{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T12:35:55Z","timestamp":1791894955652,"version":"4.3.4"},"reference-count":74,"publisher":"Public Library of Science (PLoS)","issue":"12","license":[{"start":{"date-parts":[[2022,12,15]],"date-time":"2022-12-15T00:00:00Z","timestamp":1671062400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/publicdomain\/zero\/1.0\/"}],"funder":[{"name":"NIH"},{"DOI":"10.13039\/100006492","name":"Division of Intramural Research, National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["ZIA AI000796-25"],"award-info":[{"award-number":["ZIA AI000796-25"]}],"id":[{"id":"10.13039\/100006492","id-type":"DOI","asserted-by":"publisher"}]},{"name":"National Science Foundation","award":["2109828"],"award-info":[{"award-number":["2109828"]}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:p><jats:italic>Yersinia pestis<\/jats:italic>, the bacterial agent of plague, is enzootic in many parts of the world within wild rodent populations and is transmitted by different flea vectors. The ecology of plague is complex, with rodent hosts exhibiting varying susceptibilities to overt disease and their fleas exhibiting varying levels of vector competence. A long-standing question in plague ecology concerns the conditions that lead to occasional epizootics among susceptible rodents. Many factors are involved, but a major one is the transmission efficiency of the flea vector. In this study, using <jats:italic>Oropsylla montana<\/jats:italic> (a ground squirrel flea that is a major plague vector in the western United States), we comparatively quantified the efficiency of the two basic modes of flea-borne transmission. Transmission efficiency by the early-phase mechanism was strongly affected by the host blood source. Subsequent biofilm-dependent transmission by blocked fleas was less influenced by host blood and was more efficient. Mathematical modeling predicted that early-phase transmission could drive an epizootic only among highly susceptible rodents with certain blood characteristics, but that transmission by blocked <jats:italic>O<\/jats:italic>. <jats:italic>montana<\/jats:italic> could do so in more resistant hosts irrespective of their blood characteristics. The models further suggested that for most wild rodents, exposure to sublethal doses of <jats:italic>Y<\/jats:italic>. <jats:italic>pestis<\/jats:italic> transmitted during the early phase may restrain rapid epizootic spread by increasing the number of immune, resistant individuals in the population.<\/jats:p>","DOI":"10.1371\/journal.ppat.1010996","type":"journal-article","created":{"date-parts":[[2022,12,15]],"date-time":"2022-12-15T18:32:06Z","timestamp":1671129126000},"page":"e1010996","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":13,"title":["A Role for Early-Phase Transmission in the Enzootic Maintenance of Plague"],"prefix":"10.1371","volume":"18","author":[{"given":"Cedar L.","family":"Mitchell","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ashley R.","family":"Schwarzer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ad\u00e9la\u00efde","family":"Miarinjara","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Clayton O.","family":"Jarrett","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Angela D.","family":"Luis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6240-7936","authenticated-orcid":true,"given":"B. Joseph","family":"Hinnebusch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2022,12,15]]},"reference":[{"key":"ppat.1010996.ref001","first-page":"213","volume-title":"Recovery of the black-footed ferret, progress and continuing challenges","author":"KL Gage","year":"2006"},{"issue":"2","key":"ppat.1010996.ref002","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1051\/vetres:2008039","article-title":"Adaptive strategies of Yersinia pestis to persist during inter-epizootic and epizootic periods","volume":"40","author":"RJ Eisen","year":"2009","journal-title":"Vet Res"},{"key":"ppat.1010996.ref003","first-page":"85","article-title":"A review of plague persistence with special emphasis on fleas","volume":"46","author":"J Wimsatt","year":"2009","journal-title":"J Vector Borne Dis"},{"key":"ppat.1010996.ref004","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1007\/978-94-024-0890-4_5","article-title":"Ecology of Yersinia pestis and