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Thesis submitted to the Faculty of Science, University of the Witwatersrand, in fulfilment of the requirement for the degree of Doctor of Philosophy 2019 School of Public Health University of the Witwatersrand, South Africa / Background: Spatial targeting of interventions is increasingly recognized as essential for malaria control, particularly in areas aiming for elimination. The associations between house characteristics and malaria transmission is known, but gaps remain on whether transmission is also influenced by factors such as distances between households or the degree to which houses are clustered. It is also important to identify new interventions that can be implemented by targeting critical points in the biology of major malaria vectors and common characteristics of human settlements. Such efforts will be essential to complement current major tools. Aims: This study had the following aims; (i) understand how households densities and their distances influence malaria transmission the study area , (ii) identify housing-related factors affecting residual transmission risks in the area (iii) assess opinions of residents on how house characteristics, settlement patterns and other environmental factors influencing malaria transmission, and (iv) identify effective complementary approaches that could be used to improve malaria control in these residual transmission area with high coverage of basic interventions such as long lasting treated nets. Methodology: A mixed methods approach was used, which included: (i) indoor and outdoor mosquito collections from fixed as well as randomly selected households over 12 months, (ii) characterization of physical and microclimatic conditions of the houses and surrounding environmental variables, (iii) assessing effects of spatial clustering of households on malaria transmission risks, and (iv) assessing community concerns regarding household and environmental factors influencing transmission. During these studies, swarms of Anopheles mosquitoes were discovered for the first time in this area. Therefore, additional quantitative and qualitative observations were made to characterize the swarms and assess how they could be targeted to complement malaria control efforts. Key findings: Despite the expansive use of LLINs in the area, factors associated with housing characteristics and settlement patterns as well as people’s perceptions contribute to persistent malaria transmission, and will need to be addressed for eventual elimination to be reached. The main findings of this study were as follows: (i) household occupancy influenced indoor mosquito density (ii) high house densities increased Anopheles biting risk but mosquito density declined as distances between houses increased beyond 50m; (iii) abundance of the vector Anopheles arabiensis peaked during high rainfall months (February-May), but An. funestus densities remained stable into the dry season (May-August); (iv) there were higher indoor densities of An. arabiensis and An. funestus in houses with mud walls compared to plastered or brick walls, open eaves compared to closed eaves and unscreened windows compared to screened windows; (v) most respondents were aware of associations between their house characteristics and malaria risks but carrying out improvements was constrained by financial costs and other household priorities; (vi) in all our surveys, An. funestus mosquitoes contributed approximately 85% of ongoing malaria transmission in the areas, even when occurring in far smaller densities than An. arabiensis; and (vii) with regards to complementary interventions, small scale studies demonstrated that mating swarms of both An. arabiensis and An. funestus could be readily identified and characterized (in this case by volunteer community members), and that targeting the swarms using aerosol spraying could possibly reduce overall biting risk in the communities. Conclusions: This study yielded evidence that malaria transmission risks are significantly lower when the distances between houses are high. Variation in malaria transmission risk within a village might be important for planning and implementing spatially targeted interventions. With limited resources, malaria control efforts must be prioritized in locations with significantly higher risk in order to obtain maximum benefit. Thus, the distances between houses should be considered when planning malaria vector control strategies. Furthermore, the overall clustering of indoor densities of major disease-transmitting