{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T05:38:33Z","timestamp":1790660313566,"version":"4.1.0"},"reference-count":121,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2021,9,12]],"date-time":"2021-09-12T00:00:00Z","timestamp":1631404800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Mosquito-borne West Nile virus (WNV) is the causative agent of West Nile disease in humans, horses, and some bird species. Since the initial introduction of WNV to the United States (US), approximately 30,000 horses have been impacted by West Nile neurologic disease and hundreds of additional horses are infected each year. Research describing the drivers of West Nile disease in horses is greatly needed to better anticipate the spatial and temporal extent of disease risk, improve disease surveillance, and alleviate future economic impacts to the equine industry and private horse owners. To help meet this need, we integrated techniques from spatiotemporal epidemiology, eco-phylogenetics, and distributional ecology to assess West Nile disease risk in horses throughout the contiguous US. Our integrated approach considered horse abundance and virus exposure, vector and host distributions, and a variety of extrinsic climatic, socio-economic, and environmental risk factors. Birds are WNV reservoir hosts, and therefore we quantified avian host community dynamics across the continental US to show intra-annual variability in host phylogenetic structure and demonstrate host phylodiversity as a mechanism for virus amplification in time and virus dilution in space. We identified drought as a potential amplifier of virus transmission and demonstrated the importance of accounting for spatial non-stationarity when quantifying interaction between disease risk and meteorological influences such as temperature and precipitation. Our results delineated the timing and location of several areas at high risk of West Nile disease and can be used to prioritize vaccination programs and optimize virus surveillance and monitoring.<\/jats:p>","DOI":"10.3390\/v13091811","type":"journal-article","created":{"date-parts":[[2021,9,12]],"date-time":"2021-09-12T21:48:01Z","timestamp":1631483281000},"page":"1811","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["Integrating Spatiotemporal Epidemiology, Eco-Phylogenetics, and Distributional Ecology to Assess West Nile Disease Risk in Horses"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8464-0886","authenticated-orcid":false,"given":"John M.","family":"Humphreys","sequence":"first","affiliation":[{"name":"Pest Management Research Unit, Agricultural Research Service, US Department of Agriculture, Sidney, MT 59270, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Angela M.","family":"Pelzel-McCluskey","sequence":"additional","affiliation":[{"name":"Veterinary Services, Animal and Plant Health Inspection Service (APHIS), US Department of Agriculture, Fort Collins, CO 80526, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lee W.","family":"Cohnstaedt","sequence":"additional","affiliation":[{"name":"Arthropod-Borne Animal Disease Research Unit, Agricultural Research Service, US Department of Agriculture, Manhattan, KS 66502, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7271-725X","authenticated-orcid":false,"given":"Bethany L.","family":"McGregor","sequence":"additional","affiliation":[{"name":"Arthropod-Borne Animal Disease Research Unit, Agricultural Research Service, US Department of Agriculture, Manhattan, KS 66502, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kathryn A.","family":"Hanley","sequence":"additional","affiliation":[{"name":"Department of Biology, New Mexico State University, Las Cruces, NM 88003, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5814-7492","authenticated-orcid":false,"given":"Amy R.","family":"Hudson","sequence":"additional","affiliation":[{"name":"Big Data Initiative and SCINet Program for Scientific Computing, Agricultural Research Service, US Department of Agriculture, Beltsville, MD 20704, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katherine I.","family":"Young","sequence":"additional","affiliation":[{"name":"Department of Biology, New Mexico State University, Las Cruces, NM 88003, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5464-8097","authenticated-orcid":false,"given":"Dannele","family":"Peck","sequence":"additional","affiliation":[{"name":"Northern Plains Climate Hub, US Department of Agriculture, Fort Collins, CO 80526, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9270-8900","authenticated-orcid":false,"given":"Luis