Source: PENNSYLVANIA STATE UNIVERSITY submitted to
INTERACTIONS BETWEEN INSECTS AND PATHOGENS/PARASITES
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
REVISED
Funding Source
Reporting Frequency
Annual
Accession No.
1010032
Grant No.
(N/A)
Project No.
PEN04608
Proposal No.
(N/A)
Multistate No.
(N/A)
Program Code
(N/A)
Project Start Date
Jul 1, 2016
Project End Date
Jun 30, 2021
Grant Year
(N/A)
Project Director
Hughes, DA.
Recipient Organization
PENNSYLVANIA STATE UNIVERSITY
208 MUELLER LABORATORY
UNIVERSITY PARK,PA 16802
Performing Department
Entomology
Non Technical Summary
The justification for this work is to better understand insect and their pathogens and pests in an integrated manner to increase our ability to reduce the negative effect of insects as disease vectors in human and agricultural settings, as well as gain general insights into evolutionary processes.
Animal Health Component
0%
Research Effort Categories
Basic
45%
Applied
45%
Developmental
10%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
72231101130100%
Goals / Objectives
This project builds upon previous work on insects and pathogens in disease control but in the current work we expand this to consider a broader evolutionary approach in addition to the applied aspect. This integration will, we think, increase the effectiveness with which we can tailor control strategies as well as more fully understand the reasons why some insects becomes pests. In addition the work represents an effective integration of applied and fundamental work that we think will lead to serendipitous discoveries that will lead to synergisms, better control of pests and a better understanding of the co-evolutionary dynamics between insects and the pathogens/pests that exploit themThe objectives are:1) Understand the ecology and evolution of pestiferous insect and mite pests of humans and domestic animals. (Thomas, Read, Bjornstad, Machtinger, McGraw, Hughes)2) Understand the pathogens and parasites of insects and how a close study of their ecology and evolution helps us reduce the negative impact of insect/mite pests. (Hughes, Thomas, Read, McGraw, Bjornstad)3) Integrate across technologies from field studies to mathematical modelling to advanced molecular techniques like CRISPR CAS-9. (Cui, Rasgon, Bjornstad, Read)4) Use the science created to inform public policy and decision making processes at local, regional, national and international levels. (Machtinger)
Project Methods
We combine behavioral methods with molecular techniques, modeling, ecological experiments and social studies as we measure human behavior. The Hughes lab is focused on the ecology and evolution of diseases in ant societies. Ants and other social insects are highly damaging pest in agricultural and urban settings. We work on developing databases of ants pests and modelling the effect of disease on colony growth and at the individual level determining the virulence of fungal pathogens on ant behavior. We use behavioral studies in the lab and field following natural and artificial infections. Our behavioral work involves the use of Go-pro cameras with modified lenses that allow night recording and with nest recording. We employ human/machine learning tools for tracking individual ants. We analyze our work using a range of standard statistical test appropriate to the data type. Much of our work develops and deploys continuous time movement models in spatial statistics. Our epidemiological modelling work uses standard Susceptible-Infected models where colony growth is studied under a perturbation such as worker loss due to infection. We complement this work with mesocosm studies of ant foraging behavior to parametrize exposure to pathogens and effect on colony demographics. The Cui lab uses the CRISPR/cas9 technology to study the drug resistance in the malaria parasite Plasmodium falciparum. Drug resistance in malaria parasites is hindering malaria control and elimination. Recently, the parasites have developed resistance to the frontline treatment artemisinin, however, the resistance mechanism is poorly understood. One of the genes associated with artemisinin resistance is the kelch domain protein K13. Our current work focuses on the deciphering the significance of the mutations we identified in Southeast Asian parasites in mediating artemisinin resistance through genetic manipulation of the parasites using the CRISPR/cas9 technology.The Bjornstad lab uses mathematical and computational model to study the spatiotemporal dynamics of insect pests of importance to human health and agroecosystems. The goal is to improve models to forecast outbreaks; use models to better mitigate health and economic burdens of pestiferous insects; and understand how fundamental aspects of insect life histories shape outbreak dynamics. Numerous mathematical and statistical methods are in use including: Geostatistics, differential equations, coupled-map lattice models, individual based simulations and distributed delay models. Research in the Thomas lab explores many aspects of the ecology and evolution of insect pests and diseases with the aim of better understanding the consequences of global change and improving the effectiveness and sustainability of pest and disease management. The research spans many systems across diverse topics including host-pathogen interactions, predicting and understanding the impact of invasive species, biodiversity and ecosystem health, and many aspects of biological control. Current projects include research on the effects of environmental temperature on transmission of vector-borne diseases, understanding the consequences of insecticide resistance for malaria control, and developing and evaluating novel control tools for the development of improved integrated vector management. Methods range from highly controlled lab studies using incubators to examine how abiotic and biotic factors affect key life history traits of mosquitoes and parasites to determine transmission potential, through to large scale cluster randomized trials in Africa to evaluate impact of novel control tools on malaria transmission in the field. The approaches tend to focus on demographic and population level traits, but we do employ molecular tools as appropriate to help elucidate mechanisms, such as innate immune function and insecticide resistance. Finally, much of the work is informed by use of computer-based models of disease transmission to explore broader implications of our empirical findings. The Read lab studies the ecological and evolutionary determinants of resistance in mosquito populations to insecticides and of resistance in the malaria parasites they transmit. We are investigating mosquito life histories and in particular how the age specific mortality and reproductive schedules of female Anophelines impacts rates of spread of alleles conferring resistance to insecticides and how alleles conferring resistance to new technologies such as selfish genetic elements might also spread. A substantial interest is the role of environment drivers in altering rates of evolution. Drug resistance work focuses on competition between sensitive and resistant parasites in vertebrate and mosquito hosts and is aimed at identifying treatment strategies and drug combinations which might retard resistance evolution. We recently discovered that resource limitation can intensify competition between resistant and sensitive parasites and so prevent the emergence of resistance. We use an iterative combination of mathematical models and experimental work to make progress.The Rasgon lab is developing novel targeted tissue-specific delivery methods to deliver Cas9 ribonuceloprotein complex and other gene editing factors to specific insect tissues, including the germline. Using these new technologies, genetic modification of arthropods and non-model species can be easily and cheaply accomplished with a minimum of training. This technology is patent pending and is currently being commercialized.The McGraw lab studies the relationship between mosquito vectors and the viruses they transmit, including dengue and Zika. In particular we are determining how mosquito and viral genotypes interact to determine transmission rates of viruses to humans. This relationship varies across geographic landscapes and so can help to explain the distribution of human outbreaks. In addition, we are working with a bacterial symbiont in mosquitoes that limits the ability of the mosquito to transmit virus to humans. This bacterium is being released throughout the tropics and subtropics as a means of biocontrol against dengue and Zika. We are attempting to understand how the bacterium acts so that if resistance to the bacterium emerges either in viruses or mosquitoes, we may design counter measures that help maintain the efficacy of the biocontrol strategy. We use a combination of laboratory based infection/transmission assays, molecular genetic, genomic and modeling techniques. The data and models we are generating inform epidemiologists and practitioners in vector control. The mission of the veterinary entomology lab is to investigate the ecological relationships between vertebrates and their ectoparasites and other arthropod pests to facilitate development of control methods and IPM strategies. Through a better understanding of the ecology of vectors and their animal hosts we can develop novel approaches for vector control. Our research focuses primarily on arthropod pests of wildlife, in particular ticks and tick ecology, and on filth fly control in livestock, poultry, and equine systems. Current projects include areawide tick suppression, spatial ecology of deer and mouse movement in relation to tick vectors, analysis of immune function and tick host attraction, developing improved biological control for filth fly vectors, and understanding the ecology of Sarcoptes scabiei on black bear hosts in Pennsylvania. We use spatial analysis, behavioral studies, comparative genomics and other genetic analyses, field trials, and observational data in our research. Data are analyzed with arcGIS, modeling techniques, and inferential statistics as required by the project and data set. These data are used in complement with other research-based knowledge and recommendations and provided to stakeholders as part of the Cooperative Extension mission at Penn State.