the epidemiology of plague","volume":"918","author":"VM Dubyanskiy","year":"2016","journal-title":"Adv Exp Med Biol"},{"issue":"10","key":"ppat.1010996.ref005","doi-asserted-by":"crossref","first-page":"e0004949","DOI":"10.1371\/journal.pntd.0004949","article-title":"Zoonoses as ecological entities: a case review of plague","volume":"10","author":"CG Zeppelini","year":"2016","journal-title":"PLoS Negl Trop Dis"},{"key":"ppat.1010996.ref006","doi-asserted-by":"crossref","first-page":"903","DOI":"10.1038\/35038073","article-title":"Metapopulation dynamics of bubonic plague","volume":"407","author":"MJ Keeling","year":"2000","journal-title":"Nature"},{"key":"ppat.1010996.ref007","doi-asserted-by":"crossref","first-page":"634","DOI":"10.1038\/nature07053","article-title":"The abundance threshold for plague as a critical percolation phenomenon","volume":"454","author":"S Davis","year":"2008","journal-title":"Nature"},{"key":"ppat.1010996.ref008","doi-asserted-by":"crossref","first-page":"1655","DOI":"10.1111\/j.1539-6924.2009.01309.x","article-title":"Threshold conditions for the persistence of plague transmission in urban rats","volume":"29","author":"DP Durham","year":"2009","journal-title":"Risk Anal"},{"key":"ppat.1010996.ref009","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1111\/j.1461-0248.2012.01767.x","article-title":"A curve of thresholds governs plague epizootics in Central Asia","volume":"15","author":"J Reijniers","year":"2012","journal-title":"Ecol Lett"},{"key":"ppat.1010996.ref010","doi-asserted-by":"crossref","first-page":"14247","DOI":"10.1073\/pnas.1002826107","article-title":"Plague outbreaks in prairie dog populations explained by percolation thresholds of alternate host abundance","volume":"107","author":"DJ Salkeld","year":"2010","journal-title":"Proc Natl Acad Sci USA"},{"issue":"5","key":"ppat.1010996.ref011","doi-asserted-by":"crossref","first-page":"e1003039","DOI":"10.1371\/journal.pcbi.1003039","article-title":"Host resistance, population structure and the long-term persistence of bubonic plague: contributions of a modelling approach in the Malagasy focus","volume":"9","author":"F Gascuel","year":"2013","journal-title":"PLoS Comput Biol"},{"issue":"11","key":"ppat.1010996.ref012","doi-asserted-by":"crossref","first-page":"e2382","DOI":"10.1371\/journal.pntd.0002382","article-title":"Understanding the persistence of plague foci in Madagascar","volume":"7","author":"V Andrianaivoarimanana","year":"2013","journal-title":"PLoS Negl Trop Dis"},{"key":"ppat.1010996.ref013","first-page":"774","article-title":"Further notes on the mechanism of the transmission of plague by fleas","volume":"14","author":"AW Bacot","year":"1915","journal-title":"J Hygiene Plague Suppl 4"},{"key":"ppat.1010996.ref014","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1146\/annurev-micro-090816-093521","article-title":"\"Fleaing\" the plague: Adaptations of Yersinia pestis to its insect vector that lead to transmission","volume":"71","author":"BJ Hinnebusch","year":"2017","journal-title":"Annu Rev Microbiol"},{"key":"ppat.1010996.ref015","first-page":"423","article-title":"Observations on the mechanism of the transmission of plague by fleas","volume":"13","author":"AW Bacot","year":"1914","journal-title":"J Hygiene Plague Suppl 3"},{"issue":"1","key":"ppat.1010996.ref016","doi-asserted-by":"crossref","first-page":"e1006859","DOI":"10.1371\/journal.ppat.1006859","article-title":"Infectious blood source alters early foregut infection and regurgitative transmission of Yersinia pestis by rodent fleas","volume":"14","author":"DM Bland","year":"2018","journal-title":"PLoS Pathog"},{"key":"ppat.1010996.ref017","doi-asserted-by":"crossref","first-page":"2216","DOI":"10.1099\/mic.0.037952-0","article-title":"Biofilm formation is not required for early-phase transmission of Yersinia pestis","volume":"156","author":"SM Vetter","year":"2010","journal-title":"Microbiology"},{"issue":"4","key":"ppat.1010996.ref018","doi-asserted-by":"crossref","first-page":"e1008440","DOI":"10.1371\/journal.ppat.1008440","article-title":"A refined model of how Yersinia pestis produces a transmissible infection in its flea vector","volume":"16","author":"A Dewitte","year":"2020","journal-title":"PLoS Pathog"},{"key":"ppat.1010996.ref019","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1146\/annurev-ento-120710-100717","article-title":"Transmission