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The adaptive evolution of virulence: a review of theoretical predictions and empirical tests

  • CLAYTON E. CRESSLER (a1) (a2), DAVID V. McLEOD (a1), CARLY ROZINS (a1), JOSÉE VAN DEN HOOGEN (a1) and TROY DAY (a1) (a2) (a3)...

Summary

Why is it that some parasites cause high levels of host damage (i.e. virulence) whereas others are relatively benign? There are now numerous reviews of virulence evolution in the literature but it is nevertheless still difficult to find a comprehensive treatment of the theory and data on the subject that is easily accessible to non-specialists. Here we attempt to do so by distilling the vast theoretical literature on the topic into a set of relatively few robust predictions. We then provide a comprehensive assessment of the available empirical literature that tests these predictions. Our results show that there have been some notable successes in integrating theory and data but also that theory and empiricism in this field do not ‘speak’ to each other very well. We offer a few suggestions for how the connection between the two might be improved.

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This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

*Corresponding author. Department of Mathematics, Statistics & Biology, Queen's University, Kingston, ON K7L 3N6, Canada. E-mail: tday@mast.queensu.ca

References

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Agnew, P. and Koella, J. C. (1997). Virulence, parasite mode of transmission, and host fluctuating asymmetry. Proceedings of the Royal Society of London B: Biological Sciences 264, 915.
Agnew, P. and Koella, J. C. (1999). Life history interactions with environmental conditions in a host-parasite relationship and the parasite's mode of transmission. Evolutionary Ecology 13, 6789.
Alizon, S. (2008 a). Decreased overall virulence in coinfected hosts leads to the persistence of virulent parasites. American Naturalist 172, E67E79.
Alizon, S. (2008 b). Transmission-recovery trade-offs to study parasite evolution. American Naturalist 172, E113E121.
Alizon, S. (2013 a). Co-infection and super-infection models in evolutionary epidemiology. Interface Focus 3, 20130031.
Alizon, S. (2013 b). Parasite co-transmission and the evolutionary epidemiology of virulence. Evolution (N. Y) 67, 921933.
Alizon, S., Hurford, A., Mideo, N. and Van Baalen, M. (2009). Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. Journal of Evolutionary Biology 22, 245259.
Alizon, S. and Lion, S. (2011). Within-host parasite cooperation and the evolution of virulence. Proceedings of the Royal Society of London B: Biological Sciences 278, 37383747.
Alizon, S. and Michalakis, Y. (2015). Adaptive virulence evolution: the good old fitness-based approach. Trends in Ecology & Evolution 30, 248254.
Alizon, S. and van Baalen, M. (2005). Emergence of a convex trade-off between transmission and virulence. American Naturalist 165, E155E167.
Alizon, S. and van Baalen, M. (2008). Multiple infections, immune dynamics, and the evolution of virulence. American Naturalist 172, E150E168.
Altizer, S. M. and Augustine, D. J. (1997). Interactions between frequency-dependent and vertical transmission in host-parasite systems. Proceedings of the Royal Society B: Biological Sciences 264, 807814.
Anderson, R. M. and May, R. M. (1982). Coevolution of hosts and parasites. Parasitology 85(Pt 2), 411426.
André, J. B., Ferdy, J. B. and Godelle, B. (2003). Within-host parasite dynamics, emerging trade-off, and evolution of virulence with immune system. Evolution (N. Y) 57, 14891497.
André, J. B. and Gandon, S. (2006). Vaccination, within-host dynamics, and virulence evolution. Evolution 60, 1323.
Antia, R., Levin, B. R. and May, R. M. (1994). Within-host population dynamics and the evolution and maintenance of microparasite virulence. American Naturalist 144, 457472.
Atkins, K. E., Read, A. F., Savill, N. J., Renz, K. G., Islam, A. F., Walkden-Brown, S. W. and Woolhouse, M. E. J. (2013). Vaccination and reduced cohort duration can drive virulence evolution: Marek's disease virus and industrialized agriculture. Evolution (N. Y) 67, 851860.
Barclay, V. C., Rå berg, L., Chan, B. H. K., Brown, S., Gray, D. and Read, A. F. (2008). CD4+T cells do not mediate within-host competition between genetically diverse malaria parasites. Proceedings of the Royal Society B: Biological. Sciences 275, 11711179.
Barclay, V. C., Sim, D., Chan, B. H. K., Nell, L. A., Rabaa, M. A., Bell, A. S., Anders, R. F. and Read, A. F. (2012). The evolutionary consequences of blood-stage vaccination on the rodent malaria Plasmodium chabaudi . PLoS Biology 10, e1001368.