Progress 10/01/19 to 09/30/20

Outputs
Target Audience:The justification for this work is to better understand insects and their pathogens and pests in an integrated manner to increase our ability to reduce the negative effect of insects as disease vectors in human and agricultural settings, as well as gain general insights into evolutionary processes. This will enable a broad group of stakeholders from researchers, extension staff, policymakers and the public to understand the critical intersection between insects and their pathogens and pests. Changes/Problems:Bjornstad Lab: We have been heavily involved in modelling the COVID-19 Pandemic since it broke in January 2020 with multiple grants awarded or pending. Our investigation of transmission control measures during the first 50 days of the COVID-19 epidemic in China was an important first analysis of the utility of social lockdowns. The publication that appeared in Science in April has already been cited almost 500 times. What opportunities for training and professional development has the project provided?The project has given the opportunity for research training to undergraduates, graduate students and postdocs. Across our groups we have provided such opportunities for a large number of individuals. How have the results been disseminated to communities of interest?The PIs have a track record of dissemination of their work to relevant stakeholders including state, national and international policy makers in agriculture and public health. In addition, the PIs have worked locally to engage the public through a range of outreach events at PSU and in schools. What do you plan to do during the next reporting period to accomplish the goals?The team of PIs will continue to progress their individual project goals while integrating across the broader network.

Impacts
What was accomplished under these goals? Objective 1 (McGraw, Machtinger, Sakamoto, Hughes, Jenkins) McGraw Lab: We have developed a set of hypotheses about how the endosymbiont Wolbachia works to prevent arbovirus replication inside mosquitoes and have begun functionally testing each hypothesis. Understanding how the agent works will have direct impact on its evolution in the field where it is being deployed globally for biocontrol. Machtintger Lab: We worked on properties of mechanical and biological vectors. We hosted a tick series and delivered three webinars and a vector-borne disease workshop. The Project Investigator (PI)gave one guest lecture on tick Integrated Pest Management (IPM) and gave three tick-related extension talks. Sakamoto Lab: We have been studying the historical distribution, behavior, and microbiomes of blacklegged ticks from central Pennsylvania. Manuscripts of the historical distribution and microbiomes have been completed and accepted/published. Hughes Lab: We developed machine learning tools to automatically track ants in both the confines of a colony and on trails outside the nest. Ants are themselves pestiferous insects so our work would help in the control of ants. The work is also of great interest to the study and control of disease in any high density settings from farm animals to humans. We also developed tools to track transboundary pests like locusts and fall armyworm. Jenkins Lab: Spotted Lanternfly - New activities this year included the initiation of field trials to evaluate the efficacy of fungal pathogens for the control of Spotted Lanternfly. Continued work on biocontrol of bed bugs. Continued research on factors affecting the efficacy of the Penn State developed technology using Beauvieria bassiana for control and prevention of bed bugs is providing essential information for use by the pest control industry. Mushroom flies - Ongoing research into novel management strategies for mushroom sciarid and phroid flies resulted in one research publications. Objective 2 (McGraw, Hughes, Myrick, Read, Jenkins) McGraw Lab: We developed Wolbachia transinfection for the buffalo fly - a leading pest insect of cattle to understand the ecological interactions. Hughes Lab: Using our ant model we developed a protocol to seed a complex society with an infectious agent (green fluorescent protein (GFP) labelled fungal spores) and track the distribution of the spores inside the nest at a micron scale. We also developed statistical models to track ants to determine the rate of transmission and how both frequency and density dependent process affect disease transmission. Myrick Lab: Developed flight mills and apparatus for measuring insect performance which is critical for detailed work on insect ecology. Read Lab: Our effortsfocused on the dynamics of antimicrobial resistance emergence. With elegant experimentation, we demonstrated that it is possible to suppress antibiotic resistance emergence using ecological principles to craft evolution-retarding treatment regimens. We experimentally evaluated the impact of antimicrobial treatment dose and duration on drug resistance emergence in a vector borne disease. Jenkins Lab: Spotted Lanternfly - New activities this year included the initiation of field trials to evaluate the efficiency of fungal pathogens for the control of Spotted Lanternfly. A large field trial in Norristown Farm Park in summer/fall 2019 providedpromising results following two applications of a commercially available Beauveria product (BoteGHA) using a tractor-mounted hand gun on four replicated split polts. Additionally, potted plant trials were conducted to evaluate the relative efficacy of three commercial fungal biopesticides at PSU Berks campus. Continued work on bed bugs. Objective 3 (Rasgon, Hughes) Rasgon Lab: 1) Identified a receptor for Zika virus in vertebrate cells; 2) Used the ReMOT Control gene editing technique (developed in the Rasgon Lab) to edit the genomes of Anopheles stephensi, Nasonia vitripennis, and for the first time, Bemisia tabac; 3) Demonstrated that the insect-specific parvovirus (AgDNV) negatively affects replication of the pathogenic arbovirus Mayaro virus in Anopheles mosquitoes and cells; 4) Used CRISPR/Cas9 gene editing to demonstrate the roleof the forked gene in actin bundle formation and scale and bristle formation in Aedes aegypti; 5) contributed to the whole genome sequencing of the mosquito Culex tarsalis; 7) identified small RNA responses in mosquito cell lines. Hughes Lab: Using our ant model we developed a protocol to seed a complex society with an infectious agent (GFP labelled fungal spores) and track the distribution of the spores inside the nest at a micron scale. We also developed statistical models to track ants to determine the rate of transmission and how both frequency and density dependent processes affect disease transmission. Objective 4 (Machtinger, Jenkins, Read Bjornstad Sakamoto) Jenkins Lab: In our Spotted Lanternfly we continued to inform state policies and efforts. Read Lab: Our efforts we focused on the dynamics of antimicrobial resistance emergence, aimed at mitigating antimicrobial resistance. With a chart review, we analyzed the factors associated with unnecessary antibiotic prescribing at our university student health clinic. We also reviewed the evolutionary risks of off-target selection following therapeutic antibiotic use. Sakamoto Lab: We have been studying the historical distribution, behavior, and microbiomes of blacklegged ticks from central Pennsylvania. Manuscripts of the historical distribution and microbiomes have been completed and accepted/published.

