Unpacking β: Within-host dynamics and the evolutionary ecology of pathogen transmission

Annual Review of Ecology, Evolution, and Systematics

Volumn 39, Issue , 2008, Pages 415-437

  Antolin, Michael F ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Infectious disease; Microbial genetics; Pathogenesis; Plague; Virulence

Indexed keywords

BACTERIUM; DISEASE TRANSMISSION; ENVIRONMENTAL GRADIENT; EVOLUTIONARY BIOLOGY; GENETIC VARIATION; GENETICS; HOST SELECTION; HOST-PATHOGEN INTERACTION; INFECTIOUS DISEASE; NATURAL SELECTION; PATHOGENICITY; TRADE-OFF; VIRULENCE;

ARTHROPODA; BACTERIA (MICROORGANISMS); EUKARYOTA; MAMMALIA; PROTOZOA; SIPHONAPTERA (FLEAS); YERSINIA PESTIS;

EID: 58549099698     PISSN: 1543592X     EISSN: 15452069     Source Type: Book Series    
DOI: 10.1146/annurev.ecolsys.37.091305.110119     Document Type: Review

References (157)

1. Achtman M, Morelli G, Zhu P, Wirth T, Diehl I, et al. 2004. Microevolution and history of the plague bacillus, Yersinia pestis. Proc. Natl. Acad. Sci. USA 101:17837-42
2. Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P. 2006. Seasonality and the dynamics of infectious diseases. Ecol. Lett. 9:467-84
3. Anderson RM, May RM. 1991. Infectious Diseases of Humans: Dynamics and Control. Oxford UK: Oxford Univ. Press. 757 pp.
4. Andre JB, Day T. 2005. The effect of disease life history on the evolutionary emergence of novel pathogens. Proc. R. Soc. Lond. B 272:1949-56
5. Anisimov AP, Lindler LE, Pier GB. 2004. Intraspecific diversity of Yersinia pestis. Clin. Microbiol. Rev. 17:434-464
6. Antia R, Regoes RR, Koella JC, Bergstrom CT. 2003. The role of evolution in the emergence of infectious diseases. Nature 426:658-61
7. Antolin MF, Gober P, Luce B, Biggins DE, van Pelt WE, et al. 2002. The influence of sylvatic plague on North American wildlife at the landscape level, with special emphasis on black-footed ferret and prairie dog conservation. Trans. N. Am. Wildl. Nat. Res. Conf. 67:104-127
8. Antolin MF, Savage LT, Eisen RJ. 2006. Landscape features influence genetic structure of black-tailed prairie dogs (Cynomys ludovicianus). Land. Ecol. 21:867-75
9. Baigent SJ, McCauley JW. 2003. Influenza type A in humans, mammals and birds: determinants of virus virulence, host-range and interspecies transmission. BioEssays 25:657-71
10. Baranowski E, Ruiz-Jarabo CM, Domingo E. 2001. Evolution of cell recognition by viruses. Science 292:1102-5
11. Begon M, Bennett M, Bowers RG, French MP, Hazel SM, Turner J. 2002. A clarification of transmission terms in host-microparasite models: numbers, densities and areas. Epidemiol. Infect. 129:147-53
12. Bergstrom CT, McElhany P, Real LA. 1999. Transmission bottlenecks as determinants of virulence in rapidly evolving pathogens. Proc. Natl. Acad. Sci. USA 96:5095-100
13. Biggins DE, Kosoy MY. 2001. Influences of introduced plague on North American mammals: implications from ecology of plague in Asia. J. Mammal. 82:906-916
14. Bjørnstad ON, Finkenstadt BF, Grenfell BT. 2002. Dynamics of measles epidemics: estimating scaling of transmission rates using a time series SIR model. Ecol. Monogr. 72:169-84
15. Blanpain C, Lee B, Tackoen M, Puffer B, Boom A, et al. 2000. Multiple nonfunctional alleles of CCR5 are frequent in various human populations. Blood 96:1638-45
16. Blokesch M, Schoolnik GK. 2007. Serogroup conversion of Vibrio cholerae in aquatic reservoirs. PLoS Pathogens 3:e81
17. Boots M, Hudson PJ, Sasaki A. 2003. Large shifts in pathogen virulence relate to host population structure. Science 303:842-44
18. Brubaker RR. 2003. Interleukin-10 and inhibition of innate immunity to yersiniae: roles of Yops and LcrV (V antigen). Inf. Immun. 71:3673-81
19. Bull JJ. 1994. Virulence. Evolution 48:1423-37
20. Burnet M, White DO. 1972. Natural History of Infectious Disease. Fourth Ed. Cambridge, UK: Cambridge Univ. Press. 278 pp.