of flea-borne zoonotic agents","volume":"57","author":"RJ Eisen","year":"2012","journal-title":"Ann Rev Entomol"},{"key":"ppat.1010996.ref020","doi-asserted-by":"crossref","first-page":"15380","DOI":"10.1073\/pnas.0606831103","article-title":"Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics","volume":"103","author":"RJ Eisen","year":"2006","journal-title":"Proc Natl Acad Sci USA"},{"key":"ppat.1010996.ref021","doi-asserted-by":"crossref","first-page":"1183","DOI":"10.1093\/jme\/tjv128","article-title":"The role of early-phase transmission in the spread of Yersinia pestis","volume":"52","author":"RJ Eisen","year":"2015","journal-title":"J Med Entomol"},{"key":"ppat.1010996.ref022","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1603\/033.046.0403","article-title":"Studies of vector competency and efficiency of North American fleas for Yersinia pestis: state of the field and future research needs","volume":"46","author":"RJ Eisen","year":"2009","journal-title":"J Med Entomol"},{"issue":"1","key":"ppat.1010996.ref023","doi-asserted-by":"crossref","first-page":"e0005276","DOI":"10.1371\/journal.pntd.0005276","article-title":"Comparative ability of Oropsylla montana and Xenopsylla cheopis fleas to transmit Yersinia pestis by two different mechanisms","volume":"11","author":"BJ Hinnebusch","year":"2017","journal-title":"PLoS Negl Trop Dis"},{"key":"ppat.1010996.ref024","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1126\/science.273.5273.367","article-title":"Role of the Yersinia pestis hemin storage (hms) locus in the transmission of plague by fleas","volume":"273","author":"BJ Hinnebusch","year":"1996","journal-title":"Science"},{"key":"ppat.1010996.ref025","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1089\/vbz.2012.1017","article-title":"Effects of low-temperature flea maintenance on the transmission of Yersinia pestis by Oropsylla montana","volume":"13","author":"SK Williams","year":"2013","journal-title":"Vector Borne Zoonotic Dis"},{"key":"ppat.1010996.ref026","doi-asserted-by":"crossref","first-page":"2517","DOI":"10.1099\/mic.0.082123-0","article-title":"Yersinia murine toxin is not required for early-phase transmission of Yersinia pestis by Oropsylla montana (Siphonaptera: Ceratophyllidae) or Xenopsylla cheopis (Siphonaptera: Pulicidae)","volume":"160","author":"TL Johnson","year":"2014","journal-title":"Microbiology"},{"issue":"12","key":"ppat.1010996.ref027","doi-asserted-by":"crossref","first-page":"e1009092","DOI":"10.1371\/journal.ppat.1009092","article-title":"Comparison of the transmission efficiency and plague progression dynamics associated with two mechanisms by which fleas transmit Yersinia pestis","volume":"16","author":"CF Bosio","year":"2020","journal-title":"PLoS Pathog"},{"key":"ppat.1010996.ref028","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1017\/S0022172400014042","article-title":"Sylvatic plague studies. The vector efficiency of nine species of fleas compared with Xenopsylla cheopis","volume":"45","author":"AL Burroughs","year":"1947","journal-title":"J Hygiene"},{"key":"ppat.1010996.ref029","doi-asserted-by":"crossref","first-page":"1907","DOI":"10.1086\/429931","article-title":"Poor vector competence of fleas and the evolution of hypervirulence in Yersinia pestis","volume":"191","author":"EA Lorange","year":"2005","journal-title":"J Inf Dis"},{"key":"ppat.1010996.ref030","doi-asserted-by":"crossref","first-page":"933","DOI":"10.1093\/jmedent\/45.5.933","article-title":"Source of host blood affects prevalence of infection and bacterial loads of Yersinia pestis in fleas","volume":"45","author":"RJ Eisen","year":"2008","journal-title":"J Med Entomol"},{"key":"ppat.1010996.ref031","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1017\/S0031182000018321","article-title":"Sylvatic plague studies X. Survival of rodent fleas in the laboratory","volume":"43","author":"AL Burroughs","year":"1953","journal-title":"Parasitology"},{"key":"ppat.1010996.ref032","volume-title":"Janeway\u2019s Immunobiology","author":"K Murphy","year":"2012","edition":"8"},{"key":"ppat.1010996.ref033","doi-asserted-by":"crossref","first-page":"552","DOI":"10.4269\/ajtmh.2000.62.552","article-title":"Quantitative competitive PCR as a technique for exploring flea-Yersina pestis