L.","family":"Rodriguez","sequence":"additional","affiliation":[{"name":"Plum Island Animal Disease Center, US Department of Agriculture, Orient Point, NY 11957, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5842-8099","authenticated-orcid":false,"given":"Debra P. C.","family":"Peters","sequence":"additional","affiliation":[{"name":"Big Data Initiative and SCINet Program for Scientific Computing, Agricultural Research Service, US Department of Agriculture, Beltsville, MD 20704, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,9,12]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1713","DOI":"10.1086\/322700","article-title":"West Nile Encephalitis: An Emerging Disease in the United States","volume":"33","author":"Strausbaugh","year":"2001","journal-title":"Clin. Infect. Dis."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1475","DOI":"10.1093\/jme\/tjz146","article-title":"West Nile Virus Mosquito Vectors in North America","volume":"56","author":"Rochlin","year":"2019","journal-title":"J. Med. Entomol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Byas, A.D., and Ebel, G.D. (2020). Comparative Pathology of West Nile Virus in Humans and Non-Human Animals. Pathogens, 9.","DOI":"10.3390\/pathogens9010048"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1146\/annurev.ento.54.110807.090510","article-title":"Ecology and geographical expansion of Japanese encephalitis virus","volume":"54","author":"Ritchie","year":"2009","journal-title":"Annu. Rev. Entomol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"4522","DOI":"10.1128\/JVI.02686-13","article-title":"Dynamics of the emergence and establishment of a newly dominant genotype of Japanese encephalitis virus throughout Asia","volume":"88","author":"Schuh","year":"2014","journal-title":"J. Virol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"e232","DOI":"10.1017\/S0950268819001213","article-title":"Usutu virus: A new threat?","volume":"147","author":"Beck","year":"2019","journal-title":"Epidemiol. Infect."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1093\/trstmh\/trx045","article-title":"The ecology and epidemiology of Ross River and Murray Valley encephalitis viruses in Western Australia: Examples of One Health in Action","volume":"111","author":"Mackenzie","year":"2017","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1137","DOI":"10.15585\/mmwr.mm6741a1","article-title":"West Nile Virus and Other Nationally Notifiable Arboviral Diseases\u2014United States, 2017","volume":"67","author":"Curren","year":"2018","journal-title":"MMWR. Morb. Mortal. Wkly. Rep."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Humphreys, J.M., Young, K.I., Cohnstaedt, L.W., Hanley, K.A., and Peters, D.P.C. (2021). Vector Surveillance, Host Species Richness, and Demographic Factors as West Nile Disease Risk Indicators. Viruses, 13.","DOI":"10.3390\/v13050934"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1463","DOI":"10.1093\/jme\/tjz125","article-title":"West Nile Virus: Veterinary Health and Vaccine Development","volume":"56","author":"Bowen","year":"2019","journal-title":"J. Med. Entomol."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Saiz, J.C. (2020). Animal and Human Vaccines against West Nile Virus. Pathogens, 9.","DOI":"10.3390\/pathogens9121073"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1007\/s11250-007-9055-8","article-title":"The economic impact of West Nile virus infection in horses in the North Dakota equine industry in 2002","volume":"40","author":"Mongoh","year":"2008","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Lonker, N.S., Fechner, K., and Abd El Wahed, A. (2020). Horses as a Crucial Part of One Health. Vet. Sci., 7.","DOI":"10.3390\/vetsci7010028"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Ronca, S.E., Ruff, J.C., and Murray, K.O. (2021). A 20-year historical review of West Nile virus since its initial emergence in North America: Has West Nile virus become a neglected tropical disease?. PLoS Negl. Trop. Dis., 15.","DOI":"10.1371\/journal.pntd.0009190"},{"key":"ref_15","unstructured":"APHIS (2021, July 02). USDA, Animal and Plant Health Inspection Service (APHIS), West Nile Virus, Available online: https:\/\/www.aphis.usda.gov\/aphis\/ourfocus\/animalhealth\/animal-disease-information\/equine\/wnv\/west-nile-virus."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1354\/vp.38-4-414","article-title":"Pathologic and Immunohistochemical Findings in Naturally Occurring West Nile Virus Infection in Horses","volume":"38","author":"Cantile","year":"2001","journal-title":"Vet. Pathol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"665","DOI":"10.3201\/eid0704.017412","article-title":"Equine West Nile encephalitis, United States","volume":"7","author":"Ostlund","year":"2001","journal-title":"Emerg. Infect. Dis."