21. Carniel E. 2003. Evolution of pathogenic Yersinia, some lights in the dark. Adv. Exp. Med. Biol. 529:3-12
22. Carniel E, Hinnebusch BJ, eds. 2004. Yersinia Molecular and Cellular Biology. Norfolk, UK: Horiz. Biosci. 431 pp.
23. Casadevall A, Pirofski L. 2001. Host-pathogen interactions: the attributes of virulence. J. Infect. Dis. 184:337-44
24. Cavanaugh DC. 1971. Specific effect of temperature upon transmission of the plague bacillus by the Oriental rat flea, Xenopsylla cheopis. Am. J. Trop. Med. Hyg. 20:264-73
25. Cavanaugh DC, Marshall JD Jr. 1972. The influence of climate on the seasonal prevalence of plague in the Republic of Vietnam. J. Wildl. Dis. 8:85-94
26. Chain PSG, Carniel E, Larimer FW, Lamerdin J, Stoutland PO, et al. 2004. Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. USA 101:13826-31
27. Cleaveland S, Haydon DT, Taylor L. 2007. Overviews of pathogen emergence: Which pathogens emerge, when, and why? Curr. Top. Microbiol. Immunol. 315:85-111
28. Collinge SK, Johnson WC, Ray C, Matchett R, Grensten J, et al. 2005. Testing the generality of a trophiccascade model for plague. EcoHealth 2:1-11
29. Conrad PA, Miller MA, Kreuder C, James ER, Mazet J, et al. 2005. Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. Int. J. Parasitol. 35:1155-68
30. 0 as a predictor of disease invasion in structured populations. J. R. Soc. Interface 4:315-324
31. Crow JF. 1958. Some possibilities for measuring selection intensities in man. Hum. Biol. 30:1-13
32. Darby C, Hsu JW, Ghori N, Falkow S. 2002. Caenorhabditis elegans: Plague bacteria biofilm blocks food intake. Nature 417:243-44
33. Davis S, Calvet E, Leirs H. 2005. Fluctuating rodent populations and risk to humans from rodent-borne zoonoses. Vector-Borne Zoo. Dis. 5:305-314
34. Davis S, Klassovskiy N, Ageyev V, Suleimenov B, Atshabar B, et al. 2007. Plague metapopulation dynamics in a natural reservoir: the burrow system as the unit of study. Epidemiol. Infect. 135:740-48
35. Day T. 2001. Parasite transmission modes and the evolution of virulence. Evolution 55:389-400
36. Day T. 2002. On the evolution of virulence and the relationship between various measures of mortality. Proc. R. Soc. London B 269:1317-23
37. Day T, Proulx SR. 2004. A general theory for the evolutionary dynamics of virulence. Am. Nat. 163:E40-63
38. Dean M, Carrington M, O'Brien SJ. 2002. Balanced polymorphism selected by genetic versus infectious human disease. Annu. Rev. Genom. Hum. Genet. 3:263-92
39. Dean M, Carrington M, Winkler C, Huttley GA, Smith MW, et al. 1996. Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Science 273:1856-62
40. De Roode JC, Pansini R, Cheesman SJ, Helinski MEH, Huijben S, et al. 2005. Virulence and competitive ability in genetically diverse malaria infections. Proc. Natl. Acad. Sci. USA 102:7624-28
41. Dieckmann U. 2002. Adaptive dynamics of pathogen - host interactions. See Dieckmann et al. 2002, pp. 39-59
42. Dieckmann U, Metz JAJ, Sabelis MW, Sigmund K. 2002. Adaptive Dynamics of Infectious Diseases. Cambridge, UK: Cambridge Univ. Press. 463 pp.