dynamics","volume":"62","author":"DM Engelthaler","year":"2000","journal-title":"Am J Trop Med Hyg"},{"key":"ppat.1010996.ref034","doi-asserted-by":"crossref","first-page":"2052","DOI":"10.1128\/IAI.72.4.2052-2056.2004","article-title":"Flea-borne transmission model to evaluate vaccine efficacy against naturally acquired bubonic plague","volume":"72","author":"CO Jarrett","year":"2004","journal-title":"Infect Immun"},{"key":"ppat.1010996.ref035","doi-asserted-by":"crossref","first-page":"5526","DOI":"10.1073\/pnas.0509544103","article-title":"Role of the Yersinia pestis plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea-borne plague","volume":"103","author":"F Sebbane","year":"2006","journal-title":"Proc Natl Acad Sci USA"},{"key":"ppat.1010996.ref036","doi-asserted-by":"crossref","first-page":"1222","DOI":"10.1128\/IAI.00950-08","article-title":"The Yersinia pestis caf1M1A1 fimbrial capsule operon promotes transmission by flea bite in a mouse model of bubonic plague","volume":"77","author":"F Sebbane","year":"2009","journal-title":"Infect Immun"},{"issue":"12","key":"ppat.1010996.ref037","doi-asserted-by":"crossref","first-page":"e14379","DOI":"10.1371\/journal.pone.0014379","article-title":"Role of the Yersinia pestis yersiniabactin iron acquisition system in the incidence of flea-borne plague","volume":"5","author":"F Sebbane","year":"2010","journal-title":"PloS One"},{"issue":"9","key":"ppat.1010996.ref038","doi-asserted-by":"crossref","first-page":"e3196","DOI":"10.1371\/journal.pntd.0003196","article-title":"Evaluation of the murine immune response to Xenopsylla cheopis flea saliva and its effect on transmission of Yersinia pestis","volume":"8","author":"CF Bosio","year":"2014","journal-title":"PLoS Negl Trop Dis"},{"issue":"11","key":"ppat.1010996.ref039","doi-asserted-by":"crossref","first-page":"e0141103","DOI":"10.1371\/journal.pone.0141103","article-title":"Dynamics of a tularemia outbreak in a closely monitored free-roaming population of wild house mice","volume":"10","author":"A Dobay","year":"2015","journal-title":"PloS One"},{"key":"ppat.1010996.ref040","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1093\/jmedent\/44.4.678","article-title":"Early-phase transmission of Yersinia pestis by unblocked Xenopsylla cheopis (Siphonaptera: Pulicidae) is as efficient as transmission by blocked fleas","volume":"44","author":"RJ Eisen","year":"2007","journal-title":"J Med Entomol"},{"key":"ppat.1010996.ref041","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1007\/s10393-008-0165-1","article-title":"Transmission efficiency of two flea species (Oropsylla tuberculata cynomuris and Oropsylla hirsuta) involved in plague epizootics among prairie dogs","volume":"5","author":"AP Wilder","year":"2008","journal-title":"EcoHealth"},{"issue":"47","key":"ppat.1010996.ref042","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1098\/rsif.2009.0386","article-title":"The construction of next-generation matrices for compartmental epidemic models","volume":"7","author":"O Diekmann","year":"2010","journal-title":"J R Soc Interface"},{"key":"ppat.1010996.ref043","doi-asserted-by":"crossref","first-page":"674","DOI":"10.1093\/jme\/tjw004","article-title":"Infection prevalence, bacterial loads, and transmission efficiency in Oropsylla montana (Siphonaptera: Ceratophyllidae) one day after exposure to varying concentrations of Yersinia pestis in blood","volume":"53","author":"KA Boegler","year":"2016","journal-title":"J Med Entomol"},{"key":"ppat.1010996.ref044","volume-title":"Plague in the western part of the United States","author":"CR Eskey","year":"1940"},{"key":"ppat.1010996.ref045","doi-asserted-by":"crossref","first-page":"6236","DOI":"10.1073\/pnas.0510090103","article-title":"Classic flea-borne transmission does not drive plague epizootics in prairie dogs","volume":"103","author":"CT Webb","year":"2006","journal-title":"Proc Natl Acad Sci USA"},{"key":"ppat.1010996.ref046","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1089\/vbz.2007.0181","article-title":"Oropsylla hirsuta (Siphonaptera: Ceratophyllidae) can support plague epizootics in black-tailed prairie dogs (Cynomys ludovicianus) by early-phase transmission of Yersinia pestis","volume":"8","author":"AP Wilder","year":"2008","journal-title":"Vector Borne Zoonotic