Bashey, F., Young, S. K., Hawlena, H. and Lively, C. M. (2012). Spiteful interactions between sympatric natural isolates of Xenorhabdus bovienii benefit kin and reduce virulence. Journal of the Evolutionary Biology 25, 431437.
Becker, D. J. and Hall, R. J. (2014). Too much of a good thing: resource provisioning alters infectious disease dynamics in wildlife. Biology Letters 10, 20140309.
Bell, A. S., de Roode, J. C., Sim, D. and Read, A. F. (2006). Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60, 13581371.
Ben-Ami, F., Regoes, R. R. and Ebert, D. (2008). A quantitative test of the relationship between parasite dose and infection probability across different host-parasite combinations. Proceedings of the Royal Society B: Biological Sciences 275, 853859.
Ben-Ami, F. and Routtu, J. (2013). The expression and evolution of virulence in multiple infections: the role of specificity, relative virulence and relative dose. BMC Evolutionary Biology 13, 97.
Berngruber, T. W., Froissart, R., Choisy, M. and Gandon, S. (2013). Evolution of virulence in emerging epidemics. PLoS Pathogens 9, e1003209.
Berngruber, T. W., Lion, S. and Gandon, S. (2015). Spatial structure, transmission modes and the evolution of viral exploitation strategies. PLOS Pathogens 11, e1004810.
Best, A. and Hoyle, A. (2013). A limited host immune range facilitates the creation and maintenance of diversity in parasite virulence. Interface Focus 3, 20130024.
Best, A., White, A. and Boots, M. (2010). Resistance is futile but tolerance can explain why parasites do not always castrate their hosts. Evolution (N. Y) 64, 348357.
Bolker, B. M., Nanda, A. and Shah, D. (2010). Transient virulence of emerging pathogens. Journal of the Royal Society Interface 7, 811822.
Bolzoni, L. and De Leo, G. A. (2013). Unexpected consequences of culling on the eradication of wildlife diseases: the role of virulence evolution. American Naturalist 181, 301–13.
Bonhoeffer, S., Lenski, R. E. and Ebert, D. (1996). The curse of the pharaoh: the evolution of virulence in pathogens with long living propagules. Proceedings of the Royal Society B: Biological Sciences 263, 715721.
Boots, M., Hudson, P. J. and Sasaki, A. (2004). Large shifts in pathogen virulence relate to host population structure. Science 303, 842844.
Boots, M. and Mealor, M. (2007). Local interactions select for lower pathogen infectivity. Science 315, 12841286.
Boots, M. and Sasaki, A. (1999). ‘Small worlds’ and the evolution of virulence: infection occurs locally and at a distance. Proceedings of the Royal Society B: Biological Sciences 266, 19331938.
Boots, M. and Sasaki, A. (2000). The evolutionary dynamics of local infection and global reproduction in host-parasite interactions. Ecology Letters 3, 181185.
Bremermann, H. J. and Pickering, J. (1983). A game-theoretical model of parasite virulence. Journal of Theoretical Biology 100, 411426.
Bremmerman, H. J. and Thieme, H. R. (1989). A competitive exclusion principle for pathogen virulence. Journal of Mathematical Biology 27, 179190.
Brown, S. P. (2001). Collective action in an RNA virus. Journal of Evolutionary Biology 14, 821828.
Brown, S. P., Cornforth, D. M. and Mideo, N. (2012). Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control. Trends in Microbiology 20, 336342.
Brown, S. P. and Grenfell, B. T. (2001). An unlikely partnership: parasites, concomitant immunity and host defence. Proceedings of the Royal Society B: Biological Sciences 268, 25432549.
Bull, J. J. and Ebert, D. (2008). Invasion thresholds and the evolution of nonequilibrium virulence. Evolutionary Applications 1, 172182.
Bull, J. J. and Lauring, A. S. (2014). Theory and empiricism in virulence evolution. PLoS Pathogens 10, 13.
Bull, J. J., Molineux, I. J. and Rice, W. R. (1991). Selection of benevolence in a host parasite system. Evolution (N. Y) 45, 875882.
Caraco, T., Glavanakov, S., Li, S., Maniatty, W. and Szymanski, B. K. (2006). Spatially structured superinfection and the evolution of disease virulence. Theoretical Population Biology 69, 367384.