43. Dieckmann U. 2002. Adaptive dynamics of pathogen - host interactions. See Dieckmann et al. 2002, pp. 39-59
44. Dobson A, Meagher M. 1996. The population dynamics of Brucellosis in Yellowstone National Park. Ecology 77:1026-36
45. Duplantier J-M, Duchemin J-B, Chanteau S, Carniel E. 2005. From the recent lessons of the Malagasy foci towards a global understanding of the factors involved in plague reemergence. Vet. Res. 36:437-53
46. Dwyer G, Dushoff J, Elkinton JS, Burand JP, Levin SA. 2002. Host heterogeneity in susceptibility: lessons from an insect virus. See Dieckmann et al. 2002, pp. 74-84
47. Dybdahl MF, Storfer A. 2003. Parasite local adaptation: Red Queen versus Suicide King. Trends Ecol. Evol. 18:523-530
48. Ebert D, Bull JJ. 2003. Challenging the trade-off model for the evolution of virulence: Is virulence management feasible? Trends Microbiol. 11:15-20
49. Engelthaler DM, Hinnebusch BJ, Rittner CM, Gage KL. 2000. Quantitative competitive PCR as a method for exploring flea-Yersinia pestis dynamics. Am. J. Trop. Med. Hyg. 62:552-60
50. Enscore RE, Biggerstaff BJ, Brown TL, Fulgham RF, Reynolds PJ, et al. 2002. Modeling relationships between climate and the frequency of human plague cases in the southwestern United States, 1960-1997. Am. J. Trop. Med. Hyg. 66:186-96
51. Erickson DL, Jarrett CO, Wren BW, Hinnebusch BJ. 2006. Serotype differences and lack of biofilm formation characterize Yersinia pseudotuberculosis infection of the Xenopsylla cheopis flea vector of Yersinia pestis. J. Bacteriol. 188:1113-19
52. Ewald PW. 1994. Evolution of Infectious Disease. Oxford, UK: Oxford Univ. Press. 298 pp.
53. Falush D, Wirth T, Linz B, Pritchard JK, Stephens M, et al. 2003. Traces of human migrations in Helicobacter pylori populations. Science 299:1582-85
54. Fenton A, Fairbairn JP, Norman R, Hudson PJ. 2002. Parasite transmission: reconciling theory and reality. J. Anim. Ecol. 71:893-905
55. Ferguson HM, MacKinnon MJ, Chan BH, Read AF. 2003a. Mosquito mortality and the evolution of malaria virulence. Evolution 57:2792-804
56. Ferguson NM, Galvani AP, Bush RM. 2003b. Ecological and immunological determinants of influenza evolution. Nature 422:428-33
57. 0 of an infectious pathogen by a removal method. Math. Biosci. 198:14-26
58. Frank SA. 1996. Models of parasite virulence. Q. Rev. Biol. 71:37-78
59. Frank SA, Schmid-Hempel P. 2008. Mechanisms of pathogenesis and the evolution of pathogen virulence. J. Evol. Biol. 21:396-404
60. Gage KL, Kosoy MY. 2005. Natural history of plague: perspectives from more than a century of research. Annu. Rev. Entomol. 50:505-28
61. Galvani AP. 2003. Epidemiology meets evolutionary ecology. Trends Ecol. Evol. 18:132-39
62. 32 HIV-resistance allele. Proc. Natl. Acad. Sci. USA 100:15276-79
63. Gandon S, Agnew P, Michalakis Y. 2002. Coevolution between parasite virulence and host life-history traits. Am. Nat. 160:374-88
64. Ganusov VV. 2003. Evolution of virulence: adaptive or not? Trends Microbiol. 11:112-13
65. Ganusov VV, Antia R. 2003. Trade-offs and the evolution of virulence of microparasites: Do details matter? Theoret. Popul. Biol. 64:211-20
66. Girard JM, Wagner DM, Vogler AJ, Keys C, Allender CJ, et al. 2004. Differential plague-transmission dynamics determine Yersinia pestis population genetic structure on local, regional, and global scales. Proc. Natl. Acad. Sci. USA 101:8408-13
67. Gog JR, Woodroffe R, Swinton J. 2002. Disease in endangered metapopulations: the importance of alternative hosts. Proc. R. Soc. London Ser. A 269:671-76