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"4608","DOI":"10.1016\/j.vaccine.2011.04.058","article-title":"Protection provided by a recombinant ALVAC\u00ae-WNV vaccine expressing the prM\/E genes of a lineage 1 strain of WNV against a virulent challenge with a lineage 2 strain","volume":"29","author":"Minke","year":"2011","journal-title":"Vaccine"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/j.vetmic.2013.08.013","article-title":"West Nile viral infection of equids","volume":"167","author":"Angenvoort","year":"2013","journal-title":"Vet. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"528","DOI":"10.1186\/s13071-020-04399-2","article-title":"Molecular characterization of the re-emerging West Nile virus in avian species and equids in Israel, 2018, and pathological description of the disease","volume":"13","author":"Schvartz","year":"2020","journal-title":"Parasites Vectors"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.vetmic.2017.11.008","article-title":"West Nile virus in horses during the summer and autumn seasons of 2015 and 2016, Portugal","volume":"212","author":"Barros","year":"2017","journal-title":"Vet. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Bertram, F.M., Thompson, P.N., and Venter, M. (2021). Epidemiology and Clinical Presentation of West Nile Virus Infection in Horses in South Africa, 2016\u20132017. Pathogens, 10.","DOI":"10.3390\/pathogens10010020"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"471","DOI":"10.4269\/ajtmh.1940.s1-20.471","article-title":"A Neurotropic Virus Isolated from the Blood of a Native of Uganda","volume":"s1-20","author":"Smithburn","year":"1940","journal-title":"Am. J. Trop. Med."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1051\/vetres:2004022","article-title":"West Nile virus infection of horses","volume":"35","author":"Wood","year":"2004","journal-title":"Vet. Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1080\/00034983.1963.11686194","article-title":"Natural and Experimental Infection of Egyptian Equines with West Nile Virus","volume":"57","author":"Schmidt","year":"1963","journal-title":"Ann. Trop. Med. Parasitol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2676","DOI":"10.1128\/JCM.41.6.2676-2679.2003","article-title":"Epitope-Blocking Enzyme-Linked Immunosorbent Assays for Detection of West Nile Virus Antibodies in Domestic Mammals","volume":"41","author":"Blitvich","year":"2003","journal-title":"J. Clin. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"51","DOI":"10.5501\/wjv.v1.i2.51","article-title":"West Nile virus: A re-emerging pathogen revisited","volume":"1","author":"Saiz","year":"2012","journal-title":"World J. Virol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1111\/tbed.13043","article-title":"West Nile virus associated with equid encephalitis in Brazil, 2018","volume":"66","author":"Silva","year":"2019","journal-title":"Transbound. Emerg. Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"796","DOI":"10.1038\/s41564-020-0714-0","article-title":"The continued threat of emerging flaviviruses","volume":"5","author":"Pierson","year":"2020","journal-title":"Nat. Microbiol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"31","DOI":"10.2746\/042516400777612080","article-title":"Clinical and neuropathological features of West Nile virus equine encephalomyelitis in Italy","volume":"32","author":"Cantile","year":"2000","journal-title":"Equine Vet. J."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"692","DOI":"10.3201\/eid0704.017417","article-title":"West Nile outbreak in horses in southern France, 2000: The return after 35 years","volume":"7","author":"Murgue","year":"2001","journal-title":"Emerg. Infect. Dis."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"745","DOI":"10.3201\/eid0704.017427","article-title":"West Nile virus outbreak among horses in New York State, 1999 and 2000","volume":"7","author":"Trock","year":"2001","journal-title":"Emerg. Infect. Dis."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"611","DOI":"10.3201\/eid0704.017401","article-title":"West Nile virus: A reemerging global pathogen","volume":"7","author":"Petersen","year":"2001","journal-title":"Emerg. Infect. Dis."