{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,20]],"date-time":"2026-10-20T18:35:42Z","timestamp":1792521342319,"version":"4.5.0"},"reference-count":103,"publisher":"National Academy of Sciences","issue":"51","license":[{"start":{"date-parts":[[2017,6,20]],"date-time":"2017-06-20T00:00:00Z","timestamp":1497916800000},"content-version":"vor","delay-in-days":239,"URL":"http:\/\/www.pnas.org\/site\/misc\/userlicense.xhtml"}],"content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2016,12,20]]},"abstract":"<jats:title>Significance<\/jats:title>\n                  <jats:p>Whereas pathogens are a well-known selective pressure on host immunity, few empirical examples illustrate the coupled dynamics of transmission and evolution. After the arrival of plague in colonial India, a plague-resistant rat phenotype was reported to have become prevalent in the subcontinent\u2019s hardest hit cities. Capitalizing on archival data from these investigations, we identify the evolution of resistance in rats as a driver of observed shifts of seasonal outbreaks in concert with the flea lifecycle and its climatic determinants. Disentangling climatic and evolutionary forcing, our findings\u2014based on century-old observations and experiments by the Indian Plague Commission\u2014substantiate the rapid emergence of host heterogeneity and show how evolutionary responses can buffer host populations against environmentally forced disease dynamics.<\/jats:p>","DOI":"10.1073\/pnas.1604985113","type":"journal-article","created":{"date-parts":[[2016,10,24]],"date-time":"2016-10-24T23:09:50Z","timestamp":1477350590000},"page":"14601-14608","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":23,"title":["Climatic and evolutionary drivers of phase shifts in the plague epidemics of colonial India"],"prefix":"10.1073","volume":"113","author":[{"given":"Joseph A.","family":"Lewnard","sequence":"first","affiliation":[{"name":"Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT 06520;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9890-3907","authenticated-orcid":false,"given":"Jeffrey P.","family":"Townsend","sequence":"additional","affiliation":[{"name":"Department of Biostatistics, Yale School of Public Health, New Haven, CT 06510;"},{"name":"Program in Computational Biology and Bioinformatics, Yale University, New Haven, CT 06511;"},{"name":"Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2016,10,24]]},"reference":[{"key":"e_1_3_3_1_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.pt.2009.02.004"},{"key":"e_1_3_3_2_2","doi-asserted-by":"publisher","DOI":"10.1016\/0169-5347(96)10039-2"},{"key":"e_1_3_3_3_2","doi-asserted-by":"publisher","DOI":"10.1034\/j.1600-0706.2000.880110.x"},{"key":"e_1_3_3_4_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tree.2003.08.013"},{"key":"e_1_3_3_5_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1239401"},{"key":"e_1_3_3_6_2","first-page":"205","article-title":"Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini. I. Patterns of resistance and racial variation in a large host population","volume":"45","author":"Burdon JJ","year":"1991","unstructured":"JJ Burdon, AM Jarosz, Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini. I. Patterns of resistance and racial variation in a large host population. Evolution 45, 205\u2013217 (1991).","journal-title":"Evolution"},{"key":"e_1_3_3_7_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.0022-0477.2004.00925.x"},{"key":"e_1_3_3_8_2","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2009.0011"},{"key":"e_1_3_3_9_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1558-5646.2007.00178.x"},{"key":"e_1_3_3_10_2","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1007\/978-3-642-68635-1_14","volume-title":"Population Biology of Infectious Diseases, Dahlem Workshop Reports","author":"Hamilton WD","year":"1982","unstructured":"WD Hamilton, Pathogens as causes of genetic diversity in their host populations. Population Biology of Infectious Diseases, Dahlem Workshop Reports, eds RM Anderson, RM May (Springer, Berlin), pp. 269\u2013296 (1982)."