Publications

  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Ford SA, Albert I, Allen SL, Chenoweth, SF, Jones, M, Koh, C, Sebastian, A, Sigle, LT, McGraw, EA. 2020. Artificial Selection Finds New Hypotheses for the Mechanism of Wolbachia-mediated dengue blocking in mosquitoes. Front Microbiol. 11:1456.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Madhav, M, Brown, G, Morgan, JA, Asagari, S, McGraw EA, James, P. 2020. Transinfection of buffalo flies (Haematobia irritans exigua) with Wolbachia and effect on host biology. Parasite Vectors 13:296.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Madhav, M, Brown, G, Morgan, JA, Asagari, S, McGraw EA, Munderloh, UG, Kurtti, TJ, James, P. 2020. Wolbachia successfully replicate in a newly established horn fly, Haematobia irritans irritans (L.) (Diptera: Muscidae) cell line. Pest Mngt Sci. 76:2441-2452.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Novelo, M, Hall, Pak, D, MD, Young, PR, Holmes, EC, McGraw EA. 2020. Intra-host growth kinetics of dengue virus in the mosquito Aedes aegypti. PLOS Pathog. 15:e1008218.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Chrostek, E, Hurst, GDD, McGraw, EA. 2020. Vector-borne disease control: antiviral Wolbachia limits dengue in Malaysia. Curr Biol. 30:R30-R32.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Madhav, M, Brown, G, Morgan JAT, Asgari, S, McGraw EA, James, P. 201.9 Buffalo flies receptive to Wolbachia-infection: an opportunity for population control Proc. 36:79.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Morley, V.J., Woods, R.J., & Read, A.F. (2019). Bystander selection for antimicrobial resistance: implications for public health.�Trends in Microbiology�27: 864-877
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Hansen, E., Karslake, J., Woods, R.J., Read, A.F., & Wood, K. B. (2020). Antibiotics can be used to contain drug-resistant bacteria by maintaining sufficiently large sensitive populations.�PLoS Biology�18: e3000713
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Acosta, M., Bram, J., Sim, D., & Read, A.F. (2020). The effect of drug dose and timing of treatment on the emergence of drug resistance�in vivo�in a malaria model.�Evolution, Medicine and Public Health�2020: eoaa016.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Tiffin, H. S., R. Cockerill, J. Brown, and E. T. Machtinger. Protocol for efficient digestion of skin tissue samples to determine Sarcoptes scabiei mite density. Journal of Insect Science.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Skvarla, M.J., R. Trout-Fryxell, R. Butler, C. Jones, M. Burrell, S. Bacca, K. Poh, J. Evans, and E. T. Machtinger. Additional new state and country records for North American deer keds (Diptera: Hippoboscidae: Lipoptena). Journal of the Entomological Society of Ontario.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Burgess, IV E. R., C. J. Geden, K. H. Lohmeyer, B. H. King, E. T. Machtinger, and J. G. Scott. 2020. The companion animal insecticide fluralaner outperforms industry-leading agricultural insecticides in resistant and susceptible strains of filth flies. Scientific Reports. https://doi.org/10.1038/s41598-020-68121-z
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Machtinger, E. T. and E. R. Burgess IV. 2020. Evaluation of filth fly species composition and abundance using two monitoring methods in swine confinement housing. Journal of Medical Entomology. https://doi.org/10.1093/jme/tjaa104
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Roden-Reynolds, P., A. Y. Li, E. T. Machtinger, and J. M. Mullinax. Trapping white-tailed deer (Artiodactyla:Cervidae) in suburbia for study of tick-host interactions. Journal of Insect science.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Machtinger, E. T., S. C. Williams, and M. A. Linske. Practical guide to trapping Peromyscus leucopus and Peromyscus maniculatus for vector and vector-borne pathogen surveillance and ecology. Journal of Insect Science.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Skvarla, M., K.C. Poh, and E. T. Machtinger. A Technique for dissecting the salivary glands from the abdomens of deer keds (Diptera: Hippoboscidae: Lipoptena Nitzsch, 1818 and Neolipoptena Bequaert, 1942). Journal of Insect Science.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Poh, K.C., M. Skvarla, J. Evans, and E. T. Machtinger. Collecting Lipoptena cervi (Diptera: Hippoboscidae) and ticks (Parasitiformes: Ixodidae) from hunter-harvested deer. Journal of Insect Science.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Brown, J. E., T. M. Miller, and E. T. Machtinger. Tick tubes reduce blacklegged tick burdens on white-footed mice in Pennsylvania, USA. Journal of Applied Entomology. https://doi.org/10.1111/jen.12758
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Jones, A. M., M. T. Van de Wyngaerde, E. T. Machtinger, E. G. Rajotte. 2020. Choice of laboratory tissue homogenizers matters when recovering nucleic acid from medically important ticks. Journal of Medical Entomology. 57:1221-1227. https://doi.org/10.1093/jme/tjaa006
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Fedele, K., K. Poh, J. E. Brown, A. Jones, L. Durden, H. Tifton, A. Pagac, A. Li, and E. T. Machtinger. Host distribution and pathogen infection of fleas (Siphonaptera) recovered from small mammals in Pennsylvania. Journal of Vector Ecology. https://doi.org/10.1111/jvec.12371
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Morley, V.J., Firgens, E.P.C., Vanderbilt, R.R, Zhou, Y., Zook., M., Read, A.F., & MacGeorge, E.L. (2020). Factors associated with antibiotic prescribing for acute bronchitis at a university health center.�BMC Infectious Diseases�20:177 Morley, V.J., Woods, R.J., & Read, A.F. (2019). Bystander selection for antimicrobial resistance: implications for public health.�Trends in Microbiology�27: 864-877
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Title= Genus Lycorma Stal, 1863 https://sites.udel.edu/planthoppers/north-america/north-american-fulgoridae/genus-lycorma-stal-1863/
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Shikano I. Efficacy of a Fungal Biopesticide for Bed Bug Management Is Influenced by the Toxicity and Associated Behavioral Avoidance of Harborages on Insecticide-Impregnated Box Spring Covers. J Econ Entomol. 2020 Oct 1:toaa227. doi: 10.1093/jee/toaa227. Epub ahead of print. PMID: 33001173.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Myrick, A. J. and Baker, T. C. (2019) Analysis of anemotactic flight tendencies of the spotted lanternfly (Lycorma delicatula) during the 2017 mass dispersal flights in Pennsylvania. J. Insect Behav. https://doi.org/10.1007/s10905-019-09708-x
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Baker, T. C., Smyers, E. C., Urban, J. M., Meng,, Z., Pagadala Damadaram, K. J., Myrick, A. J., Cooperband, M. F., and Domingue, M. J. (2019) Progression of seasonal activities of adults of the spotted lanternfly, Lycorma delicatula, during the 2017 season of mass flight dispersal behavior in eastern Pennsylvania. J. Asia-Pac. Entomol. 22:705-713.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Hall, L. P., Graves, F., Myrick, A., Hoover, K., and Baker, T. C. (2019) Labial and maxillary palp recordings of the Asian longhorned beetle, Anoplophora glabripennis, reveal olfactory and hygroreceptive capabilities. J. Insect Physiol. 117: 103905.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Becker, A.D., Wesolowski, A., Bj�rnstad, O.N. and Grenfell, B.T. 2019. Long term dynamics of measles in London: titrating the impact of wars, the 1918 pandemic, and vaccination. PLOS Computational Biology 15(9): e1007305. https://doi.org/10.1371/journal.pcbi.1007305
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Sezen, Z, Bj�rnstad, O.N. and Shea, K. 2020. Oviposition response of the biocontrol agent Rhinocyllus conicus to resource distribution in its invasive host, Carduus nutans. Biological Control 152: 104369. https://doi.org/10.1016/j.biocontrol.2020.104369
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Bj�rnstad, O.N, Shea, K., Krzywinski, M. and Altman, N. 2020. Modeling infectious epidemics. Nature methods 17:455-456. https://doi.org/10.1038/s41592-020-0822-z
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Herzog, C.M., de Glanville, W.A., Willett, B.J., Cattadori, I.M., Kapur, V., Hudson, P.J., Buza, J., Swai, E.S. Cleaveland, S. and O. N. Bj�rnstad. 2019. Identifying age cohorts responsible for Peste des petits ruminants virus transmission among sheep, goats, and cattle in northern Tanzania. Viruses 12:186. doi:10.3390/v12020186.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Clifton, E. H., A. E. Hajek, N. E. Jenkins, R. T. Roush, John P. Rost D. Biddinger (2020). Applications of Beauveria bassiana (Hypocreales: Cordycipitaceae) to control populations of spotted lanternfly, Lycorma delicatula (Hemiptera: Fulgoridae), in semi-natural landscapes and on grapevines. ENVENT-2020-0085.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Kurtze, C., N. E. Jenkins, D.P. Hughes (2020) Evaluation of direct and indirect transmission of fungal spores in ants ? JIP_2019_156R2.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Maria Mazin Stefanos S. Andreadis Nina E. Jenkins Kevin R. Cloonan T.C. Baker Ed G. Rajotte (2019). Activity and distribution of the mushroom phorid fly, Megaselia halterata, in and around commercial mushroom farms.Entomologia Experimentalis et Applicata 167 (5), 389-395 https://doi.org/10.1111/eea.12777.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Giles, J.R., zu Erbach-Schoenberg, E., Tatem, A.J., Gardner, L., Bj�rnstad, O.N., Metcalf, C.J.E. and Wesolowski, A. 2020. The duration of travel impacts the spatial dynamics of infectious diseases. Proceedings of the National Academy of Sciences 117: 22572-22579
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Bj�rnstad, O.N, Shea, K., Krzywinski, M. and Altman, N. 2020. The SEIRS model for infectious disease dynamics. Nature methods 17: 867-868.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Tian, H. and Bjornstad, O.N. 2020. Population serology for SARS-CoV-2 is essential to regional and global preparedness. The Lancet Microbes. DOI: https://doi.org/10.1016/S2666-5247(20)30055-0
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Tian, T., Liu, Y, Li, Y., Wu2, C.-H., Chen, B., Kraemer, M.U.G, Li, B., Cai, J., Xu, B., Yang, Q., Wang, B., Yan, P., Cui, Y., Song, Y., Zheng, P., Wang, Q., Bjornstad, O.N., Yang, R., Grenfell, B.T., Pybus, O.G, and Dye, C. 2020. An investigation of transmission control measures during the first 50 days of the COVID-19 epidemic in China. Science 368: 638-642. https://doi.org/10.1126/science.abb6105
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Lau, M.S.Y., Becker, A.D, Korevaar, H.M., Caudron, Q., Shaw, D.J., Metcalf, C.J.E., Bjornstad, O.N. and Grenfell, B.T. 2020. A competing-risks model explains hierarchical spatial coupling of measles epidemics en route to national elimination. Nature Ecology & Evolution. https://doi.org/10.1038/s41559-020-1186-6
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Shikano, I. L Gomez, GS Bellicanta, NE Jenkins (2019) Persistence and Lethality of a Fungal Biopesticide (Aprehend) Applied to Insecticide-impregnated and Encasement-type Box Spring Covers for Bed Bug Management Journal of economic entomology 112 (5), 2489-2492.
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Chaverra-Rodriguez D, Benetta ED, Heu CC, Rasgon JL, Ferree PM, Akbari OS. 2020. Germline mutagenesis of Nasonia vitripennis through ovarian delivery of CRISPR-Cas9 ribonucleoprotein. Insect Molecular Biology. Online ahead of print (Preprint available at bioRxiv 087494)
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Ma Q, Srivastav SP, Gamez S, Feitosa-Suntheimer F, Patterson EI, Johnson RM, Matson E, Gold A, Brackney D, Connor J, Colpitts T, Hughes GL, Rasgon JL, Nolan T, Akbari OS, Lau N. 2020. An integrated mosquito small RNA genomics resource reveals dynamic evolution and host responses to viruses and transposons. bioRxiv 061598
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Urakova N, Brustolin M, Joseph RE, Johnson RM, Pujhari S, Rasgon JL. 2020. Anopheles gambiae densovirus (AgDNV) negatively affects Mayaro virus infection in Anopheles gambiae cells and mosquitoes. Parasites and Vectors. 13: 143
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Heu CC, McCullough F, Luan J, Rasgon JL. 2020. CRISPR/Cas9-based genome editing in the silverleaf whitefly (Bemisia tabaci). CRISPR Journal. 3: 89-96. (Preprint available at bioRxiv 996801)
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Dokic S, Anna B, Zurim I , Urakova N, Rasgon JL, Abdu U. 2020. Actin bundles play different role in shaping scale as compared to bristle in mosquito Aedes aegypti. Scientific Reports. Online ahead of print. (Preprint available at bioRxiv 027110)
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Macias VM, McKeand S, Chaverra-Rodriguez D, Hughes GL, Fazekas A, Pujhari S, Jasinskiene N, James AA, Rasgon JL. 2020. Cas9-mediated gene-editing in the malaria mosquito Anopheles stephensi by ReMOT Control. G3. 4: 1353-1360. (Preprint available at: bioRxiv 775312).
  • Type: Journal Articles Status: Accepted Year Published: 2020 Citation: Jennifer R Gordon, Urban Entomology Highlights From 2019 Help Create Integrated Pest Management Plans, Journal of Medical Entomology, Volume 57, Issue 5, 1 September 2020, Pages 13421348, https://doi.org/10.1093/jme/tjaa121