mosquitoes is significantly associated with household occupancy and its spatial distribution within the villages. Further research is needed to assess the potential of using this information for predicting, identifying and targeting the most intense foci of mosquito-borne disease transmission based on household occupancy. Understanding the factors influencing malaria transmission at a small scale is crucial for planning malaria control interventions. Malaria transmission heterogeneity does not only exist on a large scale, but also at small scales, which may be influenced by small variations of environmental features, such as seasonality. These variations should be considered when improving malaria control interventions. While An. funestus showed variation in density during the year, numbers of mosquitoes remained high throughout the dry season, whereas An. arabiensis showed a definite peak in the rainy season with a subsequent drop during the dry season. Further studies are required to investigate the survival strategies of major malaria vectors during the dry season. Understanding this particular feature of An. funestus may lead to the design of new control strategies or improve existing interventions so as to reduce the malaria burden in such rural areas. This study also documented high mosquito densities in mud-walled houses compared to houses with brick or plastered walls. These findings further indicate the necessity of considering house improvement as a malaria control strategy. While the community members had fairly high awareness that improved houses were associated with reduced mosquito nuisance, many families in rural areas are living in poorly constructed houses. It is therefore necessary to consider inter-sectoral collaborations to integrate housing into health policies in Tanzania. Further studies are also needed to provide epidemiological evidence on how housing design affects malaria transmission. Furthermore, community-based house improvement programs should be promoted, including simple, scalable and affordable house improvements for the populations living in high malaria endemic areas in rural communities. Generally, this study has generated information which sets the basis for further studies on the relationship between the exact house location and malaria transmission risk in rural malaria endemic countries. / MT 2020

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Four developmental inhibitors (Altosid, Altozar, ZR-619 and ZR-777) and two organophosphates (Parathion and Abate) were tested on Aedes aegypti under laboratory conditions. When applied to fourth-instar larvae, the organophosphates were more toxic than the developmental inhibitors. Concentrations required for standard kills (LC50 and LC95) were lower for Altosid and ZR-619 than for Altozar and ZR-777. Field applications of Altosid SR-10 controlled Culiseta inornata for two weeks at 4 ounces per acre. With the exception of Dolichopodidae, most non-target aquatic organisms showed little response to Altosid SR-10. Although the developmental inhibitors Altosid and ZR-619 require higher concentrations for mosquito control, they inflict a minimum amount of damage to non-target aquatic organisms.

This paper presents information concerning the bionomics of Culex tarsalis Coquillett in Utah County. Observations indicate that rock piles and talus slides are typical hibernation sites. The spring emergence from hibernation occurred between 28 March and 7 April 1959. Larvae breed in a great variety of habitats, including street-gutters, animal tracks, marshes and waste water from irrigation systems. The peak population density for both larvae and adults occurred during the first week in August. Charts, graphs, drawings and photographs are used in the presentation of data.

Culex tarsalis Coquillett is a common evening pest mosquito throughout the summer in most of temperate Western North America. Present evidence indicates this mosquito as the principal naturally infected vector of western equine encephalomyeltic (WEE) viruses. Certain interrelationships of WEE epidemiology and tarsalis bionomics are basically understood; however, in areas where winters are severe little is know of tarsalis hibernation, and the survival mechanism for WEE viruses in unknown. The purpose of this study, conducted from 1 September 1959 to 20 May 1960, was to gather ecological information on the hibernation of Culex tarsalis in Utah Valley, and secondly to collect pools of hibernating tarsalis and determine the index of infection, in any by WEE viruses.

