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Understanding the Mechanisms of Insecticide Resistance in Phlebotomus Papatasi and Lutzoymia Longipalpis Sand Flies (Diptera: Psychodidae: Phlebotominae)

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Understanding the Mechanisms of Insecticide Resistance in Phlebotomus Papatasi and Lutzoymia Longipalpis Sand Flies (Diptera: Psychodidae: Phlebotominae) Utah State University DigitalCommons@USU All Graduate Theses and Dissertations Graduate Studies 5-2017 Understanding the Mechanisms of Insecticide Resistance in Phlebotomus papatasi and Lutzoymia longipalpis Sand Flies (Diptera: Psychodidae: Phlebotominae) David Denlinger Utah State University Follow this and additional works at: https://digitalcommons.usu.edu/etd Part of the Biotechnology Commons, and the Plant Sciences Commons Recommended Citation Denlinger, David, "Understanding the Mechanisms of Insecticide Resistance in Phlebotomus papatasi and Lutzoymia longipalpis Sand Flies (Diptera: Psychodidae: Phlebotominae)" (2017). All Graduate Theses and Dissertations. 5730. https://digitalcommons.usu.edu/etd/5730 This Dissertation is brought to you for free and open access by the Graduate Studies at DigitalCommons@USU. It has been accepted for inclusion in All Graduate Theses and Dissertations by an authorized administrator of DigitalCommons@USU. For more information, please contact [email protected]. UNDERSTANDING THE MECHANISMS OF INSECTICIDE RESISTANCE IN PHLEBOTOMUS PAPATASI AND LUTZOMYIA LONGIPALPIS SAND FLIES (DIPTERA: PSYCHODIDAE: PHLEBOTOMINAE) by David S. Denlinger A dissertation submitted in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY in Biology Approved: _________________________ _________________________ Scott A. Bernhardt, Ph.D. Carol D. von Dohlen, Ph.D. Major Professor Committee Member _________________________ _________________________ Lee F. Rickords, Ph.D. Zachariah Gompert, Ph.D. Committee Member Committee Member _________________________ _________________________ Diane G. Alston , Ph.D. Mark R. McLellan, Ph.D. Committee Member Vice President for Research and Dean of the School of Graduate Studies UTAH STATE UNIVERSITY Logan, Utah 2017 ii Copyright © David S. Denlinger 2017 All Rights Reserved iii ABSTRACT Understanding the Mechanisms of Insecticide Resistance in Phlebotomus papatasi and Lutzoymia longipalpis Sand Flies (Diptera: Psychodidae: Phlebotominae) by David S. Denlinger, Doctor of Philosophy Utah State University, 2017 Major Professor: Dr. Scott A. Bernhardt Department: Biology The prevalence of insecticide resistance in vector species around the world is a continuous threat for any success at mitigating the spread of vector-borne diseases. With a limited arsenal of new insecticides, it is crucial for public health programs to understand the geographic range and the genetic mechanisms of resistance to best approach controlling insect vectors. Insecticide resistance is being increasingly observed in phlebotomine sand fly (Diptera: Psychodidae) populations in both the Old World and New World. Sand flies transmit the protozoans that cause leishmaniasis, a disfiguring disease that kills tens of thousands of people each year. The goal of this dissertation was to have both an applied and basic research focus towards understanding resistance in phlebotomines. I began by comparing in vivo and in vitro methods for blood-feeding two species of sand flies, Phlebotomus papatasi and Lutzomyia longipalpis, in the laboratory, both of which are important leishmaniasis vectors. I investigated the susceptibility of both species to ten different insecticides by calculating lethal concentrations that caused varying levels of mortality. Based on these results, I determined diagnostic doses and diagnostic times for both species to the same ten insecticides using an accepted, but novel, assay for sand flies. Finally, I tested for known mechanisms of insecticide resistance in four artificially iv resistant-selected colonies of sand flies, as well as tested for novel resistance mechanisms. Through applied research, I developed methods for efficient sand fly rearing and for determination of population resistance to insecticides, tools that have worldwide applicability. Through basic research, I determined that laboratory populations of sand flies have sufficient standing genetic variation needed to survive sublethal doses of insecticides; however, I was unable to develop artificially-selected colonies resistant to these insecticides. My research has generated information to provide new insights into the evolution of insecticide resistance in natural sand fly populations. My results support that resistance development may be possible, but evolutionary challenging, an encouraging finding that may be exploited by vector biologists and public health officials to prevent or slow the development of resistance in sand flies to insecticides (257 pages) v PUBLIC ABSTRACT Understanding the Mechanisms of Insecticide