Progress 10/01/18 to 09/30/19

Outputs
Target Audience:The target audience for this project continues to be a broad range of stakeholder. As our focus is on injurious and pest insects an important target audience of those interested in human and animal health (e.g. livestock). These are at the State, National and Internationa scale and include government workers, NGOs and international development partners Changes/Problems:There were no changes or problems What opportunities for training and professional development has the project provided?Working groups: We worked with members of working group developing guidelines for SIT-based interventions for control of Aedes mosquitoes and Aedes-borne diseases, jointly supported by the IAEA and the TDR/WHO and NTD/WHO Departments. How have the results been disseminated to communities of interest?1) On-Line course The Epidemics MOOC which is completely free to all learners provides a broad overview of the science of outbreak ecology and related topics. It is currently the top ranked science MOOC according to web-rankings. We believe the course have, by science outreach standards, significant societal impact. Of the 34,410 learners since the course went 'on-demand' in 2015. The enrollment has been 46% are female and 54% male with age-distrbution of the learners 13-17 (0.2%), 18-24 (9%), 25-34 (22%), 35-44(9%), 45-54 (4%), 55-64 (3%), 65+ (2%). Educational status: Full-time student (31%) Part-time student (11%) Not a student (58%). Highest Education Level: Doctorate degree (12%) Professional school degree (11%) Master's degree (29%) Bachelor's degree (28%) Associate degree (5%) Some college but no degree (8%) High school diploma (6%) Some high school (2%). Employment Status: Employed full-time (50%) Employed part-time (10%) Self-employed full-time (4%) Self-employed part-time (4%) Unemployed and looking for work (13%) Unemployed and not looking for work (8%) Other (11%). Geographic reach: North America (41%) Europe (21%) Asia (20%) South America (8%) Africa (8%) Oceania (3%). 2) The Great Insect Fair: The work was widely shared with members of the public who came to see the Department of Entomolohgy's annua Insect Fair. What do you plan to do during the next reporting period to accomplish the goals?The team of PIs will continue to progress their individual project goals while integrating across the broader network.

Impacts
What was accomplished under these goals? McGraw Lab: We have developed the likely way that Wolbachia mediated blocking of dengue virus in the mosquito Aedes aegypti will evolve in the field and examined the challenge to viruses to evolve resistance against blocking (1,2). This trait is the basis of a global program of biocontrol against dengue and zika virus transmission to humans. We have also contributed further to defining the mechanism by which blocking works. Lastly, through collaborations we have examined the role of temperature in chikungunya virus transmission by the mosquito, Aedes albopictus. Bjornstad Lab: We have been continuing to develop new mathematical and computational frameworks for Disease and Outbreak dynamics (1). Including a new suite of predictive models for the spatial spread of infections. We further developed new models for how temperature affect the dynamics of insect vectors and other outbreaking insect pests (1,2, 3). We published textbook on 'Infectious Disease Dynamics using R' associated open-source software that is a step-by-step guide to developing mathematical models. Machtinger Lab: we developed a citizen science project to evaluate keds as potential disease vectors in Pennsylvania with over 500 participating stakeholders. This resulted in over 700 samples and addition of many state and county records for three different species of keds. We demonstrated that white-footed mouse use of tick control bait boxes was similar to adding the caloric benefits of local oak acorns which may lead to increased mouse numbers and thus increased tick-borne diseases (1). We demonstrated the efficacy of several common repellents for use against house flies on horses. We showed that school administrators have limited knowledge of tick-borne diseases and tick control, which may lead to greater educational opportunities. We developed a mange matrix to evaluate mange in Pennsylvania black bears and collected tick specimens from American black bears to evaluate the impact bears may have on tick distribution (4). Read Lab: With genomic analyses, we identified punctuated evolution as a feature of a vector-borne viral pathogen of wildlife, a canonical model of virulence evolution (2,3). We also determined the molecular epidemiological structure of a viral pathogen on PA farms, showing farm to farm transfer, coexistence and strain turnover in response to vaccination processes (3). Thomas Lab: We continued research exploring how environmental temperature affects the capacity of mosquitoes to transmit diseases such as dengue and malaria (1,2). One of our key findings has been to reveal how time of feeding interacts with daily temperature variation to dramatically alter vector competence. In environments typical of many high transmission settings mosquitoes feeding at the end of the night towards the morning have very low competence and hence contribute little to overall transmission (2). Those that feed in the early evening have elevated competence and contribute disproportionately to transmission compared with midnight feeders. These results have important implications for understanding the epidemiological consequences of 'behavioral resistance'. A further major activity has been the completion of a large randomized controlled trial testing the impact of a novel mosquito control intervention in 40 villages in central Cote d'Ivoire. Our results show 40-50% reduction in malaria incidence in the treatment villages and 60% reduction on overall mosquito transmission rate. This result was achieved above and beyond the effect of universal coverage of long lasting insecticide treated bed nets. The study represents one of the first large scale trials to demonstrate substantial epidemioogical impact of a genuinely novel mosquito control intervention. Hughes Lab: We developed machine learning tools to automatically track ants in both the confines of a colony and on trails outside the nest (1). We also developed a protocol to seed a complex society with an infectious agent (GFP labelled fungal spores) and track the distribution of the spores inside the nest at a micron scale. We also developed statistical models to track ants to determine the rate of transmission and how both frequency and density dependent process affect disease transmission. Ants are themselves pestiferous insects so our work would help in the control of ants. The work is also of great interest to the study and control of disease in any high density settings from farm animals to humans (1,2).

