Patterns and Mechanisms of the Geographic Expansion of Aedes aegypti in the Peruvian Amazon Open Access

Guagliardo, Sarah Anne Jablonski (2015)

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Transmitted to humans through the bites of infected Aedes mosquitoes, dengue is the world's most important arbovirus, with nearly 2.5 billion people at risk for disease. Although present in the Americas for centuries, the primary dengue vector Aedes aegypti is expanding from urban to peri-urban and rural areas throughout Latin America after its near continental elimination in the 1950's. In the Peruvian Amazon, Ae. aegypti is abundant in urban centers such as Iquitos (pop: ~400,000), and in recent years, has also been found in a number of neighboring communities. Ae. aegypti active dispersal (through flight) is limited to <100m, and therefore long-distance dispersal must be facilitated through human activity. In this dissertation I: 1) assess risk factors for Ae. aegypti invasion through entomological surveys in 34 communities; 2) clarify the relative importance of different vehicles (i.e.- boats, trucks) in the invasion process; and link vehicle infestation with transportation data to measure the frequency and intensity of new introductions ("propagule pressure"); 3) measure oviposition frequency on river boats; and 4) characterize gene flowusing 10 microsatellite markers and linked such data to long-distance dispersal mechanisms. Taken together, evidence from this dissertation highlights the importance of river boats as major drivers of Ae. aegypti regional expansion. My main findings are: 1) risk for invasion is a function of connectivity and proximity to major urban centers; 2) several vehicle types are responsible for transporting immature and adult mosquitoes (mostly barges); 3) few individual barges produce the majority of mosquitoes, acting as "super-transporters." These results have important implications for dengue control: many novel control strategies (i.e.- genetically modified "sterile" mosquitoes) falsely assume that mosquito populations are immobile, whereas my results show continual gene flow among Ae. aegypti metapopulations. From an invasion ecology perspective, I show that propagule pressure can be more precisely quantified through field surveys. I also propose a new method for evaluating genetic isolation by distance through the "Propagule Pressure Index," combining transportation data with vehicle infestation rates. Broadly, results from this study can help anticipate vector population mixing and future range expansions of dengue and other viruses transmitted by Ae. aegypti.

Table of Contents

Chapter 1: Introduction. 1

1.1 Emerging and Re-emerging Infectious Diseases. 1

1.2 Dengue Fever Biology, Ecology, and Epidemiology. 2

1.3 Aedes aegypti Biology, Ecology, and Global Expansion. 5

1.4 Theoretical Foundations of Invasion Ecology. 7

1.5 Dissertation Objectives. 8

1.6 Study Area. 11

1.7 Figures. 12

Figure 1.1. Steps in the invasion process. 12

1.8 References Cited. 13

Chapter 2: Patterns of Geographic Expansion of Aedes aegypti in the Peruvian Amazon. 21

2.1 Introduction. 21

2.2 Methods. 24

2.3 Results. 33

2.4 Discussion. 37

2.5 Tables. 42

Table 2.1. Entomological Indices for communities positive for Ae. aegypti (collected data only) 42

Table 2.2. Multivariable logistic regressions: Ae. aegypti risk factors at the community scale 45

Table 2.3. Multivariable logistic regressions: Ae. aegypti risk factors at the house scale. 46

Table 2.4. Proportion of positive containers by type. 47

Table 2.5. Multivariable logistic regressions: Ae. aegypti risk factors at the container scale 48

2.6 Figures. 49

Figure 2.1. Map of study area. 49

Figure 2.2. Ae. aegypti presence-absence by data source. 50

Figure 2.3. Mann-Whitney Wilcoxon tests for median differences in Ae. aegypti positive vs. negative communities. 51

Figure 2.4. Laval and pupal productivity by container type. 52

Figure 2.5. Geographic border of Ae. aegypti colonization along the Iquitos-Nauta highway 53

2.7 Supplementary Tables. 54

Table S2.1. Characteristics of communities included in the study. 54

Table S2.2. Datasets, ecological scales, and statistical analyses employed. 58

Table S2.3. Community-level univariable logistic regression models. 59

Table S2.4. House-level univariable logistic regression models. 60

Table S2.5. Container-level univariable logistic regression models. 61

Table S2.6. Container-level univariable logistic regression models demonstrating multicollinearity among all possible combinations of predictor variables. 62

2.8 Supplementary Figures. 64

Figure S2.1. River/ stream water vs. other water types by population and distance from Iquitos 64

2.9 References Cited. 65

Chapter 3: River Boats Contribute to the Regional Spread of Dengue Vector Aedes aegypti in the Peruvian Amazon. 74

3.1 Introduction. 74

3.2 Methods. 77

3.3 Results. 82

3.5 Tables. 92

Table 3.1. Most commonly found adult mosquitoes found on large and medium barges and buses 92

Table 3.2. Ae. aegypti adult mosquitoes on large and medium barges. 93

Table 3.3. Immature indices by month for large and medium barges. 95

Table 3.4. Proportion of positive containers by type - large barges. 97

3.6 Figures. 98

Figure 3.1. Vehicle types surveyed. 98

Figure 3.2. Common transportation routes in the Iquitos region. 99

Figure 3.3. Proportion of vehicles infested with Ae. aegypti mosquitoes. 100

Figure 3.4. Ae. aegypti adults and immatures per boat by location for all periods - large barges 101

Figure 3.5. Formation of puddles in cargo holds. 102

3.7 Supplementary Tables. 103

Table S3.1. Adult mosquitoes found on large barges by season. 103

Table S3.2. Adult mosquitoes found on medium barges by season. 105

Table S3.3. Adult mosquitoes found on buses by season. 107

Table S3.4. Adult mosquitoes found on speed boats by season. 108

Table S3.5. Adult mosquitoes found on water taxis by season. 109

3.8 Supplementary Figures. 110

Figure S3.1. NOAA precipitation and rainfall data for Iquitos. 110

3.9 References Cited. 111

Chapter 4: Evidence for Aedes aegypti Oviposition on Boats in the Peruvian Amazon. 116

4.1 Introduction. 116

4.2 Materials and Methods. 118

4.3 Results. 120

4.4 Discussion. 121

4.5 Tables. 123

Table 4.1. Proportion of positive boats by date. 123

Table 4.2. Number of Ae. aegypti eggs and larvae per trap by month. 124

4.6 References Cited. 125

Chapter 5: River Boats Drive Aedes aegypti Gene Flow in the Peruvian Amazon.. 128

5.2 Methods. 130

5.3 Results. 134

5.4 Discussion. 135

5.5 Tables. 139

Table 5.1. Characteristics of Study Sites. 139

Table 5.2. Summary of variation at 10 microsatellite loci by sampling location. 140

Table 5.3. Pairwise FST Table. 142

5.6. Figures. 144

Figure 5.1. Map of study collection sites. 144

Figure 5.2. Geographic distance models. 145

Figure 5.3. Isolation by distance models for three measures of geographic distance and for one measure of network distance. 146

Figure 5.4. Structure Diagrams. 147

Figure 5.5. Structure results superimposed on maps. 148

5.7 References Cited. 149

Chapter 6: Conclusion. 157

6.1 Summary. 157

6.2 Further Research. 160

6.3 Theoretical Contributions to Invasion Ecology. 162

6.3 Figures. 164

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