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International malaria control initiatives such as the Roll Back Malaria Initiative (RBM) and the Medicines for Malaria Venture (MMV) mobilize resources and spur research aimed at vector control as well as the treatment and eventual eradication of the disease. These efforts have managed to reduce incidence of malaria by an estimated 37% worldwide since 2000. However, despite the promising success of control efforts such as these, the World Health Organization reports a staggering 438,000 deaths from malaria in 2015. The continuing high death toll of malaria as well as emerging insecticide and antimalarial drug resistance suggests that while encouraging, success in reducing malaria incidence may be tenuous. Current vector control strategies are often complicated by ecological and behavioral heterogeneity of vector mosquito populations. As an additional obstruction, mosquito genomes are highly plastic as evidenced by the wealth or chromosomal inversions that have occurred in this genus. Chromosomal inversions have been correlated with differences in adaptation to aridity, insecticide resistance, and differences in resting behavior. However, a good understanding of the molecular mechanisms for inversion generation is still lacking. One possible contributor to inversion formation in Anopheles mosquitoes includes repetitive DNA such as transposable elements (TEs), tandem repeats (TRs) and inverted repeats (IRs). This dissertation provides physical maps for two important malaria vectors, An. stephensi and An. albimanus (Ch.2 and Ch. 3) and then applies those maps to the identification of inversion breakpoints in malaria mosquitoes. Repeat content of each chromosomal arm and the molecular characterization of lineage specific breakpoints is also investigated (Ch. 2 and Ch.4). Our study reveals differences in patterns of chromosomal evolution of Anopheles mosquitoes vs. Drosophila. First, mosquito chromosomes tend to shuffle as intact elements via whole arm translocations and do not under fissions or fusions as seen in fruitflies. Second, the mosquito sex chromosome is changing at a much higher rate relative to the autosomes in malaria mosquitoes than in fruit flies. Third, our molecular characterization of inversion breakpoints indicates that TEs and TRs may participate in inversion genesis in an arm specific manner. / Ph. D. / Malaria is a complex and devastating disease vectored by the bite of a female Anopheles mosquito. This disease claimed an estimated 438,000 lives in 2015. The mobilization of funding and resources as part of global malaria eradication initiatives have reduced the global incidence of malaria by 37% in the last 15 years. Deaths from malaria are also 60% lower vs. the year 2000. These promising gains are threatened by the ability of Anopheles mosquitoes to adapt in the face of malaria control efforts. Anopheles mosquito chromosomes are known to be highly plastic, as evidenced by numerous chromosomal inversions. Recent years have seen increases in insecticide resistance, and behavioral change in mosquito populations that allow them to avoid insecticides and remain prolific vectors of disease. This ability of mosquito vectors to adapt threatens to unravel recent progress towards a malaria free world. The projects presented in this dissertation explore mechanisms of chromosomal evolution, specifically the potential role of repetitive DNA in the generation of chromosomal inversions. The exploration of chromosomal inversions was facilitated by the creation of physical maps for Anopheles species. Prominent malaria vectors An. stephensi andAn. albimanus were physically mapped in Chapter 2 and Chapter 3 respectively. In chapter 1 and chapter 3 physical maps are utilized for the identification of chromosomal inversion breakpoints using 2 species (Ch. 2) and many species (Ch. 4). Repeat content was quantified along each chromosomal arm (Ch 2,4) and in inversion breakpoint regions (Ch 3). This dissertation presents physical maps for two important malaria species that have been applied to the study of chromosomal evolution and will also serve as community tools for further study of malaria mosquitoes. Our work on chromosomal evolution has revealed the Anopheles chromosomes tend to undergo translocations as intact elements and do not under fissions and fusions as seen in fruitflies. We also find that the malaria mosquito sex chromosome changes much more rapidly relative to the autosomes than in fruitflies. Additionally, repetitive DNA including transposable elements (TEs) and tandem repeats (TRs) may be encouraging chromosomal inversions but with differing roles on different chromosomal arms.