},{"key":"e_1_3_3_11_2","doi-asserted-by":"publisher","DOI":"10.1071\/ZO9900697"},{"key":"e_1_3_3_12_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0031182000055360"},{"key":"e_1_3_3_13_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.0014-3820.2000.tb00007.x"},{"key":"e_1_3_3_14_2","doi-asserted-by":"publisher","DOI":"10.1006\/jtbi.1999.1009"},{"key":"e_1_3_3_15_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2003.2655"},{"key":"e_1_3_3_16_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.96.8.4478"},{"key":"e_1_3_3_17_2","doi-asserted-by":"publisher","DOI":"10.2307\/2390128"},{"key":"e_1_3_3_18_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1999.0650"},{"key":"e_1_3_3_19_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1998.0471"},{"key":"e_1_3_3_20_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.91.10.4120"},{"key":"e_1_3_3_21_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2003.2497"},{"key":"e_1_3_3_22_2","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2008.0141"},{"key":"e_1_3_3_23_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1461-0248.2006.00995.x"},{"key":"e_1_3_3_24_2","doi-asserted-by":"publisher","DOI":"10.1890\/08-1130.1"},{"key":"e_1_3_3_25_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1215429"},{"key":"e_1_3_3_26_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0022172400037773"},{"key":"e_1_3_3_27_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10393-010-0312-3"},{"key":"e_1_3_3_28_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.meegid.2008.07.005"},{"key":"e_1_3_3_29_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-294X.2010.04633.x"},{"key":"e_1_3_3_30_2","doi-asserted-by":"publisher","DOI":"10.1111\/mec.12115"},{"key":"e_1_3_3_31_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.ento.50.071803.130337"},{"key":"e_1_3_3_32_2","first-page":"213","volume-title":"Recovery of the Black-Footed Ferret: Progress and Continuing Challenges","author":"Gage KL","year":"2005","unstructured":"KL Gage, MY Kosoy, Recent trends in plague ecology. Recovery of the Black-Footed Ferret: Progress and Continuing Challenges, eds JE Roelle, BJ Miller, JL Godbey, DE Biggins (US Geological Survey, Reston, VA), pp. 213\u2013231 (2005)."},{"key":"e_1_3_3_33_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pmed.0050003"},{"key":"e_1_3_3_34_2","doi-asserted-by":"publisher","DOI":"10.1016\/S1473-3099(13)70323-2"},{"key":"e_1_3_3_35_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature10549"},{"key":"e_1_3_3_36_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.220225197"},{"key":"e_1_3_3_37_2","volume-title":"Plague Ports: The Global Urban Impact of Bubonic Plague, 1894-1901","author":"Echenberg M","year":"2010","unstructured":"M Echenberg Plague Ports: The Global Urban Impact of Bubonic Plague, 1894-1901 (New York Univ Press, New York, 2010)."},{"key":"e_1_3_3_38_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2015.10.009"},{"key":"e_1_3_3_39_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature14507"},{"key":"e_1_3_3_40_2","doi-asserted-by":"publisher","DOI":"10.1353\/jwh.2002.0033"},{"key":"e_1_3_3_41_2","doi-asserted-by":"publisher","DOI":"10.1038\/ng.705"},{"key":"e_1_3_3_42_2","first-page":"229","article-title":"LI. The immunity of the wild rat in India","volume":"12","author":"Indian Plague Commission","year":"1912","unstructured":"; Indian Plague Commission, LI. The immunity of the wild rat in India. J Hyg (Lond) 12, 229\u2013265 (1912).","journal-title":"J Hyg (Lond)"},{"key":"e_1_3_3_43_2","first-page":"506","article-title":"VI. A note on the immunity of Bombay rats to subcutaneous injection of plague cultures","volume":"6","author":"Indian Plague Commission","year":"1906","unstructured":"; Indian Plague Commission, VI. A note on the immunity of Bombay rats to subcutaneous injection of plague cultures. J Hyg (Lond) 6, 506\u2013508 (1906).","journal-title":"J Hyg (Lond)"},{"key":"e_1_3_3_44_2","first-page":"71","article-title":"On the present methods of combating the plague","volume":"1","author":"Haffkine WM","year":"1908","unstructured":"WM Haffkine, On the present methods of combating the plague. Proc R Soc Med 1, 71\u201381 (1908).","journal-title":"Proc R Soc Med"},{"key":"e_1_3_3_45_2","doi-asserted-by":"publisher","DOI":"10.1136\/bmj.1.2474.1282"},{"key":"e_1_3_3_46_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0022172400003314"},{"key":"e_1_3_3_47_2","doi-asserted-by":"publisher","DOI":"10.1186\/1476-072X-5-12"},{"key":"e_1_3_3_48_2","doi-asserted-by":"publisher","DOI":"10.1007\/s11252-013-0305-4"},{"key":"e_1_3_3_49_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.286.5441.968"},{"key":"e_1_3_3_50_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1172330"},{"key":"e_1_3_3_51_2","doi-asserted-by":"publisher","DOI":"10.1038\/414716a"},{"key":"e_1_3_3_52_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.287.5453.667"},{"key":"e_1_3_3_53_2","first-page":"221","article-title":"XLIX. Statistics of the occurrence of plague in man and rats in Bombay, 