[Source: Proceedings of the National Academy of Sciences of the United States of American, full page: (LINK). Abstract, edited.]
Climatic and evolutionary drivers of phase shifts in the plague epidemics of colonial India
Joseph A. Lewnard a and Jeffrey P. Townsend b,c,d,1
Author Affiliations: a Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT 06520; b Department of Biostatistics, Yale School of Public Health, New Haven, CT 06510; c Program in Computational Biology and Bioinformatics, Yale University, New Haven, CT 06511; d Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520
Edited by Alan Hastings, University of California, Davis, CA, and approved September 23, 2016 (received for review April 29, 2016)
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’s 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—based on century-old observations and experiments by the Indian Plague Commission—substantiate the rapid emergence of host heterogeneity and show how evolutionary responses can buffer host populations against environmentally forced disease dynamics.
Immune heterogeneity in wild host populations indicates that disease-mediated selection is common in nature. However, the underlying dynamic feedbacks involving the ecology of disease transmission, evolutionary processes, and their interaction with environmental drivers have proven challenging to characterize. Plague presents an optimal system for interrogating such couplings: Yersinia pestis transmission exerts intense selective pressure driving the local persistence of disease resistance among its wildlife hosts in endemic areas. Investigations undertaken in colonial India after the introduction of plague in 1896 suggest that, only a decade after plague arrived, a heritable, plague-resistant phenotype had become prevalent among commensal rats of cities undergoing severe plague epidemics. To understand the possible evolutionary basis of these observations, we developed a mathematical model coupling environmentally forced plague dynamics with evolutionary selection of rats, capitalizing on extensive archival data from Indian Plague Commission investigations. Incorporating increased plague resistance among rats as a consequence of intense natural selection permits the model to reproduce observed changes in seasonal epidemic patterns in several cities and capture experimentally observed associations between climate and flea population dynamics in India. Our model results substantiate Victorian era claims of host evolution based on experimental observations of plague resistance and reveal the buffering effect of such evolution against environmental drivers of transmission. Our analysis shows that historical datasets can yield powerful insights into the transmission dynamics of reemerging disease agents with which we have limited contemporary experience to guide quantitative modeling and inference.
1 To whom correspondence should be addressed. Email: Jeffrey.Townsend@Yale.edu.
Author contributions: J.A.L. and J.P.T. designed research; J.A.L. performed research; J.A.L. and J.P.T. contributed new reagents/analytic tools; J.A.L. analyzed data; and J.A.L. and J.P.T. wrote the paper.
The authors declare no conflict of interest.
This paper results from the Arthur M. Sackler Colloquium of the National Academy of Sciences, “Coupled Human and Environmental Systems,” held March 14–15, 2016, at the National Academies of Sciences in Washington, DC. The complete program and video recordings of most presentations are available on the NAS website at http://www.nasonline.org/Coupled_Human_and_Environmental_Systems.
This article is a PNAS Direct Submission.
This article contains supporting information online at http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1604985113/-/DCSupplemental.
Keywords: Plague; India.