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1590\/S1020-49892006000200006","article-title":"West Nile virus activity in Latin America and the Caribbean","volume":"19","author":"Komar","year":"2006","journal-title":"Rev. Panam. Salud Publica = Pan Am. J. Public Health"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1448","DOI":"10.1093\/jme\/tjz151","article-title":"Introduction, Spread, and Establishment of West Nile Virus in the Americas","volume":"56","author":"Kramer","year":"2019","journal-title":"J. Med. Entomol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1111\/j.1749-6632.2001.tb02712.x","article-title":"Experimental Infection of Horses with West Nile Virus and Their Potential to Infect Mosquitoes and Serve as Amplifying Hosts","volume":"951","author":"Bunning","year":"2001","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1007\/s00114-008-0352-5","article-title":"Biogeography of diseases: A framework for analysis","volume":"95","author":"Peterson","year":"2008","journal-title":"Die Naturwissenschaften"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1174","DOI":"10.3389\/fmicb.2016.01174","article-title":"Advances and Limitations of Disease Biogeography Using Ecological Niche Modeling","volume":"7","author":"Escobar","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Lawson, A.B. (2018). Bayesian Disease Mapping: Hierarchical Modeling in Spatial Epidemiology, Chapman and Hall\/CRC Press. [3rd ed.].","DOI":"10.1201\/9781351271769"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1093\/condor\/103.3.599","article-title":"Predicting species\u2019 geographic distributions based on ecological niche modeling","volume":"103","author":"Peterson","year":"2001","journal-title":"Condor"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"102","DOI":"10.4322\/natcon.2012.019","article-title":"Species distribution modeling and ecological niche modeling: Getting the Concepts Right","volume":"10","author":"Peterson","year":"2012","journal-title":"Nat. Conserv."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"100342","DOI":"10.1016\/j.sste.2020.100342","article-title":"Using geospatial methods to measure the risk of environmental persistence of avian influenza virus in South Carolina","volume":"34","author":"Patyk","year":"2020","journal-title":"Spat. Spatio-Temporal Epidemiol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"2592","DOI":"10.1038\/s41598-020-59077-1","article-title":"Waterfowl occurrence and residence time as indicators of H5 and H7 avian influenza in North American Poultry","volume":"10","author":"Humphreys","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Humphreys, J.M., Douglas, D.C., Ramey, A.M., Mullinax, J.M., Soos, C., Link, P., Walther, P., and Prosser, D.J. (2021). The spatial-temporal relationship of blue-winged teal to domestic poultry: Movement state modeling of a highly mobile avian influenza host. J. Appl. Ecol.","DOI":"10.1111\/1365-2664.13963"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"2184","DOI":"10.3201\/eid2412.180382","article-title":"Terrestrial Bird Migration and West Nile Virus Circulation, United States","volume":"24","author":"Swetnam","year":"2018","journal-title":"Emerg. Infect. Dis."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"103701","DOI":"10.1016\/j.actao.2020.103701","article-title":"What do you mean by \u201cniche\u201d? Modern ecological theories are not coherent on rhetoric about the niche concept","volume":"110","author":"Sales","year":"2021","journal-title":"Acta Oecologica"},{"key":"ref_47","first-page":"1","article-title":"Interpretation of Models of Fundamental Ecological Niches and Species\u2019 Distributional Areas","volume":"2","author":"Peterson","year":"2005","journal-title":"Biodivers. Infor."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"166","DOI":"10.20506\/rst.19.1.1201","article-title":"West Nile viral encephalitis","volume":"19","author":"Komar","year":"2000","journal-title":"Rev. Sci. Tech. (Int. Off. Epizoot.)"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"319","DOI":"10.3201\/eid0604.000401","article-title":"Migratory birds and spread of West Nile virus in the Western Hemisphere","volume":"6","author":"Rappole","year":"2000","journal-title":"Emerg. Infect. Dis."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1089\/153036603322662192","article-title":"Serologic evidence of West Nile Virus infection in birds, Tamaulipas State, M\u00e9xico","volume":"3","author":"Blitvich","year":"2003","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"311","DOI":"10.3201\/eid0903.020628","article-title":"Experimental infection of North American birds with the New York 1999 strain of West Nile virus","volume":"9","author":"Komar","year":"2003","journal-title":"Emerg. Infect. Dis."