68. Graham AL, Allen JE, Read AF. 2005. Evolutionary causes and consequences of immunopathology. Annu. Rev. Ecol. Evol. Syst. 36:373-97
69. Grenfell BT. 2001. Dynamics and epidemiological impact of microparasites. In New Challenges To Health: The Threat of Virus Infection, ed. GL Smith, WL Irving, JW McCauley, DJ Rowlands, pp. 33-52. Cambridge, UK: Cambridge Univ. Press
70. Grenfell BT, Pybus OG, Gog JR, Wood JLN, Daly JM, et al. 2004. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303:327-32
71. Gupta S. 2005. Parasite immune escape: new views into parsite-host interactions. Curr. Opin. Microbiol. 8:428-33
72. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, et al. 2002. Climate warming and disease risks for terrestrial and marine biota. Science 296:2158-62
73. 0 and a recipe for its calculation. Acta Biotheor. 50:189-204
74. Hess G. 1996. Disease in metapopulation models: implications for conservation. Ecology 77:1617-32
75. Hinnebusch BJ. 2005. The evolution of flea-borne transmission in Yersinia pestis. Curr. Issues Mol. Biol. 7:197-212
76. Hinnebusch BJ, Perry RD, Schwan TG. 1996. Role of the Yersinia pestis hemin storage (hms) locus in the transmission of plague by fleas. Science 273:367-70
77. Hinnebusch BJ, Rosso ML, Schwan TG, Carniel E. 2002a. High-frequency conjugative transfer of antibiotic resistance genes to Yersinia pestis in the flea midgut. Molec. Microbiol. 46:349-54
78. Hinnebusch BJ, Rudolph AE, Cherepanov P, Dixon JE, Schwan TG, Forsberg A. 2002b. Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science 296:733-35
79. Hummel S, Schmidt D, Kremeyer B, Herrmann B, Oppermann M. 2005. Detection of the CCR5-Δ32 HIV resistance gene in Bronze Age skeletons. Gene. Immun. 6:371-74
80. Jarrett CO, Deak E, Isherwood KE, Oyston PC, Fischer ER, et al. 2004. Transmission of Yersinia pestis from an infectious biofilm in the flea vector. J. Inf. Dis. 190:783-92
81. Joshua GWP, Karlyshev AV, Smith MP, Isherwood KE, Titball RW, Wren BW. 2003. A Caenorhabditis elegans model of Yersinia infection: biofilm formation on a biotic surface. Microbiology 149:3221-29
82. Kartman L, Prince FM. 1956. 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. Am. J. Trop. Med. Hyg. 5:1058-70
83. Keeling MJ, Bjørnstad ON, Grenfell BT. 2004. Metapopulation dynamics of infectious diseases. In Ecology, Genetics and Evolution of Metapopulations, ed. I Hanski, OE Gaggiotti, pp. 415-45. New York: Academic
84. 0. J. Theor. Biol. 203:51-61
85. Klevytska AM, Price LB, Schupp JM, Worsham PL, Wong J, Keim P. 2001. Identification and characterization of variable-number tandem repeats in the Yersinia pestis genome. J. Clin. Microbiol. 39:3179-85
86. Koelle K, Rodo X, Pascual M, Yunus M, Mostafa G. 2006. Refractory periods and climate forcing in cholera dynamics. Nature 436:696-700
87. Kuiken T, Holmes EC, McCauley J, Rimmelzwaan GF, Williams CS, Grenfell BT. 2006. Host species barriers to influenza virus infections. Science 312:394-397
88. Kukkonen M, Suomalainen M, Kyllönen P, Lähteenmäki K, Láng H, et al. 2004. Lack of O-antigen is essential for plasminogen activation by Yersinia pestis and Salmonella enterica. Mol. Microbiol. 51:215-25
89. Lathem WW, Price PA, Miller VL, Goldman WE. 2007. A plasminogen- activating protease specifically controls the development of primary pneumonic plague. Science 315:509-13
90. Levin BR, Antia R. 2001. Why we don't get sick: the within-host population dynamics of bacterial infections. Science 292:1112-15
91. Levin BR, Lipsitch M, Bonhoeffer S. 1999. Population biology, evolution, and infectious disease: convergence and synthesis. Science 283:806-9