Caraco, T. and Wang, I. N. (2008). Free-living pathogens: life-history constraints and strain competition. Journal of Theoretical Biology 250, 569579.
Charlesworth, B. (1994). Evolution in Age-Structured Populations, 2nd Edn. Cambridge University Press, Cambridge, UK.
Chen, H., Deng, G., Li, Z., Tian, G., Li, Y., Jiao, P., Zhang, L., Liu, Z., Webster, R. G. and Yu, K. (2004). The evolution of H5N1 influenza viruses in ducks in southern China. Proceedings of the National Academy of Sciences of the United States of America 101, 1045210457.
Choisy, M. and de Roode, J. C. (2010). Mixed infections and the evolution of virulence: effects of resource competition, parasite plasticity, and impaired host immunity. American Naturalist 175, E105E118.
Choo, K., Williams, P. D. and Day, T. (2003). Host mortality, predation and the evolution of parasite virulence. Ecology Letters 6, 310315.
Claessen, D. and de Roos, A. M. (1995). Evolution of virulence in a host-pathogen system with local pathogen transmission. Oikos 74, 401.
Coombs, D., Gilchrist, M. A. and Ball, C. L. (2007). Evaluating the importance of within- and between-host selection pressures on the evolution of chronic pathogens. Theoretical Population Biology 72, 576591.
Cooper, V. S., Reiskind, M. H., Miller, J. A., Shelton, K. A., Walther, B. A., Elkinton, J. S. and Ewald, P. W. (2002). Timing of transmission and the evolution of virulence of an insect virus. Proceedings of the Royal Society B: Biological Sciences 269, 11611165.
Cox, F. E. (2001). Concomitant infections, parasites and immune responses. Parasitology 122(Suppl), S23S38.
Cressler, C. E., Nelson, W. A., Day, T. and McCauley, E. (2014). Disentangling the interaction among host resources, the immune system and pathogens. Ecology Letters 17, 284293.
Day, T. (2001). Parasite transmission modes and the evolution of virulence. Evolution 55, 23892400.
Day, T. (2002 a). On the evolution of virulence and the relationship between various measures of mortality. Proceedings of the Royal Society B: Biological Sciences 269, 13171323.
Day, T. (2002 b). The evolution of virulence in vector-borne and directly transmitted parasites. Theoretical Population Biology 62, 199213.
Day, T. (2002 c). Virulence evolution via host exploitation and toxin production in spore-producing pathogens. Ecology Letters 5, 471476.
Day, T., Alizon, S. and Mideo, N. (2011). Bridging scales in the evolution of infectious disease life histories: theory. Evolution (N. Y) 65, 34483461.
Day, T. and Gandon, S. (2006). Insights from Price's equation into evolutionary epidemiology. DIMACS Series in Discrete Mathematics 71, 2344.
Day, T. and Gandon, S. (2007). Applying population-genetic models in theoretical evolutionary epidemiology. Ecology Letters 10, 876888.
Day, T., Graham, A. L. and Read, A. F. (2007). Evolution of parasite virulence when host responses cause disease. Proceedings of the Royal Society B: Biological Sciences 274, 26852692.
Day, T. and Proulx, S. R. (2004). A general theory for the evolutionary dynamics of virulence. American Naturalist 163, E40E63.
De Paepe, M. and Taddei, F. (2006). Viruses’ life history: towards a mechanistic basis of a trade-off between survival and reproduction among phages. PLoS Biology 4, 12481256.
de Roode, J. C., Pansini, R., Cheesman, S. J., Helinski, M. E. H., Huijben, S., Wargo, A. R., Bell, A. S., Chan, B. H. K., Walliker, D. and Read, A. F. (2005). Virulence and competitive ability in genetically diverse malaria infections. Proceedings of the National Academy of Sciences of the United States of America 102, 76247628.
Dennehy, J. J., Abedon, S. T. and Turner, P. E. (2007). Host density impacts relative fitness of bacteriophage Φ6 genotypes in structured habitats. Evolution (N. Y) 61, 25162527.
Dusi, E., Gougat-Barbera, C., Berendonk, T. U. and Kaltz, O. (2015). Long-term selection experiment produces breakdown of horizontal transmissibility in parasite with mixed transmission mode. Evolution 69, 10691076.
Ebert, D. (1998). Experimental evolution of parasites. Science 282, 14321435.
Ebert, D. (2013). The epidemiology and evolution of symbionts with mixed-mode transmission. Annual Review of Ecology, Evolution, and Systematics 44, 623643.