1907-11","volume":"12","author":"Indian Plague Commission","year":"1912","unstructured":"; Indian Plague Commission, XLIX. Statistics of the occurrence of plague in man and rats in Bombay, 1907-11. J Hyg (Lond) 12, 221\u2013226 (1912).","journal-title":"J Hyg (Lond)"},{"key":"e_1_3_3_54_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0022172400043072"},{"key":"e_1_3_3_55_2","first-page":"724","article-title":"XXII. Epidemiological observations in Bombay City","volume":"7","author":"Indian Plague Commission","year":"1907","unstructured":"; Indian Plague Commission, XXII. Epidemiological observations in Bombay City. J Hyg (Lond) 7, 724\u2013798 (1907).","journal-title":"J Hyg (Lond)"},{"key":"e_1_3_3_56_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2000.1272"},{"key":"e_1_3_3_57_2","doi-asserted-by":"publisher","DOI":"10.1038\/35038073"},{"key":"e_1_3_3_58_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1003039"},{"key":"e_1_3_3_59_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2435.2010.01777.x"},{"key":"e_1_3_3_60_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0002-9440(10)62360-7"},{"key":"e_1_3_3_61_2","first-page":"90","volume-title":"The Lifespan of Animals, Volume 5: Colloquia on Ageing","author":"Bourliere F","year":"2009","unstructured":"F Bourliere, Lifespans of mammalian and bird populations in nature. The Lifespan of Animals, Volume 5: Colloquia on Ageing, eds GEW Wolstenholme, M O\u2019Conner (Wiley, New York), pp. 90\u2013103 (2009)."},{"key":"e_1_3_3_62_2","unstructured":"Centers for Disease Control and Prevention (2016) Resources for Clinicians: Plague . Available at www.cdc.gov\/plague\/healthcare\/clinicians.html. Accessed April 13 2016."},{"key":"e_1_3_3_63_2","first-page":"293","article-title":"Epidemiological studies of plague in India. 2. The changing pattern of rodents and fleas in Calcutta and other cities","volume":"23","author":"Seal SC","year":"1960","unstructured":"SC Seal, Epidemiological studies of plague in India. 2. The changing pattern of rodents and fleas in Calcutta and other cities. Bull World Health Organ 23, 293\u2013300 (1960).","journal-title":"Bull World Health Organ"},{"key":"e_1_3_3_64_2","doi-asserted-by":"publisher","DOI":"10.1093\/infdis\/129.Supplement_1.S62"},{"key":"e_1_3_3_65_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1558-5646.1976.tb00911.x"},{"key":"e_1_3_3_66_2","first-page":"300","article-title":"LV. Observations on flea-breeding in Poona","volume":"12","author":"Indian Plague Commission","year":"1912","unstructured":"; Indian Plague Commission, LV. Observations on flea-breeding in Poona. J Hyg (Lond) 12, 300\u2013325 (1912).","journal-title":"J Hyg (Lond)"},{"key":"e_1_3_3_67_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1744-7917.1999.tb00135.x"},{"key":"e_1_3_3_68_2","first-page":"157","article-title":"XLVI. Observations on plague in Eastern Bengal and Assam","volume":"11","author":"Indian Plague Commission","year":"1911","unstructured":"; Indian Plague Commission, XLVI. Observations on plague in Eastern Bengal and Assam. J Hyg (Lond) 11, 157\u2013192 (1911).","journal-title":"J Hyg (Lond)"},{"key":"e_1_3_3_69_2","first-page":"446","article-title":"XXXVI. Observations on rat and human plague in Belgaum","volume":"10","author":"Indian Plague Commission","year":"1910","unstructured":"; Indian Plague Commission, XXXVI. Observations on rat and human plague in Belgaum. J Hyg (Lond) 10, 446\u2013482 (1910).","journal-title":"J Hyg (Lond)"},{"key":"e_1_3_3_70_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0022172400008548"},{"key":"e_1_3_3_71_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0038630"},{"key":"e_1_3_3_72_2","doi-asserted-by":"publisher","DOI":"10.2307\/1380270"},{"key":"e_1_3_3_73_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-7998.1952.tb06316.x"},{"key":"e_1_3_3_74_2","unstructured":"RA Becker JM Chambers AR Wilks The New S Language: A Programming Environment for Data Analysis and Graphics (Wadsworth & Brooks\/Cole Advanced Books & Software London). (1988)."},{"key":"e_1_3_3_75_2","volume-title":"Census of India, 1891: General Report","author":"Baines JA","year":"1893","unstructured":"JA Baines Census of India, 1891: General Report (Eyre and Spottiswoode, London, 1893)."},{"key":"e_1_3_3_76_2","volume-title":"Census of India, 1901: Vol. VI","author":"Gait EA","year":"1902","unstructured":"EA Gait Census of India, 1901: Vol. VI (Government of India, Calcutta, 1902)."