Publications

  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Kerr, P.J., Eden, J-S., Di Giallonardo, F., Peacock, D., Liu, J., Strive, T., Read, A.F., & Holmes, E.C Punctuated evolution of myxoma virus: rapid and disjunct evolution of a recent viral lineage in Australia. Journal of Virology 93: e01994-1
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Bell, A.S., Kennedy, D.A., Jones, M.J., Cairns, C.L., Pandey, U., Dunn, P.A., Szpara, M.L., & Read, A.F. Molecular epidemiology of Mareks disease virus in Central Pennsylvania, USA. Virus Evolution 5: vey042
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Machtinger, E. T., and A. Y. Li. Use of Select TCSTM tick control bait boxes by white-footed mice (Peromyscus leucopus) in the suburban landscape of Maryland. Ecosphere. Accepted
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Tuorinsky, E. V., and E. T. Machtinger. 2019. Behavioral inhibition of the house fly, Musca domestica (Diptera: Muscidae), when exposed to commercial equine fly repellents. Journal of Economic Entomology. Accepted.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Machtinger, E.T., A.Y. Li, and Yifen Liu. 2019. Tick Bite risk and tick-borne disease perceptions of schools in the Mid-Atlantic United States. Journal of School Health Accepted
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Skvarla, M.X., E.T. Machtinger. 2019. Deer keds (Diptera: Hippoboscidae: Lipoptena and Neolipoptena) in the United States and Canada: New State and County Records, Pathogen Records, and an Illustrated Key to Species. Journal of Medical Entomology. 56:744-760. https://doi.org/10.1093/jme/tjy238
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Herzog, C.M., de Glanville, W.A., Willett, B.J., Kibona, T.J., Cattadori, I.M., Kapur, V., Hudson, P.J., Buza, J., Cleaveland, S. and O. N. Bj�rnstad. 2019. Pastoral production is associated with increased peste des petits ruminants seroprevalence in northern Tanzania across sheep, goats and cattle. Epidemiology and Infection, 147, E242.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Vindstad, O.P.L., Jepsen, J.U., Yoccoz, N.G., Bj�rnstad, O.N., Mesquita, M.D.S and Ims, R.A. 2019. Spatial synchrony in sub-arctic geometrid moth outbreaks reflects dispersal in larval and adult lifecycle stages. Journal of Animal Ecology.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Li, R., Xu, L., Bj�rnstad, O.N., Liu, K., Song, T., Chen, A., Xu, B., Liu, B. and Stenseth, N.C. 2019. Climate-driven variation in mosquito density predicts the spatio-temporal dynamics of dengue. Proceedings of the National Academy of Sciences USA 116: 3624-3629.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Goldstein, J., Park, J., Haran, M., Liebhold, A. and Bj�rnstad, O.N. 2019. Quantifying spatio-temporal variation of invasion spread. Proceedings of the Royal Society of London Series B 286: 20182294.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Nelson, W.A., Jouncour, B., Pak, D. and Bj�rnstad, O.N. 2019. Asymmetric interactions and their consequences for vital rates and dynamics: the smaller tea tortrix as a model system. Ecology 100(2):e02558. doi.org/10.1002/ecy.2558
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Barreaux, A.M., Oumbouke, W.A., Tia I.Z., Koffi, A.A., Nguessan, R., Thomas, M.B. (2019). Semi-field evaluation of the cumulative effects of a Lethal House Lure on malaria mosquito mortality. Malaria Journal 18(1), 298.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Waite, J.L., Suh, E., Lynch, P.A. & Thomas, M.B. (2019). Exploring the lower thermal limits for development of human malaria, Plasmodium falciparum. Biology Letters 15, 20190275.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Mordecai, E.A., Caldwell, J.M., Grossman M.K., Lippi, C.A., Johnson, L.R., Neria, M., Rohr, J.R., Ryan S.J., Van Savage, Shocket, M.S., Sippy R., Stewart Ibarra, A.M., Thomas, M.B. & Villena, O. (2019). The thermal biology of mosquito-borne disease. Ecology Letters 22, 16901708.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Valverde-Garcia, P., Santiago-Alvarez, C., Thomas, M.B., Maranh�o, E.A.A., Garrido-Jurado, I., Quesada-Moraga, E. (2019). Sublethal effects of mixed fungal infections on the Moroccan locust, Dociostaurus maroccanus. Journal of invertebrate pathology 61, 61-69.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Modlmeier, Andreas P., Ewan Colman, Ephraim M. Hanks, Ryan Bringenberg, Shweta Bansal, and David P. Hughes. "Ant colonies maintain social homeostasis in the face of decreased density." eLife 8 (2019): e38473.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Imirzian, N., Zhang, Y., Kurze, C., Loreto, R. G., Chen, D. Z., & Hughes, D. P. (2019). Automated tracking and analysis of ant trajectories shows variation in forager exploration. Scientific reports, 9(1), 1-10.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Wimalasiri-Yapa BMCR, Stassen L, Hu W, Yakob L, McGraw EA, Pyke AT, Jansen CC, Devine GJ, Frentiu FD. 2019. Chikungunya virus transmission at low temperature by Aedes albopictus mosquitoes. Pathogens. 8:E149.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Ford SA, Allen SL, Ohm JR, Sigle LT, Sebastian A, Albert I, Chenoweth SF, McGraw EA. 2019. Selection on Aedes aegypti alters Wolbachia-mediated dengue virus blocking and fitness. Nat Microbiol. in press.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Huang X, Hu W, Yakob L, Devine GJ, McGraw EA, Jansen CC, Faddy HM, Frentiu FD.2019. El Nino Southern Oscillation, overseas arrivals and imported chikungunya cases in Australia: a time series analysis. PLoS Neglect Trop Dis. 13:e0007376.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Terradas, G and McGraw, EA. 2019. Using genetic variation in Aedes aegypti to identify candidate anti-dengue virus genes. BMC Infect Dis. 19:580.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Koh C, Audsley MD, Di Giallonardo F, Kerton EJ, Young PR, Holmes EC, McGraw EA. 2019. Sustained Wolbachia-mediated blocking of dengue virus isolates following serial passaging in Aedes aegypti cell culture. Virus Evol. 5:vez012.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Sigle LT and McGraw EA. 2019. Expanding the canon: non-classical mosquito genes at the interface of arboviral infection. Insect Biochem Mol Biol. 109:72-80.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Haqshenas, G, Terradas, G, Paradkar, PN, Duchemin, JB, McGraw, EA and Doerig, C. 2018. A role for the insulin receptor in the suppression of dengue virus and Zika virus in Wolbachia-infected mosquito cells. Cell Reports 26:529-535.e3.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Koh, C, Allen, S, McGraw, EA and Chenoweth, SF. 2018. The transcriptional response of Aedes aegypti with variable extrinsic incubation periods for dengue virus. Genome Biol Evolution 10:3141-3151.


Progress 10/01/17 to 09/30/18

Outputs
Target Audience:We are targeting diverse stakeholders ranging from other scientists to pest management specialists, policy makers and educators intersted in the public dissemination of knowledge. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?The project has given the opportunity for research training to undergraduates, graduate students and postdocs. Across our groups we have provided such opportunities for a large number of individuals. How have the results been disseminated to communities of interest?The PIs have a track record of dissemination of their work to relevant stakeholders including state, national and international policy makers in agriculture and public health. In addition, the PIs have worked locally to engage the public through a range of outreach events at PSU at in schools. What do you plan to do during the next reporting period to accomplish the goals?The team of PIs will continue to progress their individual project goals while integrating across the broader network.

