adult stages, for Aedes aegypti and Ae. albopictus lineages associated with known ancestry and shifts in their relationship with humans. Mosquitoes collected from areas with higher human population density, displaying increased human preference, and having a human-associated ancestry profile have increased egg viability following high-temperature stress. Unlike eggs, thermal tolerance among adults showed no significant correlation based on the area of collection or human-associated ancestry. This study highlights that the egg stage is likely critical to mosquito survival when associated with humans and needs to be accounted when predicting future mosquito distribution.

ecology↗

Intra-species quantification reveals differences in activity and sleep levels in the yellow fever mosquito, Aedes aegypti

Aedes aegypti is an important mosquito vector of human disease with a wide distribution across the globe. Climatic conditions and ecological pressure drive differences in the biology of several populations of this mosquito, including blood-feeding behavior and vector competence. However, no study has compared activity and/or sleep among different populations/lineages of Ae. aegypti. Having recently established sleep-like states in three mosquito species with observable differences in timing and amount of sleep among species, we investigated differences in activity and sleep levels among 17 Ae. aegypti lines drawn from both its native range in Africa and its invasive range across the global tropics. Activity monitoring indicates that all the lines show consistent diurnal activity, but significant differences in activity level, sleep amount, number of sleep bouts, and bout duration were observed among the lines. Variations in specific activity and sleep parameters were explained by differences in host preference, ancestry, and human population density for the lineages collected in Africa. This study provides evidence that the diurnal sleep and activity profiles for Ae. aegypti are consistent, but there are significant population differences for Ae. aegypti sleep and activity levels and interactions with humans may significantly impact mosquito activity and sleep.

physiology↗

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↗

Aalbo1200: global genetic differentiation and variability of the mosquito Aedes albopictus

The mosquito Aedes albopictus transmits human viruses including dengue and chikungunya and is an extremely successful invasive species expanding into new regions of the world. New tools are needed to complement existing tools to help monitor and control this species. Genomic resources are improving for this species including genome reference sequences, and whole genome sequencing data will help to catalog genetic diversity in this species and further enable genetic analysis. We collected populations of Ae. albopictus from throughout its distribution and generated whole genome sequencing data from population samples. These data will be used to address a number of basic and applied questions for this species. Here, we show genetic differentiation patterns among the tropical and temperate forms, as well as finer scale genetic clustering at the regional and population scale. These data and results will be a valuable resource for further study and tool development for this species.

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↗

Mechanisms of ecological divergence with gene flow in a reef-building coral on an isolated atoll in Western Australia

Understanding the mechanisms driving phenotypic variation in traits facing intensified selection from climate change is a crucial step in developing effective conservation and restoration initiatives. This is particularly true for reef-building corals, which are among the most vulnerable to climate change and are in dramatic decline globally. At the Rowley Shoals in Western Australia, the prominent reef flat becomes exposed on low tide and the stagnant water in the shallow atoll lagoons heats up, creating a natural laboratory for characterising the mechanisms that control phenotypic responses to different environments. We combined whole genome re-sequencing, common garden heat stress experiments, transcriptome-wide gene expression analyses, and symbiont metabarcoding to explore the mechanisms that facilitate survival in contrasting habitat conditions. Our data show that, despite high gene flow between habitats, spatially varying selection drives subtle shifts in allele frequencies at hundreds of loci. These changes were concentrated into several islands of divergence spanning hundreds of SNPs that showed strong linkage disequilibrium and were associated with a coordinated increase in minor allele frequencies in corals taken from the lagoon habitat, where the range of environmental conditions is greatest. Common garden heat stress assays showed individuals from the lagoon exhibited higher bleaching resistance than colonies from the reef slope, and RNAseq identified pronounced physiological differences between the corals from the two habitats, primarily associated with molecular pathways including cell signalling, ion transport and metabolism. Despite the pronounced physioloigical and environmental differences between habitats, metabarcoding of the Symbiodiniaceae ITS2 region revealed all colonies to be associated exclusively with the genus Cladocopium, with no detectable differences between habitats. This study contributes to the growing number of studies documenting the complex mechanisms that facilitate coral survival in extreme environments, and showcases the utility of combining multiple sequencing techniques to unravel complex climate-related traits.

genomics↗

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↗