92. Lipsitch M, Cohen T, Cooper B, Robins JM, Ma S, et al. 2003. Transmission dynamics and control of severe acute respiratory syndrome. Science 300:1966-70
93. Lipsitch M, Moxon ER. 1997. Virulence and transmissibility of pathogens: What is the relationship? Trends Microbiol. 5:31-37
94. Lipsitch M, Nowak M. 1995. The evolution of virulence in sexually transmitted HIV/AIDS. J. Theoret. Biol. 174:427-40
95. Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM. 2005. Superspreading and the effect of individual variation on disease emergence. Nature 438:355-59
96. Lorange EA, Race BL, Sebbane F, Hinnebusch BJ. 2005. Poor vector competence of fleas and the evolution of hypervirulence in Yersinia pestis. J. Infect. Dis. 191:1907-12
97. Lowell JL, Wagner DM, Atshabar B, Antolin MF, Vogler AJ, et al. 2005. Identifying sources of human exposure to plague. J. Clin. Microbiol. 43:650-56
98. Lowell JL, Zhansarina A, Yockey B, Meka-Mechenko T, Atshabar B, et al. 2007. Phenotypic and molecular characterizations of Yersinia pestis isolates from Kazakhstan and adjacent regions. Microbiology 153:169-77
99. Mackinnon MJ, Read AF. 2004. Virulence in malaria: an evolutionary viewpoint. Phil. Trans. R. Soc. London Ser. B 359:965-86
100. Massey RC, Horsburgh MJ, Lina G, Hook M, Recker M. 2006. Opinion - The evolution and maintenance of virulence in Staphylococcus aureus: a role for host-to-host transmission? Nat. Rev. Microbiol. 4:953-58
101. McCallum H, Barlow N, Hone J. 2001. How should pathogen transmission be modelled? Trends Ecol. Evol. 16:295-300
102. Mecsas J, Franklin G, Kuziel WA, Brubaker RR, Falkow S, Mosier DE. 2004. Evolutionary genetics: CCR5 mutation and plague protection. Nature 427:606
103. Meyers LA, Levin BR, Richardson AR, Stojiljkovic I. 2003. Epidemiology, hypermutation, within-host evolution and the virulence of Neisseria meningitides. Proc. R. Soc. London B 270:1667-77
104. Mills CE, Robins JM, Lipsitch M. 2004. Transmissibility of 1918 pandemic influenza. Nature 432:904-6
105. Moore J. 2002. Parasites and the Behavior of Animals. Oxford: Oxford Univ. Press. 315 pp.
106. Moran NA, Plague GR. 2004. Genomic changes following host restriction in bacteria. Curr. Opin. Genet. Dev. 14:627-33
107. Motin VL, Georgescu AM, Elliott JM, Hu P, Worsham PL, et al. 2002. Genetic variability of Yersinia pestis isolates as predicted by PCR-based IS100 genotyping and analysis of structural genes encoding glycerol-3- phospohate dehydrogenase. J. Bacteriol. 184:1019-27
108. Motin VL, Georgescu AM, Fitch JP, Gu PP, Nelson DO, et al. 2004. Temporal global changes in gene expression during temperature transition in Yersinia pestis. J. Bacteriol. 186:6298-305
109. Naug D, Smith B. 2007. Experimentally induced change in infectious period affects transmission dynamics in a social group. Proc. R. Soc. London Ser. B 274:61-65
110. Novembre J, Galvani AP, Slatkin M. 2005. The geographic spread of the CCR5 Δ32 HIV-resistance allele. PLoS Biol. 3:1954-62
111. Ochman H, Moran NA. 2001. Genes lost and genes found: Evolution of bacterial pathogenesis and symbiosis. Science 292:1096-98
112. Pascual M, Dobson A. 2005. Seasonal patterns of infectious diseases. PLoS Med. 2:18-20
113. Pascual M, Koelle K, Dobson AP. 2006. Hyperinfectivity in cholera: a new mechanism for an old epidemiological model? PLoS Med. 3:931-933
114. Perry RD, Fetherston JD. 1997. Yersinia pestis - etiologic agent of plague. Clin. Microbiol. Rev. 10:35-66
115. Perry RD, Fetherston JD, eds. 2007. The Genus Yersinia: From Genomics to Function. Vol. 603: Advances in Experimental Medicine and Biology. New York: Springer. 429 pp.