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1089\/vbz.2007.0176","article-title":"West Nile Virus Antibodies in Permanent Resident and Overwintering Migrant Birds in South-Central Kansas","volume":"8","author":"Shelite","year":"2008","journal-title":"Vector-Borne Zoonotic Dis."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Durand, B., Tran, A., Balan\u00e7a, G., and Chevalier, V. (2017). Geographic variations of the bird-borne structural risk of West Nile virus circulation in Europe. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0185962"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"20182178","DOI":"10.1098\/rspb.2018.2178","article-title":"Macroecology of birds potentially susceptible to West Nile virus","volume":"285","author":"Roche","year":"2018","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1002\/ece3.1404","article-title":"Metacommunity and phylogenetic structure determine wildlife and zoonotic infectious disease patterns in time and space","volume":"5","author":"Rico","year":"2015","journal-title":"Ecol. Evol."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Huang, Z.Y.X., de Boer, W.F., van Langevelde, F., Olson, V., Blackburn, T.M., and Prins, H.H.T. (2013). Species\u2019 Life-History Traits Explain Interspecific Variation in Reservoir Competence: A Possible Mechanism Underlying the Dilution Effect. PLoS ONE, 8.","DOI":"10.1371\/annotation\/edc86621-7e9e-4702-b5d3-40cf19ebf731"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1146\/annurev.ecolsys.33.010802.150448","article-title":"Phylogenies and Community Ecology","volume":"33","author":"Webb","year":"2002","journal-title":"Annu. Rev. Ecol. Syst."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"549","DOI":"10.1146\/annurev-phyto-102313-045959","article-title":"The Evolutionary Ecology of Plant Disease: A Phylogenetic Perspective","volume":"54","author":"Gilbert","year":"2016","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"950","DOI":"10.1111\/brv.12380","article-title":"Towards an eco-phylogenetic framework for infectious disease ecology","volume":"93","author":"Pearse","year":"2018","journal-title":"Biol. Rev."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Swaddle, J.P., and Calos, S.E. (2008). Increased avian diversity is associated with lower incidence of human West Nile infection: Observation of the dilution effect. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0002488"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1007\/s00442-008-1224-6","article-title":"Avian host community structure and prevalence of West Nile virus in Chicago, Illinois","volume":"159","author":"Loss","year":"2009","journal-title":"Oecologia"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13071-019-3656-8","article-title":"Predicting West Nile virus transmission in North American bird communities using phylogenetic mixed effects models and eBird citizen science data","volume":"12","author":"Kain","year":"2019","journal-title":"Parasites Vectors"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1186\/s13071-017-1999-6","article-title":"Avian species diversity and transmission of West Nile virus in Atlanta, Georgia","volume":"10","author":"Levine","year":"2017","journal-title":"Parasites Vectors"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"7979","DOI":"10.1073\/pnas.1807106115","article-title":"Species diversity concurrently dilutes and amplifies transmission in a zoonotic host\u2013pathogen system through competing mechanisms","volume":"115","author":"Luis","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_65","unstructured":"Centers for Disease Control and Prevention (CDC) (2019, August 21). ArboNET, Available online: https:\/\/wwwn.cdc.gov\/arbonet."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1177\/096228029800700105","article-title":"Approximate hierarchical modelling of discrete data in epidemiology","volume":"7","author":"Breslow","year":"1998","journal-title":"Stat. Methods Med. Res."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1111\/j.0006-341X.2001.00197.x","article-title":"Detecting interaction between random region and fixed age effects in disease mapping","volume":"57","author":"Dean","year":"2001","journal-title":"Biometrics"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1093\/biomet\/asv064","article-title":"Going off grid: Computationally efficient inference for log-Gaussian Cox processes","volume":"103","author":"Simpson","year":"2016","journal-title":"Biometrika"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1145","DOI":"10.1177\/0962280216660421","article-title":"An intuitive Bayesian spatial model for disease mapping that accounts for scaling","volume":"25","author":"Riebler","year":"2016","journal-title":"Stat. Methods Med. Res."