Ebert, D. and Bull, J. J. (2003). Challenging the trade-off model for the evolution of virulence. Trends in Microbiology 11, 1520.
Ebert, D. and Mangin, K. L. K. (1997). The influence of host demography on the evolution of virulence of a microsporidian gut parasite. Evolution (N. Y) 51, 1828.
Ebert, D. and Weisser, W. W. (1997). Optimal killing for obligate killers: the evolution of life histories and virulence of semelparous parasites. Proceedings of the Royal Society B: Biological Sciences 264, 985991.
Elliot, S. L., Adler, F. R. and Sabelis, M. W. (2003). How virulent should a pararite be to its vector? Ecology 84, 25682574.
Eshelman, C. M., Vouk, R., Stewart, J. L., Halsne, E., Lindsey, H. A., Schneider, S., Gualu, M., Dean, A. M. and Kerr, B. (2010). Unrestricted migration favours virulent pathogens in experimental metapopulations: evolutionary genetics of a rapacious life history. Philosophical Transactions of the Royal Society of London B: Biological Sciences 365, 25032513.
Ewald, P. W. (1983). Host-parasite relations, vectors, and the evolution of disease severity. Annual Review of Ecology and Systematics 14, 465485.
Ewald, P. W. (1991). Waterborne transmission and the evolution of virulence among gastrointestinal bacteria. Epidemiology & Infection 106, 83119.
Ewald, P. W. (1994). Evolution of Infectious Diseases. Oxford University Press, Oxford, UK.
Fenner, F. and Ratcliffe, F. N. (1965). Myxomatosis. Cambridge University Press, New York.
Fenton, A. and Perkins, S. E. (2010). Applying predator-prey theory to modelling immune-mediated, within-host interspecific parasite interactions. Parasitology 137, 10271038.
Ferguson, H. M. and Read, A. F. (2002). Genetic and environmental determinants of malaria parasite virulence in mosquitoes. Proceedings of the Royal Society B: Biological Sciences 269, 12171224.
Ferguson, N. M., Galvani, A. P. and Bush, R. M. (2003). Ecological and immunological determinants of influenza evolution. Nature 422, 428433.
Frank, S. A. (1992). A kin selection model for the evolution of virulence. Proceedings of the Royal Society B: Biological Sciences 250, 195197.
Frank, S. A. (1996). Models of parasite virulence. Quarterly Review of Biology 71, 3778.
Frank, S. A. and Schmid-Hempel, P. (2008). Mechanisms of pathogenesis and the evolution of parasite virulence. Journal of Evolutionary Biology 21, 396404.
Fraser, C., Lythgoe, K., Leventhal, G. E., Shirreff, G., Hollingsworth, T. D., Alizon, S. and Bonhoeffer, S. (2014). Virulence and pathogenesis of HIV-1 infection: an evolutionary perspective. Science 343, 1243727.
Froissart, R., Doumayrou, J., Vuillaume, F., Alizon, S. and Michalakis, Y. (2010). The virulence-transmission trade-off in vector-borne plant viruses: a review of (non-)existing studies. Philosophical Transactions of the Royal Society of London B: Biological Sciences 365, 19071918.
Gadgil, M. and Bossert, W. H. (1970). Life historical consequences of natural selection. American Naturalist 104, 124.
Gandon, S. (1998). The curse of the pharoah hypothesis. Proceedings of the Royal Society B: Biological Sciences 265, 15451552.
Gandon, S. and Day, T. (2007). The evolutionary epidemiology of vaccination. Journal of the Royal Society Interface 4, 803817.
Gandon, S. and Day, T. (2008). Evidences of parasite evolution after vaccination. Vaccine 26, 2326.
Gandon, S., Jansen, V. A. A. and Van Baalen, M. (2001 a). Host life history and the evolution of parasite virulence. Evolution (N. Y) 55, 10561062.
Gandon, S., Mackinnon, M. J., Nee, S. and Read, A. F. (2001 b). Imperfect vaccines and the evolution of pathogen virulence. Nature 414, 751756.
Gandon, S., Mackinnon, M. J., Nee, S. and Read, A. F. (2002). Antitoxin vaccines and pathogen virulence: reply. Nature 417, 610.
Gandon, S., Mackinnon, M., Nee, S. and Read, A. (2003). Imperfect vaccination: some epidemiological and evolutionary consequences. Proceedings of the Royal Society B: Biological Sciences 270, 11291136.
