Research Interests
Research in Dr. Booth's lab is primarily focused on understanding how urbanization influences the evolution of urban pest insects. Our work scales from intra-individual populations of organelles to global populations of species, with particular focus on mitochondrial evolution, the genomics of invasion and establishment, and the evolution, distribution, and diversity of insecticide resistance. To do this, we take a molecular approach, from single genes to whole genomes, both nuclear and mitochondrial. Key themes of the lab are urban evolution, invasion genetics, and population genomics.
Insecticide resistance evolution
Urban pest insects exhibit multiple mechanisms that confer resistance to insecticides. These include but are not limited to target-site mutations (e.g., knockdown associated resistance [kdr], GABA-gated chloride channel, encoded by the RDL [resistance to dieldrin] gene), and metabolic resistance by increased activities of detoxification enzymes (e.g., Cytochrome P450 monooxygenases and esterase).
We are particularly interested in understanding the evolution of target-site mutation associated resistance at both the basic and applied levels. From the applied angle, understanding how mutation frequencies and distributions change over time may provide important insight for professional pest control personnel when selecting optimal management strategies. In contrast, from the basic viewpoint, understanding mutation frequencies and distribution gives us an opportunity to understand how the genomic mechanisms for resistance arose (i.e., standing variation vs. novel mutation), how urban living imparts selection pressures (here, the application of insecticides) that may change the frequencies of these mutations over time and space, the influence of demographic factors such as population size and levels of genetic diversity and gene flow, and fitness costs associated with such mutations.
(a) Genotype distribution of kdr-associated mutations from 394 unique infestations of Cimex lectularius sampled across the U.S. Pies represent genotype frequencies within each state and the number below each indicates the number of populations sampled. (b) Change in genotype frequencies over time of three homozygous genotypes—wild type, 925, 925 & 419. Colors correspond to genotypes in a. 2007–2008 data from Zhu et al. (2010), 2014–2015 from Holleman et al. (2019).
Relevant publications
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Lewis, C.D., Levine, B.A., Schal, C., Vargo, E.L. & Booth, W. (2023) Decade-long upsurge in mutations associated with pyrethroid resistance in bed bug populations in the United States. Journal of Pest Science. 96, 415-423.
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Balvin, O., Sasínková, M., Martinů, J., Nazarizadeh, M., Bubová, T., & Booth, W., Vargo, E.L. & Štefka, J. (2021) Early evidence of establishment of the tropical bedbug (Cimex hemipterus) in Central Europe. Medical and Veterinary Entomology. 35, 462-467.
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Gaire, S., Lewis, C.D., Booth, W., Scharf, M.E., Zheng, W., Ginzel, M.D. & Gondhalekar, A.D. (2020) Bed bugs, Cimex lectularius L., exhibiting metabolic and target site deltamethrin resistance are susceptible to plant essential oils. Pesticide Biochemistry and Physiology. 169, 104667
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Lewis, C.D., Levine, B.A., Vargo, E.L., Schal, C. & Booth, W. (2020) Recent detection of multiple populations of the Tropical bed bug, (Hemiptera: Cimicidae) exhibiting kdr-associated mutations in Hawaii. Journal of Medical Entomology. 57, 1077-1081.
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Holleman, J.G., Robison, G.A., Belovich, I.J. & Booth, W. (2019) Knockdown resistance-associated mutations dominate populations of the bed bug (Hemiptera: Cimicidae) across the south central United States. Journal of Medical Entomology. 56, 1678-1683.
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Balvin, O. & Booth, W. (2018) Distribution and frequency of pyrethroid resistance-associated mutations in host lineages of the bed bug, (Hemiptera: Cimicidae) across Europe. Journal of Medical Entomology. 55, 923-928.
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Runjaic, J., Bellovich, I., Page, C.E., Brown, C.R. & Booth, W. (2017) No detectable insecticide resistance in swallow bugs (Hemiptera: Cimicidae) following long-term exposure to naked (Dibrom 8). Journal of Medical Entomology. 54, 994-998.
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Booth, W., Balvin, O., Vargo, E.L., Vilimova, J. & Schal. C. (2015) Host association drives genetic divergence in the bed bug, Cimex lectularius. Molecular Ecology. 24, 980-992.
Population and Invasion Genomics
Understanding how pest insects invade, establish, and spread is critical for the development of effective management strategies. Urban pest insects represent particularly interesting model systems given that dispersal mechanisms may be complex, involving both passive human-mediated and active modes, dispersal may be local or international, changing global conditions may result in temporally complex patterns, and socio-economic factors may represent result in locally complex and contrasting levels of genetic diversity and gene flow.
We use a variety of genomic methods to investigate the population genetics and invasion genomics of urban pest insects. These methods range from single mitochondrial genes to whole mitogenomes, and from nuclear microsatellite loci to whole nuclear genomes. We are primarily interested in human-associated cimicid insects, namely the common bed bug, Cimex lectularius, and the tropical bed bug, Cimex hemitperus, and both domestic and potentially peridomestic cockroaches, particularly the German cockroach, Blattella germanica, and the Asian cockroach, Blattella asahinai.