Mosquito phytophagy is a critical component of mosquito biology, contributing to their survival, flight activity and reproductive output and thus fueling their role as deadly vectors of disease. To alleviate the issues faced by current control methods, such as increased insecticide resistance and environmental damage, novel control strategies have emerged that exploit the mosquito's biological need to feed on sugar. However, an improved understanding of sugar feeding behavior is needed to better optimize these strategies. Here, we determined the prevalence of mosquito sugar feeding on ornamental plants and wildflowers by using DNA barcoding on mosquitoes captured in residential Blacksburg, VA, and identified their preferences for commonly planted flower species. Based on this information, we then confirmed the rate of sugar feeding on the attractive flower goldenrod (Solidago spp.) in the wild and explored its attractive qualities with the intent of developing a novel, ecologically friendly attractant. Similarly, we observed the sugar feeding behavior of invasive species Aedes japonicus on the toxic native flower fly poison and assessed its suitability as a naturally sourced attractant and toxin for use in attractive toxic sugar baits. Finally, we compared the morphology, metabolism and life history traits of mosquito species with unique host preferences. This work expands our knowledge on mosquito phytophagy and contributes to the development of new, highly needed control strategies. / Doctor of Philosophy / Mosquitoes are considered by many to be a blood-feeding nuisance and a vector of disease. While it is true that the females of several species need blood to develop their eggs and transmit disease-causing pathogens through blood feeding, mosquitoes need to frequently feed on plant-derived sugars to survive in the wild. In fact, male mosquitoes feed exclusively on sugar and both sexes use sugar as an energy source for flight. Because sugar feeding is such a critical component of mosquito biology, many novel disease vector control strategies have recently emerged that exploit this behavior, making it important to study. However, there is much that remains to be understood about their plant preferences and how they find these preferred plants in the wild. Here, we used new molecular techniques to determine what plant species mosquitoes commonly feed on in residential areas of Blacksburg, VA. We then explored the attractive qualities of goldenrod, a plant fed on frequently by mosquitoes in Montgomery County, VA. We also examined whether an invasive species, Aedes japonicus, can feed on the native toxic flower fly poison and analyzed the effect of sugar concentration on the metabolism, survival and egg-laying rate of two important invasive disease vectors: Aedes aegypti and Culex quinquefasciatus. The results found here improve our understanding of mosquito sugar feeding and have applications for the development of new disease control techniques.

Culex tarsalis is a major vector of West Nile Virus (WNV) in North America. Although the genome for this species was recently sequenced, the physical genome map has not developed. Unlike other Culex species, that have sex-determination locus on chromosome 1, the sex locus in Cx. tarsalis is located on chromosome 3, the longest chromosome. It is currently unknown if this difference is associated with chromosomal rearrangements. The objectives of this study were to develop a high-resolution map for the precise physical genome mapping in Cx. tarsalis and to compare mitotic chromosomes between three species of Culicinae mosquitoes. Using mitotic chromosomes from imaginal discs of 4th instar larvae of Cx. tarsalis, we developed idiograms based on morphology and proportions of the mitotic chromosomes. In addition, the physical mapping of ribosomal genes using fluorescence in situ hybridization was performed. The comparative analysis of Cx. tarsalis to Cx. pipiens and Cx. quinquefasciatus chromosomes showed that the total chromosome length in Cx. tarsalis is longer than the other two species suggesting the bigger genome size in this mosquito. A comparison of the relative chromosome length between the species indicated no significant differences suggesting that no large chromosomal translocation occurred between the species. Comparisons of the centromeric indexes demonstrated a significant difference in chromosome 1 between Cx. pipiens and Cx. quinquefasciatus. This difference suggests the presence of pericentric inversion between the species or amplification of ribosomal genes in Cx. pipiens. Studying mosquito chromosomes advances our understanding of Culex cytogenetics. Further comparative physical mapping of the three major mosquito genera will help us to understand the evolution of genus Culex better and to develop genome-based strategies for the vector control. / Master of Science in Life Sciences / West Nile Virus (WNV) is the most common virus transmitted to humans by mosquitoes in the United States. While many species of mosquitoes are known to carry WNV, Culex tarsalis is a major vector on the west coast of North America. However, previous research on Cx. tarsalis lack chromosome studies on this mosquito. Our study aims to develop a high-quality chromosome map for Cx. tarsalis and to compare the mitotic chromosomes of Cx. tarsalis and Cx. quinquefasciatus and Cx. pipiens in respect of chromosomal rearrangements. We used a fluorescent DNA probe to find the location of the ribosomal locus in the chromosomes of Cx. tarsalis. This study developed a cytogenetic tool for further genomic studies of Cx. tarsalis that will help to develop genome-based strategies for vector control. Comparing the physical mapping of the three major mosquito genera will help to understand the genome evolution in Culicinae mosquitoes better.