Impacts
What was accomplished under these goals? We have developed a likely mechanism by which the endosymbiont, Wolbachia limits the replication of viruses inside mosquitoes. This trait is the basis of a global program of biocontrol against dengue and zika virus transmission to humans. Understanding the mechanism will help us develop strategies for mitigating the emergence of resistance against Wolbachia. We have investigated the impact of host-targeted treatment devices on tick hosts which may help us understand the indirect effects of these control options. We have identified several novel compounds that may be exploited as repellents for common ticks that vector disease which may help reduce the risk of tick-borne disease in areas where these ticks are present. We have investigated the drivers of drug resistance in vector borne disease, in particular the role of nutrient deficiency and the fitness costs and benefits of resistance. We have also investigate the volatiles produced by malaria-infected people that attract insect vectors and finished our analysis of the evolution of virulence in a vector-born wild life pathogen. We have continued lab, semi-field and field studies to better understand how environmental factors influence transmission of vector-borne diseases, how insecticide resistance impacts the effectiveness of current control tools, and to explore the impact of novel control tools. We have investigated the mechanisms by which fungal pathogens manipulate the behavior of ants. We identified novel compounds and genes involved in this manipulation as well as development of machine learning tools to track fungal cells automatically. We also investigate the dynamics of fungal disease transmission in an ant society leading to the development of novel statistical methods. We have investigated how the malaria control efforts in countries of the Greater Mekong Subregion have impacted the malaria epidemiology, transmission and parasite population genetics. Using parasite field isolates collected from this region, we use genomic information to determine how relatedparasites on different border regions so that we can predict how human migration contributes to parasite reintroduction. We use genome data and phenotypic data to determine how resistance to antimalarial drugs evolves and spread in this region. We have developed new models of spatiotemporal spread of infectious diseases and continued to refine previous reports' model of temperature-driven models of insect vector development. These models will help predict risk of future outbreaks. For example, using measures of environmental temperature we can use models to predict how many months per year a vector borne disease such as Zika could potentially be transmitted in each of the different states in the US. We have developed new methods for CRISPR/Cas9 gene editing in mosquitoes are are currently extending the technology to other invertebrate and vertebrate organisms. This technology will allow for easy genetic manipulation of organisms of agricultural and medical importance.

Publications

  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Amuzu, HE, Tsyganov, K, Koh, C, Herbert, RI, Powell, DR and McGraw, EA. 2018. Wolbachia enhances insect-specific flavivirus infection in Aedes aegypti mosquitoes. Ecology Evolution 8:5441-5454
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Di Giallonardo, F, Audsley, MD, Shi, M, Young, PR, McGraw, EA and Holmes, EC. 2018. Complete genome of the Aedes aegypti anphevirus in the Aag2 mosquito cell line. J Gen Virol. 99:832-836
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Herbert, RI, McGraw, EA. 2018. The nature of the immune response in novel Wolbachia-host associations. Symbiosis 74:225-236
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Audsley, MD, Selezenv, A, Joubert, DA, Woolfit, M, ONeill, SL and McGraw EA. 2018. Wolbachia infection alters the relative abundance of resident bacteria an adult Aedes aegypti mosquitoes, but not larvae. Mol Ecol. 27:297-309
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Audsley, MD, Ye, YH, McGraw, EA. 2017. The microbiome composition of Aedes aegypti is not critical for Wolbachia-mediated inhibition of dengue virus. PLoS Neglect Trop Dis. 11:e0005426
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Terradas G, Joubert, DA, McGraw EA. 2017. Wolbachia-mediated blocking of dengue virus in mosquito cells is due in part to the action of the RNAi pathway. Sci Rep 7:43847
  • Type: Other Status: Accepted Year Published: 2018 Citation: Ryan-Reynolds, P, G. Hummel, E.T. Machtinger, and A.Y. Li. 2018. Development of novel raccoon exclusion device to protect Sherman traps from manipulation in the field. Wildlife Society Bulletin. Accepted.
  • Type: Journal Articles Status: Accepted Year Published: 2018 Citation: Machtinger, E.T., and A.Y. Li. 2018. Toxicity and repellency of four fatty acid compounds on lone star ticks, Amblyomma americanum. Applied Entomology and Zoology. Accepted.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Machtinger, E.T., and A. Y. Li. 2017. Evaluation of the toxicity and repellency of four commercial natural products to Amblyomma americanum. Experimental and Applied Acarology 73: 451-460.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Huijben, S., Chan, B.H.K., Nelson, W.A., & Read, A.F. (2018). The impact of within-host ecology on the fitness of a drug resistant parasite. Evolution, Medicine and Public Health 2018: 127-137
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Kennedy, D.A., Dunn, P.A., & Read, A.F. (2018). Modeling Mareks disease virus transmission: a framework for evaluating the impact of farming practices and evolution on disease. Epidemics 23: 85-95. PMC5989573
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: De Moraes, V.M., Wanjiku, C., Stanczyk, N., Pulido, H., Sims, J., Betz, H.S., Read, A.F., Torto, B. & Mescher, M.C. (2018) Volatile biomarkers of symptomatic and asymptomatic malaria infection in humans. Proceedings of the National Academy of Science USA. 115: 5780-5785. PMC5984526
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Wale, N., Sim, D.G., Jones, M.J., Salathe, R., Day, T., & Read, A.F. (2017). Resource limitation prevents the emergence of drug resistance by intensifying within host competition. Proceedings of the National Academy of Science USA 114: 13774-13779.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Liu, J., Cattadori, I.M., Sim, D.G., Eden, J-S., Holmes, E.C., Read, A.F., & Kerr, P.J. (2017). Reverse engineering field isolates of myxoma virus demonstrates that some gene disruptions or loss of function do not explain virulence changes observed in the field. Journal of Virology 91:e01289-17
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Barreaux, A.M., Koffi, A.A., NGuessan, R., Oumbouke, W.A., Tia, I.Z. and Thomas, M.B., 2018. Semi-field studies to better understand the impact of eave tubes on mosquito mortality and behaviour. Malaria journal, 17(1), p.306.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Sternberg, E.D., Cook, J., Alou, L.P.A., Aoura, C.J., Assi, S.B., Doudou, D.T., Koffi, A.A., NGuessan, R., Oumbouke, W.A., Smith, R.A. and Worrall, E., 2018. Evaluating the impact of screening plus eave tubes on malaria transmission compared to current best practice in central C�te dIvoire: a two armed cluster randomized controlled trial. BMC public health, 18(1), p.894.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Thomas, S., Ravishankaran, S., Justin, N.J.A., Asokan, A., Kalsingh, T.M.J., Mathai, M.T., Valecha, N., Montgomery, J., Thomas, M.B. and Eapen, A., 2018. Microclimate variables of the ambient environment deliver the actual estimates of the extrinsic incubation period of Plasmodium vivax and Plasmodium falciparum: a study from a malaria-endemic urban setting, Chennai in India. Malaria journal, 17(1), p.201.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Ohm, J.R., Baldini, F., Barreaux, P., Lefevre, T., Lynch, P.A., Suh, E., Whitehead, S.A. and Thomas, M.B., 2018. Rethinking the extrinsic incubation period of malaria parasites. Parasites & vectors, 11(1), p.178.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Rhodes, V.L., Thomas, M.B. and Michel, K., 2018. The interplay between dose and immune system activation determines fungal infection outcome in the African malaria mosquito, Anopheles gambiae. Developmental & Comparative Immunology, 85, pp.125-133.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Smith, R.A., Kim, Y., Zhu, X., Doudou, D.T., Sternberg, E.D. and Thomas, M.B., 2018. Integrating Models of Diffusion and Behavior to Predict Innovation Adoption, Maintenance, and Social Diffusion. Journal of health communication, 23(3), pp.264-271.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Thomas, M.B., 2018. Biological control of human disease vectors: a perspective on challenges and opportunities. BioControl, pp.1-9.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Shapiro, L.L., Whitehead, S.A. and Thomas, M.B., 2017. Quantifying the effects of temperature on mosquito and parasite traits that determine the transmission potential of human malaria. PLoS biology, 15(10), p.e2003489.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Kittichai, V., Nguitragool, W., Ngassa Mbenda, H. G., Sattabongkot, J., Cui, L. 2018. Genetic diversity of Plasmodium vivax multidrug resistant 1 gene in Thai parasite populations. Infect. Genet. Evol. 64, 168-177.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Zhao, Y., Zeng, J., Zhao, Y., Liu, Q., He, Y., Zhang, J., Yang, Z., Fan, Q., Wang, Q., Cui, L., Cao, Y. 2018. Risk factors for asymptomatic malaria infections from seasonal cross-sectional surveys along the ChinaMyanmar border. Malar. J. 17, 247.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Bai, Y., Zhang, J., Geng, J., Xu, S., Deng, S., Zeng, W., Wang, Z., Ngassa Mbenda, H.G., Zhang, J., Li, N., Wu, Y., Li, C., Liu, H., Ruan, Y., Cao, Y., Yang, Z.,* Cui, L.* 2018. Longitudinal surveillance of drug resistance in Plasmodium falciparum isolates from the China-Myanmar border reveals persistent circulation of multidrug resistant parasites. Int. J. Parasitol Drugs Drug Resist. 8, 320-328.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Siddiqui, F.A., Cabrera, M., Wang, M., Brashear, A., Kemirembe, K., Wang, Z., Miao, J., Chookajorn, T., Yang, Z., Cao, Y., Dong, G., Rosenthal, P. J., Cui, L. 2018. Plasmodium falciparum falcipain-2a polymorphism in Southeast Asia and its potential contribution to artemisinin resistance. J. Infect. Dis. 218, 434-442.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Dalziel, B.D., Kissler, S., Gog, J. Viboud, C., Bj�rnstad, O.N., Metcalf, C.J.E., Grenfell, B.T. 2018. Urbanization and humidity shape the intensity of influenza epidemics in US cities. Science 362: 75-79. doi.org/ 0.1126/science.aat6030
  • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: Tian, H., Wu, X., Cazelles, B., Chowell, G., Dong, L., Laine, M., Li, Y., Yang, H., Li, Y., Yang, Q., Tong, X., Huang, R., Xiao, H., Stenseth, N.C. 2018. Urbanization prolongs hantavirus epidemics in cities. Proceedings of the National Academy of Sciences USA 115: 4707-4712. doi.org/10.1073/pnas.1712767115
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Morris, S.E., de Blasio, B.F., Viboud, C., Wesolowski, A., Bj�rnstad, O.N. and Grenfell, B.T. Analysis of multi-level spatial data reveals strong synchrony in seasonal influenza epidemics across Norway, Sweden, and Denmark. PLoS ONE 13(5): e0197519; doi.org/10.1371/journal.pone.0197519.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Bhattacharyya, S., Ferrari, M.J. and Bj�rnstad, O.N. 2017. Species interactions may help explain the erratic periodicity of whooping cough dynamics. Epidemics 3: 64-70 doi.org/10.1016/j.epidem.2017.12.005.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Li, S-L., Bj�rnstad, O.N., Ferrari, M., Mummah, R., Runge, M.C., Fonnesbeck, C., Tildesley, M.J, Probert, W.J.M. and Shea, K. 2017. Essential information: Uncertainty and optimal control of Ebola outbreaks. Proceedings of the National Academy of Science USA 114: 56595664. doi.org/10.1073/pnas.1617482114
  • Type: Book Chapters Status: Published Year Published: 2018 Citation: Bj�rnstad, O. N. 2018. Epidemics: Models and Data using R. Springer (326 pp) ISBN 978-3-319-97487-3 https://www.springer.com/gp/book/9783319974866
  • Type: Other Status: Published Year Published: 2018 Citation: D Chaverra-Rodriguez, VM Macias, GL Hughes, S Pujhari, Y Suzuki, Targeted delivery of CRISPR-Cas9 ribonucleoprotein into arthropod ovaries for heritable germline gene editing Nature Communications 9, 3008