Relevant publications
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Balvin, O., Sasínková, M., Martinů, J., Nazarizadeh, M., Bubová, T., & Booth, W., Vargo, E.L. & Štefka, J. (2021) Early evidence of establishment of the tropical bedbug (Cimex hemipterus) in Central Europe. Medical and Veterinary Entomology. 35, 462-467.
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Lewis, C.D., Levine, B.A., Vargo, E.L., Schal, C. & Booth, W. (2020) Recent detection of multiple populations of the Tropical bed bug, (Hemiptera: Cimicidae) exhibiting kdr-associated mutations in Hawaii. Journal of Medical Entomology. 57, 1077-1081.
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Booth, W., Schal, C. & Vargo, E.L. (2018) Population Genetics of Bed Bugs. In: Advances in the Biology and Management of Modern Bed Bugs (Eds. S.L. Doggett, D.M. Miller. & C-Y Lee). John Wiley & Sons. Inc. New Jersey, U.S.A.
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Booth, W., Balvin, O., Vargo, E.L., Vilimova, J. & Schal. C. (2015) Host association drives genetic divergence in the bed bug, Cimex lectularius. Molecular Ecology. 24, 980-992.
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Vargo, E.L., Crissman, J.R., Booth, W., Santangelo, R.G., Mukha, D.V., Schal, C. (2014) Hierarchical genetic analysis of German cockroach (Blattella germanica) populations from within buildings to across continents. PLoS ONE. 9(7): e102321
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Saenz, V., Booth, W., Schal, C. and Vargo, E.L. (2012) Genetic analysis of bed bug (Cimex lectularius) populations reveals small propagule size within individual infestations but high genetic diversity across infestations from the eastern U.S. Journal of Medical Entomology. 49, 865-875.
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Booth, W., Saenz, V.L1., Santangelo, R.G., Schal, C. & Vargo, E.L. (2012) Molecular markers reveal infestation dynamics of the bed bug, Cimex lectularius, within apartment buildings. Journal of Medical Entomology. 49, 535-546.
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Booth, W., Brent, C.S., Calleri, D.V., Rosengaus, R.B., Traniello, J.F.A. & Vargo, E.L. (2012) Population genetic structure and colony breeding system in dampwood termites (Zootermopsis angusticollis and Z. nevadensis nuttungi). Insectes Sociaux. 59, 127-137.
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Booth, W., Santangelo, R.G., Vargo, E.L., Mukha, D.V. & Schal, C. (2011) Population genetic structure in German cockroaches (Blattella germanica): Differentiated islands in an agricultural landscape. Journal of Heredity. 102, 175-183.
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Crissman, J., Booth, W., Santangelo, R.G., Mukha, C., Vargo, E.L. & Schal, C. (2010) Population genetic structure of the German cockroach (Blattella germanica) within and among apartments. Journal of Medical Entomology. 47, 553-564.
Genome Evolution
We are interested in the organization and evolution of both mitochondrial and nuclear genomes.
Our specific interest in mitochondrial genome evolution lies in heteroplasmy and recombination. Our recent work has shown that common bed bugs exhibit high levels of heteroplasmy, while our laboratory crosses have provided evidence that this is the result of paternal leakage and that recombination may occur. We are currently sequencing mitogenomes from across hundreds of populations in order to understand recombination hotspots, and are generating line-specific crosses in order to investigate the genomic drivers of heteroplasmy and recombination.
Our interest in nuclear genome evolution is focused towards understanding patterns of selection and the impact of inbreeding. To do this, we have generated a new, haplotype-resolved chromosome level genome for an insecticide-susceptible common bed bug, Cimex lectularius. Genomes for bat associated C. lectularius, along with various insecticide-resistant strains will follow. Additionally, we are working towards draft genomes for the tropical bed bug, C. hemipterus, and the swallow bug, C. vicarious.
Relevant publications
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Kolokotronis, S-O., Foos, J., Rosenfeld, J., Brugler, M., Reeves, D., Benoit, J., Booth, W., Robison, G.A., Steffen, M., Palli, S., Schal, C., Richards, S., Narechania, A., Baker, R., Sorkin, L., Amato, G., Mason, CE., Sidall, ME. & DeSalle, R. The mitogenome of the bed bug Cimex lectularius (Hemiptera: Cimicidae). Mitochondrial DNA Part B: Resources. 1, 425-427.
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Benoit, J., ….…Booth, W. et al. (total 82 authors). Unique features of a global human ectoparasiteidentified through sequencing of the bed bug genome. Nature Communication. 6, 10165.
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Robison, G.A., Balvin, O., Schal, C., Vargo, E.L. & Booth, W. Extensive mitochondrial heteroplasmy in natural populations of a resurging human pest, the bed bug (Hemiptera: Cimicidae). Journal of Medical Entomology. 52, 734-738.
Funding Agencies
Our research has been supported from funding awarded from the following private, state, and federal agencies.