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Bivand, R., and Piras, G. (2015). Comparing Implementations of Estimation Methods for Spatial Econometrics. J. Stat. Softw., 63.","DOI":"10.18637\/jss.v063.i18"},{"key":"ref_71","unstructured":"PRISM (2020, July 12). Total Annual Precipitation and Mean Maximum Temperature Climate Data. Available online: http:\/\/prism.oregonstate.edu."},{"key":"ref_72","unstructured":"Hart, E.M., and Bell, K. (2015). prism: Download Data from the Oregon Prism Project, R Package Version 0.0.6."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.biocon.2013.11.003","article-title":"The eBird enterprise: An integrated approach to development and application of citizen science","volume":"169","author":"Sullivan","year":"2014","journal-title":"Biol. Conserv."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1038\/nature11631","article-title":"The global diversity of birds in space and time","volume":"491","author":"Jetz","year":"2012","journal-title":"Nature"},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Strimas-Mackey, M., Miller, E., and Hochachka, W. (2018). auk: EBird Data Extraction and Processing with AWK, R Package Version 0.3.0.","DOI":"10.32614\/CRAN.package.auk"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"884","DOI":"10.4269\/ajtmh.2012.11-0342","article-title":"Effects of Temperature on Emergence and Seasonality of West Nile Virus in California","volume":"86","author":"Hartley","year":"2012","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1186\/s13071-018-2781-0","article-title":"Association of spring-summer hydrology and meteorology with human West Nile virus infection in West Texas, USA, 2002\u20132016","volume":"11","author":"Ukawuba","year":"2018","journal-title":"Parasites Vectors"},{"key":"ref_78","doi-asserted-by":"crossref","unstructured":"Bouckaert, R., Heled, J., K\u00fchnert, D., Vaughan, T., Wu, C.H., Xie, D., Suchard, M.A., Rambaut, A., and Drummond, A.J. (2014). BEAST 2: A Software Platform for Bayesian Evolutionary Analysis. PLoS Comput. Biol., 10.","DOI":"10.1371\/journal.pcbi.1003537"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1463","DOI":"10.1093\/bioinformatics\/btq166","article-title":"Picante: R tools for integrating phylogenies and ecology","volume":"26","author":"Kembel","year":"2010","journal-title":"Bioinformatics"},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Cadotte, M.W., and Davies, T.J. (2016). Phylogenies in Ecology: A Guide to Concepts and Methods, Princeton University Press.","DOI":"10.23943\/princeton\/9780691157689.001.0001"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"1670","DOI":"10.1111\/j.1523-1739.2006.00555.x","article-title":"Incorporating Evolutionary Measures into Conservation Prioritization","volume":"20","author":"Redding","year":"2006","journal-title":"Conserv. Biol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1031","DOI":"10.1111\/geb.12182","article-title":"A global 1-km consensus land-cover product for biodiversity and ecosystem modelling","volume":"23","author":"Tuanmu","year":"2014","journal-title":"Glob. Ecol. Biogeogr."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.isprsjprs.2013.11.002","article-title":"EarthEnv-DEM90: A nearly-global, void-free, multi-scale smoothed, 90m digital elevation model from fused ASTER and SRTM data","volume":"87","author":"Robinson","year":"2014","journal-title":"ISPRS J. Photogramm. Remote Sens."},{"key":"ref_84","unstructured":"Census Bureau (2019, July 15). Small Area Income and Poverty Estimates (SAIPE) Program, Available online: https:\/\/www.census.gov\/programs-surveys\/saipe.html."},{"key":"ref_85","unstructured":"Recht, H. (2020). censusapi: Retrieve Data from the Census APIs, R Package Version 0.7.1."},{"key":"ref_86","unstructured":"Belsley, D.A., Kuh, E., and Welsch, R.E. (1980). Identifying Influential Data and Sources of Collinearity, John Wiley & Sons."},{"key":"ref_87","unstructured":"Hendricks, J., and Pelzer, B. (2004). Collinearity involving ordered and unordered categorical variables. RC33 Conference in Amsterdam, Available online: https:\/\/www.researchgate.net\/publication\/235994590_Collinearity_involving_ordered_and_unordered_categorical_variables."