Progress 10/01/16 to 09/30/17

Outputs
Target Audience: We are targeting diverse stakeholders ranging from other scientists (who build upon or work) to pest management specialists, policy makers and educators interested in the public dissemination of knowledge. Changes/Problems:We did not experience any major problems during this reporting period. What opportunities for training and professional development has the project provided?At the core of our approach is training undergraduates,graduate students, post-docs visitimg scientists. We have trained numerous individuals at all categories during this year. How have the results been disseminated to communities of interest?Across all the PIs there is a strong interest to dissemination to communities. We have engaged state, national and international policy makers We have engaged in multiple outreach events both at PSU and in schools around the state to communicate our work What do you plan to do during the next reporting period to accomplish the goals?Our work is very integrtaed and well funded and we will continue to work in a directed, interdisciplinary fashion.

Impacts
What was accomplished under these goals? Development of an Artificial Intelligence(AI) assistant to automate diagnosis of pests and pathogens of crops in North America, South America and Africa. The AI assistant relies upon the construction and training of convolutional neural networks where the machine learns the disease symptoms and provides a diagnosis in real time via a smart phone by placing a box over the symptom as camera is viewing the crop. This box is a form of machine learning called object level classification and the user see both the disease category and the machine's probability that it is correct. This AI assistant works offline so an intenret connection is not needed making it useful for both the developing world and rural areas in the devloped world where coverage is poor. The AI app is built on TensorFlow which is a popular machine learning library and is integrated within a native Android app. This app then allows downstream functions. The first is the delivery of extension advice immediately upon diagnosis. The app call also send reminders at a set time after diagnosis (e.g. follow up alert 3 days later). The app integrates withhttp://plantvillage.psu.eduwhere stakeholders (e.g. Department of Agriculture, extension services) can see a map of the records and examine records for human verification. We have built a Fall Armyworm AI assistant and a Cassava disease AI that recognizes 5 diseases. The former is being rolled out across 30 countries in Africa via the UN FAO who are leading efforts to understand and control this emerging pest in Africa which is expected to cost $6bn/year in damages. The latter tool is in collaboration with CGIAR and is being field trialled now in East Africa with the intent to use it in South America, Africa and Asia. Locally we are building an AI assistant to diagnose Spotted Lantern Fly which is considered by the PA Department of Agriculture to have the potential to destroy $18bn worth of commodity crops. Our SLF AI assistant will be integrated into the existing databases for PA. It will also be designed to encourage scouting by 4-H kids, landscape gardeners and the general public. At the backend it will provide extension with real time mapping of the spread. Large field trials across multiple African villages to test the efficacy of a new technology to reduce vector entrance into homes and the resultanttransmission of diseases.The trial is being conducted in 40 villages in central Cote d'Ivoire, with 20 villages in the treatment arm and 20 villages in the control arm. The intervention being tested is a type of house modification called the "Eave Tube".Eave tubes are a novel house-based intervention for delivering targeted doses of insecticide against malaria mosquitoes as they attempt to enter the house. The eave tube device itself consists of a section of PVC pipe fitted into an otherwise closed eave, with a screened insert that is placed inside the tube. The screening of the insert is treated with insecticide. By relying on the host cues that typically draw malaria mosquitoes into human dwellings, eave tubes turn the house into what is effectively a "lure and kill" device. Eaves are targeted because the open eaves found in many traditional African houses are a particularly important source of attractive cues for malaria mosquitoes, and represent the key entry point for An. gambiae in sub-Saharan Africa. In setting up the field trial we put eave tubes in >3000 houses and are now evaluating impact on mosquito populations and malaria transmission by monitoring clinical incidence of malaria in cohorts of 50 children in each of the 40 villages (i.e. total of 2000 children enrolled, with each child visited 2-times per month). Thetrial currently supports >65 project personnel, with and additional 800 volunteers responsible for mosquito sampling.The trial is due to run for 2 years. At present we have only conducted a preliminary analysis on the first 3 months of epidemiological data. This shows a 31% reduction in likelihood of clinical malaria in the study cohorts in the treatment arm. To observe a significant reduction in risk of malaria so soon after establishing the intervention is extremely encouraging.The entomology data also show a significant impact of the intervention, with a 50% reduction in total vector population and an 80% reduction in the number of vectors caught indoors. Experimental and mathematical studies of the evolution of virulence and transmission dynamics. Our molecular genetic and phenotyping studies of the myxoma virus evolution have revealed escalating virulence evolution in the virus. The virus now kills standard test hosts as fast or faster than the ancestral virus released in the 1950s as a biocontrol agent. Our studies show that this escalation is almost certainly an evolutionary response to increases in host resistance which have occurred as result of virally-imposed natural selection for host resistance. The virus has now become hyper-immunosuppressive, effectively turning off innate antiviral responses in the host shortly after first infection. In the field this escalation of host resistance and viral virulence has left the final host-pathogen interaction sitting in much the same place - the hosts and virus have fought themselves to a standstill. But this has important implications for agricultural and human health: viral evolution in response to enhanced host resistance (as can be achieved in farm animals with, for instance, selective breeding, genetic modification, improved husbandry and vaccination) can create the conditions in which highly immunosuppressive viruses evolve. These could cause serious problems should they spill into unprotected populations (organic operations, wildlife, neighboring farms with the relevant technology. We have also wrapped up our three-year surveillance of Marek's disease in PA farm poultry farms. This has revealed the on-going transmission of virus in vaccinated flocks, erratic dynamics most easily understood in terms of local eradication and reintroduction (meta-population dynamics) and the co-circulation of genetically distinct strains of possibly different levels of virulence. Roughly a third of broiler farms have detectable virus on them at any point in time, but flock health is not being impacted because of the anti-disease impact of vaccination. The conditions exist for the evolution of more immunosuppressive viruses, as has we saw in the myxoma-wildlife setting. We continue to work on the molecular epidemiology and evolution dynamical modelling of the data set and samples we have collected. We also completed theoretical work on why drug resistance evolves so readily but vaccine resistance does not. The hypotheses we generated and which we demonstrated are mathematically allow us to identity settings and features of next generation vaccines which would make them vulnerable to the evolution of vaccine resistance. It also makes clear the properties need to generate next generation antimicrobial drugs which would be more evolution-proof.