116. Pollitzer R. 1954. Plague. World Health Organization Monograph Series No. 22. Geneva:World Health Organ. 698 pp.
117. Real LA, Biek R. 2007. Infectious disease modeling and the dynamics of transmission. Curr. Top. Microbiol. Immunol. 315:33-49
118. Real LA, Henderson JC, Biek R, Snaman J, Jack TL, et al. 2005. Unifying the spatial population dynamics and molecular evolution of epidemic rabies virus. Proc. Natl. Acad. Sci. USA 102:12107-11
119. Reed KD, Meece JK, Henkel JS, Shukla SK. 2003. Birds, migration and emerging zoonoses: west Nile virus, lyme disease, influenza A and enteropathogens. Clin. Med. Res. 1:5-12
120. Roberts MG. 2007. The pluses and minuses of R0. J. R. Soc. Interface 4:949-61
121. Sabeti PC, Walsh E, Schaffner SF, Varilly P, Fry B, et al. 2005. The case for selection at CCR5-Δ32. PLoS Biol. 3:1963-69
122. Schmid-Hempel P, Ebert D. 2003. On the evolutionary ecology of specific immune defence. Trends Ecol. Evol. 18:27-32
123. Sebbane F, Gardner D, Long D, Gowen BB, Hinnebusch BJ. 2005. Kinetics of disease progression and host response in a rat model of bubonic plague. Am. J. Pathol. 166:1427-39
124. Sebbane F, Jarrett CO, Gardner D, Long D, Hinnebusch BJ. 2006a. Role of the Yersinia pestis plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea-borne plague. Proc. Natl. Acad Sci. USA 103:5526-30
125. Sebbane F, Lemaitre N, Sturdevant DE, Rebeil R, Virtaneva K, et al. 2006b. Adaptive response of Yersinia pestis to extracellular effectors of innate immunity during bubonic plague. Proc. Natl. Acad. Sci. USA 103:11766-71
126. Shackelton LA, Parrish CR, Truyen U, Holmes EC. 2005. High rate of viral evolution associated with the emergence of carnivore parvovirus. Proc. Natl. Acad. Sci. USA 102:379-84
127. Skurnik M, Peippo A, Ervelä E. 2000. Characterization of the O-antigen gene clusters of Yersinia pseudotuberculosis and the cryptic O-antigen gene cluster of Yersinia pestis shows that the plague bacillus is most closely related to and has evolved from Y. pseudotuberculosis serotype O:1b. Mol. Microbiol. 37:316-30
128. Smith DL, Dushoff J, Snow RW, Hay SI. 2005. The entomological inoculation rate and Plasmodium falciparum infection in African children. Nature 438:492-95
129. Smith DL, Lucey B, Waller LA, Childs JE, Real LA. 2002. Predicting the spatial dynamics of rabies epidemics on heterogeneous landscapes. Proc. Natl. Acad. Sci. USA 99:3668-72
130. Snäll T, O'Hara RB, Ray C, Collinge SK. 2008. Climate-driven spatial dynamics of plague among prairie dog colonies. Am. Nat. 171:238-48
131. Song YJ, Tong ZZ, Wang J, Wang L, Guo ZB, et al. 2004. Complete genome sequence of Yersinia pestis strain 91001, an isolate avirulent to humans. DNA Res. 11:179-97
132. Stapp P. 2007. Trophic cascades and disease ecology. Ecohealth 4:121-22
133. Stapp P, Antolin MF, Ball M. 2004. Patterns of extinction in prairie dog metapopulations: Plague outbreaks follow El Niño events. Front. Ecol. Environ. 2:235-40
134. Stenseth NC, Samia NI, Viljugrein H, Kausrud KL, Begon M, et al. 2006. Plague dynamics are driven by climate variation. Proc. Natl. Acad. Sci. USA 103:13110-15
135. Stevens L, Giordano R, Fialho RF. 2001. Male-killing, nematode infections, bacteriophage infection, and virulence of cytoplasmic bacteria in the genus Wolbachia. Annu. Rev. Ecol. Syst. 32:519-45
136. Stewart AD, Logsdon JM, Kelley SE. 2005. An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution 59:730-39
137. Stouthamer R, Breeuwer JAJ, Hurst GDD. 1999. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 53:71-102
138. Straley SC, Perry RD. 1995. Environmental modulation of gene-expression and pathogenesis in Yersinia. Trends Microbiol. 3:310-17
139. Taha MK, Deghmane AE, Antignac A, Zarantonelli ML, Larribe M, Alonso JM. 2002. The duality of virulence and transmissibility in Neisseria meningitidis. Trends Microbiol. 10:376-82
140. Thomas SR, Elkinton JS. 2004. Pathogenicity and virulence. J. Invert. Path. 85:146-51
141. Thomson NR, Parkhill J. 2004. Yersinia pestis chromosome. In Yersinia: Molecular and Cellular Biology, ed. E Carniel, BJ Hinnesbusch, pp. 1-17. Wymondham UK: Horiz. Biosci.