Dis"},{"key":"ppat.1010996.ref047","doi-asserted-by":"crossref","first-page":"1053","DOI":"10.1093\/jme\/tjac021","article-title":"Reevaluation of the role of blocked Oropsylla hirsuta prairie dog fleas (Siphonaptera: Ceratophyllidae) in Yersinia pestis transmission","volume":"59","author":"A Miarinjara","year":"2022","journal-title":"J Med Entomol"},{"key":"ppat.1010996.ref048","doi-asserted-by":"crossref","first-page":"1058","DOI":"10.4269\/ajtmh.1956.5.1058","article-title":"Studies on Pasteurella pestis in fleas. V. The experimental plague-vector efficiency of wild rodent fleas compared with Xenopsylla cheopis, together with observations on the influence of temperature","volume":"5","author":"L Kartman","year":"1956","journal-title":"Am J Trop Med Hyg"},{"key":"ppat.1010996.ref049","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1093\/infdis\/72.1.18","article-title":"Sylvatic plague studies. II. The fate of Pasteurella pestis in the flea","volume":"72","author":"JR Douglas","year":"1943","journal-title":"J Inf Dis"},{"key":"ppat.1010996.ref050","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/infdis\/77.1.1","article-title":"Sylvatic plague studies V. The determination of vector efficiency","volume":"77","author":"CM Wheeler","year":"1945","journal-title":"J Inf Dis"},{"key":"ppat.1010996.ref051","doi-asserted-by":"crossref","first-page":"1997","DOI":"10.1093\/jme\/tjaa113","article-title":"Influence of temperature on development of Yersinia pestis foregut blockage in Xenopsylla cheopis (Siphonaptera: Pulicidae) and Oropsylla montana (Siphonaptera: Ceratophyllidae)","volume":"57","author":"A Lemon","year":"2020","journal-title":"J Med Entomol"},{"key":"ppat.1010996.ref052","doi-asserted-by":"crossref","first-page":"672","DOI":"10.1093\/jmedent\/44.4.672","article-title":"Temporal dynamics of early-phase transmission of Yersinia pestis by unblocked fleas: secondary infectious feeds prolong efficient transmission by Oropsylla montana (Siphonaptera: Ceratophyllidae)","volume":"44","author":"RJ Eisen","year":"2007","journal-title":"J Med Entomol"},{"key":"ppat.1010996.ref053","doi-asserted-by":"crossref","first-page":"1160","DOI":"10.1093\/jmedent\/45.6.1160","article-title":"Demonstration of early-phase transmission of Yersinia pestis by the mouse flea, Aetheca wagneri (Siphonaptera: Ceratophylidae), and implications for the role of deer mice as enzootic reservoirs","volume":"45","author":"RJ Eisen","year":"2008","journal-title":"J Med Entomol"},{"issue":"7","key":"ppat.1010996.ref054","doi-asserted-by":"crossref","first-page":"e22498","DOI":"10.1371\/journal.pone.0022498","article-title":"Transmission shifts underlie variability in population responses to Yersinia pestis infection","volume":"6","author":"MG Buhnerkempe","year":"2011","journal-title":"PloS One"},{"key":"ppat.1010996.ref055","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1016\/S0014-4894(56)80003-9","article-title":"Studies on Pasteurella pestis in fleas. IV. Experimental blocking of Xenopsylla vexabilis hawaiiensis and Xenopsylla cheopis with an avirulent strain","volume":"5","author":"L Kartman","year":"1956","journal-title":"Exp Parasitol"},{"key":"ppat.1010996.ref056","doi-asserted-by":"crossref","first-page":"317","DOI":"10.4269\/ajtmh.1958.7.317","article-title":"Studies on Pasteurella pestis in fleas VII. The plague-vector efficiency of Hystrichopsylla linsdalei compared with Xenopsylla cheopis under experimental conditions","volume":"7","author":"L Kartman","year":"1958","journal-title":"Am J Trop Med Hyg"},{"key":"ppat.1010996.ref057","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1126\/science.1069972","article-title":"Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector","volume":"296","author":"BJ Hinnebusch","year":"2002","journal-title":"Science"},{"issue":"1","key":"ppat.1010996.ref058","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1186\/s13071-020-04207-x","article-title":"Biovar-related differences apparent in the flea foregut colonization phenotype of distinct Yersinia pestis strains do not impact transmission efficiency","volume":"13","author":"A Lemon","year":"2020","journal-title":"Parasit Vectors"},{"key":"ppat.1010996.ref059","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1111\/j.1749-6632.1958.tb35421.x","article-title":"New knowledge on the ecology of sylvatic plague","volume":"70","author":"L