Publications

  • Type: Journal Articles Status: Accepted Year Published: 2017 Citation: MMacias VM, Ohm JR, Rasgon JL, 2017, Gene Drive for Mosquito Control: Where Did It Come from and Where Are We Heading?
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: JC Russell, EM Hanks, A P. Modlmeier and DP Hughes (2017) Modeling Collective Animal Movement Through Interactions in Behavioral States Journal of Agricultural, Biological and Environmental Statistics Volume 22, Issue 3, pp 313334
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Ara�jo, J., and D.P. Hughes (2016) Diversity of Entomopathogenic Fungi: Which Groups Conquered the Insect Body? Advances in Genetics Vol 94: 1-39.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Pujhari S, Macias VM, Nissly RH, Nomura M, Kuchipudi, Rasgon JL, 2017, Heat Shock Protein 70 (Hsp70) Is Involved In The Zika Virus Cellular Infection Process, bioRxiv.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Hagan R, Szuter E, Rosselot A, Holmes C, Siler S, Rosendale A, Hendershot J, Elliot K, Jennings E, Rizlallah A, Xiao Y, Watanabe M, Romick-Rosendale L, Rasgon JL, Benoit J, 2017, Dehydration Bouts Prompt Increased Activity And Blood Feeding By Mosquitoes, bioRxiv.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Dodson B, Andrews ES, Turell MJ, Rasgon JL, 2017, Wolbachia Effects On Rift Valley Fever Virus Infections In Culex tarsalis Mosquitoes, bioRxiv.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Ssentongo P, Robuccio AE, Thuku G, Sim DG, Nabi A, Bahari F, Shanmugasundaram B, Billard MW, Geronimo A, Short KW, Drew PJ, Baccon J, Weinstein SL, Gilliam FG, Stoute JA, Chinchilli VM, Read AF, Gluckman BJ, Schiff SJ, 2017, A Murine Model to Study Epilepsy and SUDEP Induced by Malaria Infection, Scientific Reports.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Kennedy DA, Dunn PA, Read AF, 2017, Modeling Marek's disease virus transmission: a framework for evaluating the impact of farming practices and evolution on disease, bioRxiv.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Mordecai EA, Cohen JM, Evans MV, Gudapati P, Johnson LR, Lippi CA, Miazgowicz K, Murdock CC, Rohr JR, Ryan SJ, Savage VM, Shocket MS, Stewart Ibarra A, Thomas MB, Weikel, DP, 2017, Detecting the impact of temperature on transmission of Zika, dengue and chikungunya using mechanistic models, PLoS Neglected Tropical Diseases.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Hansen E, Woods RJ, Read AF, 2017, How to Use a Chemotherapeutic Agent When Resistance to It Threatens the Patient, PLoS Biology.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Kennedy DA, Cairns C, Jones MJ, Bell AS, Salathe RM, Baigent SJ, Nair VK, Dunn PA, Read AF, 2017, Industry-wide surveillance of Marek's disease virus on commercial poultry farms, Avian Diseases.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Beck-Johnson LM, Nelson WA, Paaijmans WA, Read AF, Thomas MB, Bjornstad ON, 2017, The importance of temperature fluctuations in understanding mosquito population dynamics and malaria risk, Open Science.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Thomas S, Ravishankaran S, Justin, NAJA, Asokan, A, Mathai MT, Valecha N, Montgomery J, Thomas MB, Eapen A, 2017, Resting and feeding preferences of Anopheles stephensi in an urban setting, perennial for malaria, Malaria Journal.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Kerr PJ, Cattadori IM, Rogers MB, Fitch A, Geber A, Liu J, Sim DG, Boag B, Eden JS, Ghedin E, Read AF, Holmes EC, 2017, Genomic and phenotypic characterization of myxoma virus from Great Britain reveals multiple evolutionary pathways distinct from those in Australia, PLos Pathogens. Kennedy DA, Read AF, 2017, Why does drug resistance readily evolve but vaccine resistance does not?, Proceedings of the Royal Society of London B.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Wale N, Sim DG, Read AF, 2017, A nutrient mediates intraspecific competition between rodent malaria parasites in vivo, Proceedings of the Royal Society of London B.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2017 Citation: Kerr PJ, Cattadori IM, Liu J, Sim DF, Dodds JW, Brooks JW, Kennett MJ, Holmes EC, Read AF, 2017, Next step in the ongoing arms race between myxoma virus and wild rabbits in Australia is a novel disease phenotype, Proceedings of the National Academy of Sciences.


Progress 07/01/16 to 09/30/16

Outputs
Target Audience:The target audience during the two month reporting period is the same as that for the entire period. We are targeting diverse stakeholders ranging from other scientists (who build upon or work) to pest management specialists, policy makers and educators interested in the public dissemination of knowledge. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals?In the next reporting period each of the five labs will work seperately and jointly to better determine the co-evolutionary relationships between insects and their pests/parasites and to use that knowledge in an applied framework.

Impacts
What was accomplished under these goals? The goal of this project is to build upon previous work at the Depatment of Entomology, Penn State on insects and pathogens in disease control. The current project aims to consider the relationship between insects and pests/parasites in a broader evolutionary approach in addition to the applied aspect. This integration will, we think, increase the effectiveness with which we can tailor control strategies as well as more fully understand the reasons why some insects becomes pests. In addition the work represents an effective integration of applied and fundamental work that we think will lead to serendipitous discoveries that will lead to synergisms, better control of pests and a better understanding of the co-evolutionary dynamics between insects and the pathogens/pests that exploit them. This project began August 1st 2016 and this progress report covers the time until September 30th 2016. In the course of these two months multiple activities occurred in line with the overall goals of the project, which is to better understand the interactions between insects and pathogen/parasites. Each of the five labs involved (Hughes, Cui, Bjornstad, Thomas and Read) have actively worked on this project but the truncated time period (2 months) doesnt allow for specific accomplishments to be highlighted.

Publications