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Under the Direction of Drs. Michael Reiskind and Robert Dunn) ABSTRACT SPENCE BEAULIEU, MEREDITH RUTH. The Ecology of Dog Heartworm Disease. (Under the direction of Drs. Michael Reiskind and Robert Dunn). Suburban development is rapidly transforming the global landscape. This anthropogenically induced land-use change affects the species around us, including mosquitoes and the pathogens that they transmit. Although the effect of urbanization has been extensively studied for key mosquito species of interest, relatively little research has addressed the effect of urbanization on mosquito species assemblages as a whole. Knowledge of the effects of urbanization on entire mosquito communities is critical, as many vector-borne diseases are transmitted by an assembly of vectors and therefore could be sensitive to community-level alterations after land-use change. Additionally, the effects of vector diversity on the transmission of multi-vectored pathogens has scarcely been explored either empirically or theoretically. In this dissertation, I investigate the effects of suburban development on mosquito assemblages and the subsequent consequences for vector-borne disease transmission using the dog heartworm, Dirofilaria immitis, as a model system. In the first experiment, I used a field study to determine the effects of suburbanization on mosquito diversity and community composition. I found that species diversity declined with neighborhood age, with the oldest suburban areas having species assemblages that are characteristically less diverse than those of undeveloped areas. The community composition differed between habitat types, with the suburban mosquito assemblage being dominated by the invasive Aedes albopictus, the Asian tiger mosquito. In the second experiment, I performed an epidemiological study comparing the within-mosquito heartworm and within-host heartworm prevalence by land-use type. I found that suburban areas had lower levels of heartworm within both the host and the vector than did the undeveloped field sites, with undeveloped wooded sites showing an intermediate pathogen presence. Since the suburban areas were overwhelmingly dominated by Ae. albopictus and had significantly lower heartworm prevalence, I then investigated the vector competence of the local population of Ae. albopictus with the hypothesis that it was a poor vector locally. In the third study, I performed a laboratory experiment testing the D. immitis developmental times, mosquito longevity and fecundity, and the vector efficiency index for Ae. albopictus and a suspected highly competent local vector, Aedes triseriatus. I found that Ae. albopictus is indeed a poor vector of heartworm in Wake County, as evidenced by significant infection-induced mortality and a vector efficiency index more than 4x lower than that of Ae. triseriatus. In the fourth study, I created a single host and multi-vector SIR-type mathematical model of dog heartworm disease. Utilizing the laboratory generated parameters for Ae. albopictus and Ae. triseriatus as well as the field data on the diversity and community composition of suburban and undeveloped areas in Wake County, I compared the model’s basic reproduction number, !", for these empirically driven scenarios. Using the critical value of !" > 1 as a threshold, I validated that Ae. triseriatus is a competent vector of D. immitis, while Ae. albopictus is insufficient to support disease transmission as the sole vector in a natural setting. I also demonstrated that the suburban mosquito assemblage had a notably lower !" than the natural area assemblage, supporting my previous observations on heartworm prevalence by habitat type. To test theoretical predictions about the effect of vector diversity on disease transmission, I then simulated many iterations of models with one, three, five, and ten vector species. While changes in diversity did not significantly affect the average !", variation in !" values decreased as the number of vectors increased. This demonstrates the stabilizing effect of vector diversity for multi-vectored pathogens while also highlighting the importance of species identity and community composition for determining the magnitude of disease transmission. In a final brief chapter, I consider the parasite manipulation hypothesis and its potential implications for vector- borne diseases. © Copyright 2019 by Meredith Ruth Spence Beaulieu All Rights Reserved The Ecology of Dog Heartworm Disease by Meredith Ruth Spence Beaulieu A dissertation submitted to the Graduate Faculty of North Carolina State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Entomology Raleigh, North Carolina 2019 APPROVED BY: _______________________________ _______________________________ Dr. Michael Reiskind Dr. Robert Dunn Committee Co-Chair Committee Co-Chair _______________________________ _______________________________ Dr. David Watson Dr. Cristina Lanzas _______________________________ Dr. Kevin Gross ii BIOGRAPHY A North Carolina native, Meredith was born and raised in Elizabeth City. She attended NC State as an undergraduate, where she was first exposed to the insect world as an undergraduate research assistant investigating ant-mediated seed dispersal. She graduated valedictorian and summa cum laude, receiving a BS in Zoology with a minor in Mathematics in 2011. She worked as a veterinary technician for three years before deciding to combine her passions for veterinary medicine, mathematics, and entomology by pursuing a PhD in Entomology at NC State. Her PhD research focuses on how human-driven land-use change affects mosquito assemblages, and how that in turn affects pathogen transmission utilizing dog heartworm disease as a model system. She was awarded a National Science Foundation Graduate Research Fellowship in 2016 to support her PhD research. She is interested broadly in vector- borne disease ecology, public health, and science policy. Outside of research, she enjoys drinking inordinate amounts of coffee and cuddling her horde of furry children: Wren the lab- poodle-shar pei mix, Logan and Cora the boxers, Grim the cat, and Ratticus Finch and Ratt Skiba the dumbo fancy rats. iii ACKNOWLEDGMENTS First and foremost I would like to thank my advisors, Michael Reiskind and Rob Dunn, for their guidance, support, and encouragement. I was incredibly lucky to have people that so deeply love science as mentors and sources of inspiration. I am indebted to the entirety of my committee, including Michael, Rob, Wes Watson, Cristina Lanzas, and Kevin Gross, for their feedback on my ideas and work. Your insights greatly improved my learning and my research. All of the Reiskind lab members have graciously shared their expertise, time, and advice, but none more so than Kristen Hopperstad. Special thanks also to Paul Labadie for assisting with my molecular work and troubleshooting when things inevitably went wrong, and to Shawn Janairo for being an encyclopedia of mosquito and heartworm rearing knowledge. My research was funded by the National Science Foundation Graduate Research Fellowship Program under Grant No. DGE-1746939 and NC State’s Department of Entomology and Plant Pathology. I would also like to acknowledge the financial support that I received from the American Mosquito Control Association, the Society for Vector Ecology, the Entomological Society of America, Central Life Sciences, Bayer, the Mid-Atlantic Mosquito Control Association, and the North Carolina Mosquito and Vector Control Association for travel to various conferences to communicate my work and enhance my professional development. I had the privilege of working with many fantastic people through a variety of extracurricular activities, including Linnaean Games, the Entomology Graduate Student Association, the university-level Graduate Student Association, and Student Government. Thank you for inspiring me to be a better team member and leader, and for helping me to leave a small mark on NC State. This also seems an appropriate place to acknowledge Michael Reiskind again, for not panicking (too much) when I insisted on being so involved in so many things. I am grateful for your flexibility and trust while I pursued my non-research passions. To the many wonderful friends that have stood by me on this journey and that I’ve met in the process: thank you, thank you, thank you. For the trivia nights, for the dancing, for the gin and tequila drinking, for the long distance phone calls, for everything. You have brought joy and reminded me that I’m still a person outside of my research when I needed reminding. My most heartfelt gratitude to my parents, John and Debbie Spence, and my sister, Leah Creed, for their constant encouragement. Finally, a million thank yous to my patient and supportive husband, Matt Beaulieu. All my love, for now, forever, for on and on and on. iv TABLE OF CONTENTS LIST OF TABLES ................................................................................................................... vi LIST OF FIGURES ................................................................................................................ vii Chapter 1: Introduction ......................................................................................................... 1 References ................................................................................................................................ 4 Chapter 2: Simplification of Vector Communities During Suburban Succession................ 6 Abstract ...................................................................................................................................
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