},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Elliott, P., Wakefield, J., Best, N., and Briggs, D. (2000). Spatial Epidemiology: Methods and Applications, Oxford University Press.","DOI":"10.1093\/acprof:oso\/9780198515326.001.0001"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1111\/j.1467-9868.2008.00700.x","article-title":"Approximate Bayesian inference for latent Gaussian models by using integrated nested Laplace approximations","volume":"71","author":"Rue","year":"2009","journal-title":"J. R. Stat. Soc. Ser. B Stat. Methodol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.csda.2013.04.014","article-title":"Bayesian computing with INLA: New features","volume":"67","author":"Martins","year":"2013","journal-title":"Comput. Stat. Data Anal."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v063.i19","article-title":"Bayesian Spatial Modelling with R-INLA","volume":"63","author":"Lindgren","year":"2015","journal-title":"J. Stat. Softw."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1214\/16-STS576","article-title":"Penalising Model Component Complexity: A Principled, Practical Approach to Constructing Priors","volume":"32","author":"Simpson","year":"2017","journal-title":"Stat. Sci."},{"key":"ref_93","first-page":"382","article-title":"Bayesian Model Averaging: A Tutorial","volume":"14","author":"Hoeting","year":"1999","journal-title":"Stat. Sci."},{"key":"ref_94","doi-asserted-by":"crossref","unstructured":"G\u00f3mez-Rubio, V., Bivand, R.S., and Rue, H. (2020). Bayesian Model Averaging with the Integrated Nested Laplace Approximation. Econometrics, 8.","DOI":"10.3390\/econometrics8020023"},{"key":"ref_95","unstructured":"Csardi, G., and Nepusz, T. (2006). The igraph software package for complex network research. InterJournal Complex Syst., 1695."},{"key":"ref_96","unstructured":"Harris, R. (2021, July 02). Visualizing Multicollinearity Using Igraph. Available online: https:\/\/rpubs.com\/profrichharris\/visual-collinearity."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1175\/1520-0493(1950)078<0001:VOFEIT>2.0.CO;2","article-title":"Verification of forecasts expressed in terms of probability","volume":"78","author":"Brier","year":"1950","journal-title":"Mon. Weather Rev."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1198\/016214506000001437","article-title":"Strictly Proper Scoring Rules, Prediction, and Estimation","volume":"102","author":"Gneiting","year":"2007","journal-title":"J. Am. Stat. Assoc."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"224","DOI":"10.2307\/3543482","article-title":"Timing and Amount of Bird Migration in Relation to Weather: A Review","volume":"30","author":"Richardson","year":"1978","journal-title":"Oikos"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"1497","DOI":"10.1111\/ddi.12960","article-title":"Seasonal occurrence and abundance of dabbling ducks across the continental United States: Joint spatio-temporal modelling for the Genus Anas","volume":"25","author":"Humphreys","year":"2019","journal-title":"Divers. Distrib."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"742","DOI":"10.3201\/eid0704.017426","article-title":"West Nile virus in overwintering Culex mosquitoes, New York City, 2000","volume":"7","author":"Nasci","year":"2001","journal-title":"Emerg. Infect. Dis."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/j.envsoft.2019.06.010","article-title":"A genetic algorithm for identifying spatially-varying environmental drivers in a malaria time series model","volume":"119","author":"Davis","year":"2019","journal-title":"Environ. Model. Softw. Environ. Data News"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1002\/fee.2298","article-title":"Working across space and time: Nonstationarity in ecological research and application","volume":"19","author":"Rollinson","year":"2021","journal-title":"Front. Ecol. Environ."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"659","DOI":"10.3201\/eid1504.080822","article-title":"Links between climate, malaria, and wetlands in the Amazon Basin","volume":"15","author":"Olson","year":"2009","journal-title":"Emerg. Infect. Dis."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1089\/vbz.2006.0590","article-title":"Inter-Annual Associations Between Precipitation and Human Incidence of West Nile Virus in the United States","volume":"7","author":"Landesman","year":"2007","journal-title":"Vector-Borne Zoonotic Dis."