Kartman","year":"1958","journal-title":"Ann N Y Acad Sci"},{"key":"ppat.1010996.ref060","volume-title":"Plague","author":"R Pollitzer","year":"1954"},{"key":"ppat.1010996.ref061","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1099\/13500872-145-1-197","article-title":"The haemin storage (Hms+) phenotype of Yersinia pestis is not essential for the pathogenesis of bubonic plague in mammals","volume":"145","author":"JW Lillard","year":"1999","journal-title":"Microbiology"},{"key":"ppat.1010996.ref062","doi-asserted-by":"crossref","first-page":"578","DOI":"10.1016\/j.chom.2014.04.003","article-title":"Retracing the evolutionary path that led to flea-borne transmission of Yersinia pestis","volume":"15","author":"YC Sun","year":"2014","journal-title":"Cell Host Microbe"},{"key":"ppat.1010996.ref063","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1002\/evl3.111","article-title":"To block or not to block: The adaptive manipulation of plague transmission","volume":"3","author":"S Gandon","year":"2019","journal-title":"Evol Lett"},{"key":"ppat.1010996.ref064","first-page":"3","article-title":"Studies upon plague in ground squirrels","volume":"43","author":"GW McCoy","year":"1911","journal-title":"Publ Hlth Bull"},{"key":"ppat.1010996.ref065","doi-asserted-by":"crossref","first-page":"618","DOI":"10.1093\/infdis\/140.4.618","article-title":"Experimental plague in the California ground squirrel","volume":"140","author":"JE Williams","year":"1979","journal-title":"J Infect Dis"},{"key":"ppat.1010996.ref066","doi-asserted-by":"crossref","first-page":"205","DOI":"10.7589\/0090-3558-21.3.205","article-title":"Experimental plague in rock squirrels, Spermophilus variegatus (Erxleben)","volume":"21","author":"TJ Quan","year":"1985","journal-title":"J Wildl Dis"},{"issue":"1","key":"ppat.1010996.ref067","doi-asserted-by":"crossref","first-page":"e165","DOI":"10.1371\/journal.pone.0000165","article-title":"Epidemic enhancement in partially immune populations","volume":"2","author":"JRC Pulliam","year":"2007","journal-title":"PloS One"},{"key":"ppat.1010996.ref068","doi-asserted-by":"crossref","first-page":"949","DOI":"10.1016\/j.pt.2019.08.004","article-title":"Multiple blood feeding: a force multiplier for transmission","volume":"35","author":"RE Tedrow","year":"2019","journal-title":"Trends Parasitol"},{"key":"ppat.1010996.ref069","doi-asserted-by":"crossref","first-page":"1980","DOI":"10.1128\/JCM.37.6.1980-1984.1999","article-title":"PCR detection of Yersinia pestis in fleas: comparison with mouse inoculation","volume":"37","author":"DM Engelthaler","year":"1999","journal-title":"J Clin Microbiol"},{"issue":"2","key":"ppat.1010996.ref070","doi-asserted-by":"crossref","first-page":"e0004413","DOI":"10.1371\/journal.pntd.0004413","article-title":"Feeding behavior modulates biofilm-mediated transmission of Yersinia pestis by the cat flea, Ctenocephalides felis","volume":"10","author":"DM Bland","year":"2016","journal-title":"PLoS Negl Trop Dis"},{"key":"ppat.1010996.ref071","article-title":"Methods in Flea Research","author":"DM Bland","year":"2017","journal-title":"BEI Resources"},{"key":"ppat.1010996.ref072","volume-title":"The Biomathematics of Malaria","author":"NTJ Bailey","year":"1982"},{"issue":"4","key":"ppat.1010996.ref073","doi-asserted-by":"crossref","first-page":"e1002588","DOI":"10.1371\/journal.ppat.1002588","article-title":"Ross, Macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens","volume":"8","author":"DL Smith","year":"2012","journal-title":"PLoS Pathog"},{"key":"ppat.1010996.ref074","volume-title":"R: A language and environment for statistical computing","author":"R Core Team","year":"2019"}],"container-title":["PLOS Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1010996","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,15]],"date-time":"2022-12-15T18:32:52Z","timestamp":1671129172000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1010996"}},"subtitle":[],"editor":[{"given":"Igor E.","family":"Brodsky","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2022,12,15]]},"references-count":74,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2022,12,15]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.ppat.1010996","relation":{},"ISSN":["1553-7374"],"issn-type":[{"value":"1553-7374","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,12,15]]}}}