Pathogen adaptation to seasonal forcing and climate change
Abstract
Many diverse infectious diseases exhibit seasonal dynamics. Seasonality in disease incidence has been attributed to seasonal changes in pathogen transmission rates, resulting from fluctuations in extrinsic climate factors. Multi-strain infectious diseases with strain-specific seasonal signatures, such as cholera, indicate that a range of seasonal patterns in transmission rates is possible in identical environments. We therefore consider pathogens capable of evolving their ‘seasonal phenotype’, a trait that determines the sensitivity of their transmission rates to environmental variability. We introduce a theoretical framework, based on adaptive dynamics, for predicting the evolution of disease dynamics in seasonal environments. Changes in the seasonality of environmental factors are one important avenue for the effects of climate change on disease. This model also provides a framework for examining these effects on pathogen evolution and associated disease dynamics. An application of this approach gives an explanation for the recent cholera strain replacement in Bangladesh, based on changes in monsoon rainfall patterns.
References
Ahmed A.U& Alam M Development of climate change scenarios with general circulation models. Vulnerability and adaptation to climate change for Bangladesh, Huq S, Karim Z, Asaduzzaman M& Mahtab F . 1999pp. 14–20. Eds. Dordrecht:Kluwer Academic Publishers. Google ScholarBoots M& Haraguchi Y . 1999The evolution of costly resistance in host–parasite systems. Am. Nat. 153, 359–370. Crossref, PubMed, ISI, Google ScholarBouma M.J& Pascual M . 2001Seasonal and interannual cycles of endemic cholera in Bengal 1891–1940 in relation to climate and geography. Hydrobiologia. 460, 147–156. Crossref, ISI, Google ScholarBowers R.G& White A . 2002The adaptive dynamics of Lotka--Volterra systems with trade-offs. Math. Biosci. 175, 67–81. Crossref, PubMed, ISI, Google ScholarBradbury J . 2003Beyond the fire-hazard mentality of medicine: the ecology of infectious diseases. PLoS Biol. 1, 148–151. Crossref, ISI, Google ScholarCoakley S.M, Scherm H& Chakraborty S . 1999Climate change and plant disease management. Annu. Rev. Phytopathol. 37, 399–426. Crossref, PubMed, ISI, Google ScholarColwell R . 1996Global climate and infectious disease: the cholera paradigm. Science. 274, 2025–2031. Crossref, PubMed, ISI, Google ScholarDay T& Proulx S.R . 2004A general theory for the evolutionary dynamics of virulence. Am. Nat. 163, E40–E63. Crossref, PubMed, ISI, Google Scholarde Jong M, Diekmann O& Heesterbeek H How does transmission of infection depend on population size?. In Epidemic models: their structure and relation to data, Mollison D& Moffatt H.K . 1995Cambridge University Press. Google Scholarde Mazancourt C& Dieckmann U . 2004Trade-off geometries and frequency-dependent selection. Am. Nat. 164, 765–778. Crossref, PubMed, ISI, Google ScholarDieckmann U Dynamics of pathogen–host interactions. Adaptive dynamics of infectious diseases: in pursuit of virulence management, Dieckmann U, Metz J.A.J, Sabelis M.W& Sigmund K . 2002Cambridge University Press. Crossref, Google ScholarEgas M, Dieckmann U& Sabelis M.W . 2004Evolution restricts the coexistence of specialists and generalists: the role of trade-off structure. Am. Nat. 163, 518–531. Crossref, PubMed, ISI, Google Scholar- FAO 1988 Land resources appraisal of Bangladesh for agriculture development. Report 3: land resource data base, volume 1:climatic data base. United Nations development programme/Food and Agriculture Organization of the United Nations. Google Scholar