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1756-3305-3-19","article-title":"Local impact of temperature and precipitation on West Nile virus infection in Culex species mosquitoes in northeast Illinois, USA","volume":"3","author":"Ruiz","year":"2010","journal-title":"Parasites Vectors"},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"20162078","DOI":"10.1098\/rspb.2016.2078","article-title":"Drought and immunity determine the intensity of west nile virus epidemics and climate change impacts","volume":"284","author":"Paull","year":"2017","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.4269\/ajtmh.14-0737","article-title":"Meteorological conditions associated with increased incidence of west nile virus disease in the United States, 2004\u20132012","volume":"92","author":"Hahn","year":"2015","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_109","unstructured":"Karl, T.R., and Koss, W.J. (1984). Regional and National Monthly, Seasonal, and Annual Temperature Weighted by Area, 1895\u20131983 (Historical Climatology Series 4-3), Technical report; National Climatic Data Center."},{"key":"ref_110","doi-asserted-by":"crossref","unstructured":"Sch\u00f6ning, J.M., Cerny, N., Prohaska, S., Wittenbrink, M.M., Smith, N.H., Bloemberg, G., Pewsner, M., Schiller, I., Origgi, F.C., and Ryser-Degiorgis, M.P. (2013). Surveillance of Bovine Tuberculosis and Risk Estimation of a Future Reservoir Formation in Wildlife in Switzerland and Liechtenstein. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0054253"},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1093\/czoolo\/59.3.427","article-title":"Climate change and infectious diseases of wildlife: Altered interactions between pathogens, vectors and hosts","volume":"59","author":"Gallana","year":"2013","journal-title":"Curr. Zool."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"575","DOI":"10.3201\/eid0806.010417","article-title":"Drought-induced amplification of Saint Louis encephalitis virus, Florida","volume":"8","author":"Shaman","year":"2002","journal-title":"Emerg. Infect. Dis."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1093\/jmedent\/42.2.134","article-title":"Drought-Induced Amplification and Epidemic Transmission of West Nile Virus in Southern Florida","volume":"42","author":"Shaman","year":"2005","journal-title":"J. Med. Entomol."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1603\/ME12035","article-title":"Drought-Induced Amplification of Local and Regional West Nile Virus Infection Rates in New Jersey","volume":"50","author":"Johnson","year":"2013","journal-title":"J. Med. Entomol."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"1867","DOI":"10.1099\/0022-1317-82-8-1867","article-title":"Phylogenetic relationships of flaviviruses correlate with their epidemiology, disease association and biogeography","volume":"82","author":"Gaunt","year":"2001","journal-title":"J. Gen. Virol."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"1695","DOI":"10.1098\/rspb.2008.0284","article-title":"Phylogeny and geography predict pathogen community similarity in wild primates and humans","volume":"275","author":"Davies","year":"2008","journal-title":"Proc. R. Soc. B Biol. Sci."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1126\/science.1188836","article-title":"Host Phylogeny Constrains Cross-Species Emergence and Establishment of Rabies Virus in Bats","volume":"329","author":"Streicker","year":"2010","journal-title":"Science"},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"542","DOI":"10.1038\/nature14372","article-title":"Phylogenetic structure and host abundance drive disease pressure in communities","volume":"520","author":"Parker","year":"2015","journal-title":"Nature"},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1146\/annurev.ecolsys.36.102803.095431","article-title":"Niche Conservatism: Integrating Evolution, Ecology, and Conservation Biology","volume":"36","author":"Wiens","year":"2005","journal-title":"Annu. Rev. Ecol. Evol. Syst."},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"R755","DOI":"10.1152\/ajpregu.1983.245.6.R755","article-title":"Metabolic adjustments of small passerine birds for migration and cold","volume":"245","author":"Dawson","year":"1983","journal-title":"Am. J. Physiol.-Regul. Integr. Comp. Physiol."},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"698","DOI":"10.1111\/brv.12252","article-title":"A guide to phylogenetic metrics for conservation, community ecology and macroecology","volume":"92","author":"Tucker","year":"2017","journal-title":"Biol. Rev."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/9\/1811\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:01:14Z","timestamp":1760166074000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/9\/1811"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,9,12]]},"references-count":121,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2021,9]]}},"alternative-id":["v13091811"],"URL":"https:\/\/doi.org\/10.3390\/v13091811","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,9,12]]}}}