142. Tong ZZ, Zhou DS, Song YJ, Zhang L, Pei DC, et al. 2005a. Genetic variations in the pgm locus among natural isolates of Yersinia pestis. J. Gen. Appl. Microbiol. 51:11-19
143. Tong ZZ, Zhou DS, Song YJ, Zhang L, Pei DC, et al. 2005b. Pseudogene accumulation might promote the adaptive microevolution of Yersinia pestis. J. Med. Microbiol. 54:259-68
144. Vizoso DB, Ebert D. 2005. Phenotypic plasticity in host-parasite interactions in response to route of infection. J. Evol. Biol. 18:911-21
145. Wang LF, Shi ZL, Zhang SY, Field H, Daszak P, Eaton BT. 2006. Review of bats and SARS. Emerg. Infect. Dis. 12:1834-40
146. Webb CT, Brooks CP, Gage KL, Antolin MF. 2006. Classic flea-borne transmission does not drive plague epizootics in prairie dogs. Proc. Natl. Acad. Sci. USA 103:6236-41
147. Webby R, Hoffmann E, Webster R. 2004. Molecular constraints to interspecies transmission of viral pathogens. Nat. Med. 10:S77-S81
148. Werren JH. 1997. Biology of Wolbachia. Annu. Rev. Entomol. 42:587-609
149. Wilder AP, Eisen RJ, Bearden SW, Montenieri JA, Tripp DW, et al. 2008. Transmission efficiency of two flea species (Oropsylla tuberculata cynomuris and Oropsylla hirsuta) involved in plague epizootics among prairie dogs. Ecohealth. In press. DOI: 10.1007/s10393-008-0165-1
150. Wolfe ND, Dunavan CP, Diamond J. 2007. Origins of major human infectious diseases. Nature 447:279-83
151. Woolhouse MEJ, Dye C, Etard JJ, Smithi T, Charlwoodi JD, et al. 1997. Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc. Natl. Acad. Sci. USA 94:338-42
152. Woolhouse MEJ, Taylor LH, Haydon DT. 2001. Population biology of multihost pathogens. Science 292:1109-12
153. Wren BW. 2003. The Yersiniae-a model genus to study the rapid evolution of bacterial pathogens. Nat. Rev. Microbiol. 1:55-64
154. Yates TL, Mills JN, Parmenter CA, Ksiazek TG, Parmenter RR, et al. 2002. The ecology and evolutionary history of an emergent disease: hantavirus pulmonary syndrome. Bioscience 52:989-98
155. Zeier M, Handermann M, Bahr U, Rensch B, Muller S, et al. 2005. New ecological aspects of hantavirus infection: a change of a paradigm and a challenge of prevention-a review. Virus Genes 30:157-80
156. Zchori-Fein E, Perlman SJ, Kelly SE, Katzir N, Hunter MS. 2004. Characterization of a 'Bacteroidetes' symbiont in Encarsia wasps (Hymenoptera: Aphelinidae): proposal of 'Candidatus Cardinium hertigii.' Int. J. Syst. Evol. Microbiol. 54:961-68
157. Zhou DS, Tong ZZ, Song Y, Han YP, Pei D, et al. 2004. Genetics of metabolic variations between Yersinia pestis biovars and the proposal of a new biovar, microtus. J. Bacteriol. 186:5147-52