Fine P.E& Clarkson J.A . 1982Measles in England and Wales—I: an analysis of factors underlying seasonal patterns. Int. J. Epidemiol. 11, 5–14. Crossref, PubMed, ISI, Google ScholarGeritz S.A.H, Kisdi E, Meszena G& Metz J.A.J . 1998Evolutionary singular strategies and the adaptive growth and branching of the evolutionary tree. Evol. Ecol. 12, 35–57. Crossref, ISI, Google ScholarGlass R.I, Becker S, Huq S.I, Stoll B.J, Khan M.U, Merson M.H, Lee J.V& Black R.E . 1982Endemic cholera in rural Bangladesh, 1966–1980. Am. J. Epidemiol. 116, 959–970. Crossref, PubMed, ISI, Google ScholarHarvell C.D, Mitchell C.E, Ward J.R, Altizer S, Dobson A.P, Ostfeld R.S& Samuel M.D . 2002Climate warming and disease risks for terrestrial and marine biota. Science. 296, 2158–2162. Crossref, PubMed, ISI, Google ScholarIslam M.S, Hasan M.K, Miah M.A, Yunus M, Zaman K& Albert M.J . 1994Isolation of Vibrio cholerae O139 synonym Bengal from the aquatic environment in Bangladesh: implications for disease transmission. Appl. Environ. Microbiol. 60, 1684–1686. Crossref, PubMed, ISI, Google ScholarKoella J.C& Doebeli M . 1999Population dynamics and the evolution of virulence in epidemiological models with discrete host generations. J. Theor. Biol. 198, 461–475. Crossref, PubMed, ISI, Google ScholarKoelle K& Pascual M . 2004Disentangling extrinsic from intrinsic factors in disease dynamics: a nonlinear time series approach with an application to cholera. Am. Nat. 163, 901–913. Crossref, PubMed, ISI, Google Scholar- Koelle, K., Rodó, X., Pascual, M., Yunus, M. & Mostafa, G. In press. Refractory periods and environmental forcing in cholera dynamics. Nature. Google Scholar
May R.M& Anderson R.M . 1983Epidemiology and genetics in the coevolution of parasites and hosts. Proc. R. Soc. B. 219, 281–313. Link, ISI, Google ScholarMcCallum H, Barlow N& Hone J . 2001How should pathogen transmission be modelled?. Trends Ecol. Evol. 16, 295–300. Crossref, PubMed, ISI, Google ScholarMetz J.A.J, Nisbet R.M& Geritz S.A.H . 1992How should we define fitness for general ecological scenarios?. Trends Ecol. Evol. 7, 198–202. Crossref, PubMed, ISI, Google ScholarMiller C.J, Drasar B.S& Feachem R.G . 1984Responses of toxigenic Vibrio cholerae 01 to physico-chemical stresses in aquatic environments. J. Hyg. Camb. 93, 475–495. Crossref, PubMed, Google ScholarPalumbi S . 2001Humans as the World's greatest evolutionary force. Science. 293, 1786–1790. Crossref, PubMed, ISI, Google ScholarPascual M, Bouma M.J& Dobson A.P . 2002Cholera and climate: revisiting the quantitative evidence. Microbes Infect. 4, 237–245. Crossref, PubMed, ISI, Google ScholarReidl J& Klose K.E . 2002Vibrio cholerae and cholera: out of the water and into the host. FEMS Microbiol. Rev. 26, 125–139. Crossref, PubMed, ISI, Google ScholarSack R.B, 2003A four-year study of the epidemiology of Vibrio cholerae in four rural areas in Bangladesh. J. Infect. Dis. 187, 96–101. Crossref, PubMed, ISI, Google ScholarSpira W.M Environmental factors in diarrhea transmission: the ecology of Vibrio cholerae 01 and cholera. Acute enteric infections in children: new prospects for treatment and prevention, Holme T, Holmgren J, Merson M.H& Mollby R . 1981Amsterdam:Elsevier. Google ScholarWatnick P.I, Lauriano C.M, Klose K.E, Croal L& Kolter R . 2001The absence of a flagellum leads to altered colony morphology, biofilm development, and virulence in Vibrio cholerae 0139. Mol. Microbiol. 39, 223–235. Crossref, PubMed, ISI, Google ScholarZo Y, Rivera I.N.G, Russek-Cohen E, Islam M.S, Siddique A.K, Yunus M, Sack R.B, Huq A& Colwell R . 2002Genomic profiles of clinical and environmental isolates of Vibrio cholerae 01 in cholera-endemic areas of Bangladesh. Proc. Natl Acad. Sci. 99, 12 409–12 414. Crossref, ISI, Google Scholar