Resistance in Phlebotomus papatasi and Lutzoymia longipalpis Sand Flies (Diptera: Psychodidae: Phlebotominae) David S. Denlinger Sand flies, like mosquitoes, ticks, fleas, and lice, transmit pathogens that cause disease in humans. Leishmaniasis, caused by pathogens transmitted by sand flies, kills tens of thousands of people every year. Insecticides have been used to control sand flies, but there is evidence of insecticide resistance in populations of sand flies around the world. The goal of this dissertation was to develop tools to maintain sand flies in the laboratory, develop the ability to identify insecticide-resistant populations of sand flies, and to investigate the genetic mechanisms of how sand flies become resistant to insecticides. I began by comparing live animal and artificial techniques for blood-feeding two species of sand flies, Phlebotomus papatasi and Lutzomyia longipalpis, in the laboratory, both of which are important leishmaniasis vectors. Next, I investigated how susceptible laboratory colonies of both species are to ten insecticides that are used worldwide to control sand flies. Based on my results, I determined diagnostic concentrations and diagnostic exposure times for the laboratory colonies to the ten insecticides using a known assay that has been used very little for sand flies, which allows researchers to determine if a population of sand flies is resistant to an insecticide. Finally, I tested for known mechanisms of insecticide resistance in four artificially resistant-selected colonies of sand flies, and I also looked for novel mechanisms. This dissertation is useful in that it provides researchers practical approaches to maintain sand flies to be used for further research and to determine resistance in the field. It also demonstrates that sand fly populations are homogenous, and it implies that it is challenging for a population to become resistant to insecticides. This aspect can vi be exploited by sand fly researchers and public health officials in effectively controlling sand fly populations, which is also beneficial for slowing the transmission of leishmaniasis. vii ACKNOWLEDGMENTS This dissertation is dedicated to my grandfathers, Herb Denlinger and Ralph Mease, two military men who served honorably in Korea and World War II. Fair winds and following seas... “It seemed as though all the insect life of the entire region had congregated here in anticipation of a glorious picnic...Ants built catacombs beneath our couches, land crabs burrowed up through the fungus-grown floor to inspect our resting places, woodticks climbed the tent-walls, whence they could select the most favorable lodging place, flies covered our food as with sackcloth and endeavored to rob us even of its scantiness, mosquitoes of unrivaled force and ferocity plied their lancets with merciless vigor, and, when their appetite were appeased, rested on the ridgepole and mockingly barked at their victim until he went to sleep, great hairy spiders built nests in the peak, strange things whizzed and buzzed and boomed through the darkness, cannon dropping on our faces with a sharp thud as if shot or alighting with sticky feet reluctant of dislodgement. All night viii long there was a rustling and a crackling of well-nigh every type of winged and creeping abomination that earth produces.” (Armed Forces Pest Management Board, Evolution of Military Medical Entomology, 2008) -To all the 72Bs, 43MXs, and 230X-1850s who, unknown to most and often unceremoniously, have, are, and will continue to honorably fight six-legged enemies in order to protect those who fight against our two-legged enemies- I think that there is no fundamentally more collaborative effort in an individual’s academic career than the pursuit of a graduate degree. I certainly would not have reached the end of my degree without the guidance, support, patience, and camaraderie of so many here at Utah State. First, a gracious thank you to Scott Bernhardt, who took a chance on me as his first graduate student: It has been a heck of a ride together. Thank you for teaching and leading me in the right directions over these past five-and-a-half years to become my own researcher; for letting me struggle, fail, and succeed; for the great conversations; for the support in all facets of graduate school; and most importantly, for the meals that sustained me. To my committee who provided insights, ideas, and ways of thinking that helped broaden this dissertation. To the USU Department of Biology staff who have been more than patient with me as I reached and overused my allotted time quotas (speaking to you Kami!). To my USU Biology graduate student family, past and present, who has been some of my greatest friends during my time in Utah- for the shared conversations over beers, movie nights, camping/collecting trips, conference trips, badminton, SLURM sessions, for being an honorary herp lab member, for being an honorary bee lab member,
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