},{"key":"e_1_3_3_77_2","volume-title":"Census of India, 1911: Vol. V, Bengala, Bihar y Orissa y Sikkim, Parte I, Informe, Calcuta","author":"O\u2019Malley L","year":"1913","unstructured":"L O\u2019Malley Census of India, 1911: Vol. V, Bengala, Bihar y Orissa y Sikkim, Parte I, Informe, Calcuta (Government of India, Calcutta, 1913)."},{"key":"e_1_3_3_78_2","volume-title":"Census of India, 1911","author":"Mead PJ","year":"1912","unstructured":"PJ Mead, GL MacGregor Census of India, 1911 (Government Central Press, Bombay, 1912)."},{"key":"e_1_3_3_79_2","doi-asserted-by":"publisher","DOI":"10.1093\/biomet\/57.1.97"},{"key":"e_1_3_3_80_2","first-page":"3571","article-title":"Asymptotic equivalence of Bayes cross validation and widely applicable information criterion in singular learning theory","volume":"11","author":"Watanabe S","year":"2010","unstructured":"S Watanabe, Asymptotic equivalence of Bayes cross validation and widely applicable information criterion in singular learning theory. J Mach Learn Res 11, 3571\u20133594 (2010).","journal-title":"J Mach Learn Res"},{"key":"e_1_3_3_81_2","doi-asserted-by":"publisher","DOI":"10.1007\/s11222-013-9416-2"},{"key":"e_1_3_3_82_2","doi-asserted-by":"publisher","DOI":"10.1177\/0049124104268644"},{"key":"e_1_3_3_83_2","first-page":"283","article-title":"Epidemiological studies of plague in India. 1. The present position","volume":"23","author":"Seal SC","year":"1960","unstructured":"SC Seal, Epidemiological studies of plague in India. 1. The present position. Bull World Health Organ 23, 283\u2013300 (1960).","journal-title":"Bull World Health Organ"},{"key":"e_1_3_3_84_2","first-page":"42","article-title":"The yearly variations in plague in India in relation to climate: Forecasting epidemics","volume":"103","author":"Rogers L","year":"1928","unstructured":"L Rogers, The yearly variations in plague in India in relation to climate: Forecasting epidemics. Proc Biol Sci 103, 42\u201372 (1928).","journal-title":"Proc Biol Sci"},{"key":"e_1_3_3_85_2","doi-asserted-by":"publisher","DOI":"10.4269\/ajtmh.2002.66.186"},{"key":"e_1_3_3_86_2","doi-asserted-by":"publisher","DOI":"10.1098\/rsbl.2008.0363"},{"key":"e_1_3_3_87_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pntd.0003155"},{"key":"e_1_3_3_88_2","doi-asserted-by":"publisher","DOI":"10.4269\/ajtmh.2012.11-0569"},{"key":"e_1_3_3_89_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0044431"},{"key":"e_1_3_3_90_2","doi-asserted-by":"publisher","DOI":"10.1089\/vbz.2007.0125"},{"key":"e_1_3_3_91_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1948-7134.2009.00004.x"},{"key":"e_1_3_3_92_2","unstructured":"AM Barnes Surveillance and Control of Bubonic Plague in the United States. Animal Disease in Relation to Animal Conservation . Available at agris.fao.org\/agris-search\/search.do?recordID=US201302197324. Accessed April 13 2016. (1982)."},{"key":"e_1_3_3_93_2","doi-asserted-by":"publisher","DOI":"10.1089\/vbz.2011.0602"},{"key":"e_1_3_3_94_2","doi-asserted-by":"publisher","DOI":"10.1644\/1545-1542(2001)082<0906:IOIPON>2.0.CO;2"},{"key":"e_1_3_3_95_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pntd.0002266"},{"key":"e_1_3_3_96_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0809558105"},{"key":"e_1_3_3_97_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2699.2009.02228.x"},{"key":"e_1_3_3_98_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1749-6632.1958.tb35421.x"},{"key":"e_1_3_3_99_2","doi-asserted-by":"publisher","DOI":"10.1128\/CMR.10.1.35"},{"key":"e_1_3_3_100_2","unstructured":"Centers for Disease Control and Prevention (2016) Maps and Statistics: Plague . Available at https:\/\/www.cdc.gov\/plague\/maps\/index.html. Accessed August 19 2016."},{"key":"e_1_3_3_101_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pntd.0004122"},{"key":"e_1_3_3_102_2","doi-asserted-by":"publisher","DOI":"10.3201\/eid0803.010250"},{"key":"e_1_3_3_103_2","doi-asserted-by":"publisher","DOI":"10.1001\/jama.283.17.2281"}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.1604985113","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,4,13]],"date-time":"2022-04-13T01:05:29Z","timestamp":1649811929000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/full\/10.1073\/pnas.1604985113"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,10,24]]},"references-count":103,"journal-issue":{"issue":"51","published-print":{"date-parts":[[2016,12,20]]}},"alternative-id":["10.1073\/pnas.1604985113"],"URL":"https:\/\/doi.org\/10.1073\/pnas.1604985113","relation":{},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,10,24]]},"assertion":[{"value":"2016-10-24","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}