Ganusov, V. V. and Antia, R. (2006). Imperfect vaccines and the evolution of pathogens causing acute infections in vertebrates. Evolution 60, 957969.
Ganusov, V. V., Bergstrom, C. T. and Antia, R. (2002). Within-host population dynamics and the evolution of microparasites in a heterogeneous host population. Evolution 56, 213223.
Garbutt, J., Bonsall, M. B., Wright, D. J. and Raymond, B. (2011). Antagonistic competition moderates virulence in Bacillus thuringiensis. Ecology Letters 14, 765772.
Gardner, A., West, S. A. and Buckling, A. (2004). Bacteriocins, spite and virulence. Proceedings of the Royal Society B: Biological Sciences 271, 15291535.
Gilchrist, M. A. and Coombs, D. (2006). Evolution of virulence: Interdependence, constraints, and selection using nested models. Theoretical Population Biology 69, 145153.
Gilchrist, M. A. and Sasaki, A. (2002). Modeling host-parasite coevolution: a nested approach based on mechanistic models. Journal of Theoretical Biology 218, 289308.
Grech, K., Chan, B. H. K., Anders, R. F. and Read, A. F. (2008). The impact of immunization on competition within Plasmodium infections. Evolution 62, 23592371.
Griffin, A. S., West, S. A. and Buckling, A. (2004). Cooperation and competition in pathogenic bacteria. Nature 430, 10241027.
Haine, E. R. (2008). Symbiont-mediated protection. Proceedings of the Royal Society B: Biological Sciences 275, 353361.
Haraguchi, Y. and Sasaki, A. (2000). The evolution of parasite virulence and transmission rate in a spatially structured population. Journal of Theoretical Biology 203, 8596.
Harrison, F., Browning, L. E., Vos, M. and Buckling, A. (2006). Cooperation and virulence in acute Pseudomonas aeruginosa infections. BMC Biology 4, 21.
Herre, E. A. (1993). Population structure and the evolution of virulence in nematode parasites of fig wasps. Science 259, 14421445.
Holt, R. D. (1977). Predation, apparent competition, and the structure of prey communities. Theoretical Population Biology 12, 197229.
Inglis, R. F., Gardner, A., Cornelis, P. and Buckling, A. (2009). Spite and virulence in the bacterium Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences of the United States of America 106, 57035707.
Jones, E. O., White, A. and Boots, M. (2007). Interference and the persistence of vertically transmitted parasites. Journal of Theoretical Biology 246, 1017.
Jones, E. O., White, A. and Boots, M. (2011). The evolution of host protection by vertically transmitted parasites. Proceedings of the Royal Society B: Biological Sciences 278, 863870.
Kakehashi, M. and Yoshinaga, F. (1992). Evolution of airborne infectious diseases according to changes in characteristics of the host population. Ecological Research 7, 235243.
Kaltz, O. and Koella, J. C. (2003). Host growth conditions regulate the plasticity of horizontal and vertical transmission in \emph{Holospora undulata}, a bacterial parasite of the protozoan Paramecium caudatum . Evolution 57, 15351542.
Kamo, M., Sasaki, A. and Boots, M. (2007). The role of trade-off shapes in the evolution of parasites in spatial host populations: an approximate analytical approach. Journal of Theoretical Biology 244, 588596.
Kerr, B., Neuhauser, C., Bohannan, B. J. M. and Dean, A. M. (2006). Local migration promotes competitive restraint in a host-pathogen ‘tragedy of the commons‘. Nature 442, 7578.
Kisdi, E., Geritz, S. A. H. and Boldin, B. (2013). Evolution of pathogen virulence under selective predation: a construction method to find eco-evolutionary cycles. Journal of Theoretical Biology 339, 140150.
Lambrechts, L. and Scott, T. W. (2009). Mode of transmission and the evolution of arbovirus virulence in mosquito vectors. Proceedings of the Royal Society B: Biological Sciences 276, 13691378.
Leggett, H. C., Cornwallis, C. K. and West, S. A. (2012). Mechanisms of pathogenesis, infective dose and virulence in human parasites. PLoS Pathogens 8, 1012.
Lenski, R. E. and May, R. M. (1994). The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. Journal of Theoretical Biology 169, 253265.
Levin, S. and Pimentel, D. (1981). Selection of intermediate rates of increase in parasite-host systems. American Naturalist 117, 308315.
Lion, S. (2013). Multiple infections, kin selection and the evolutionary epidemiology of parasite traits. Journal of Evolutionary Biology 26, 21072122.
Lion, S. and Boots, M. (2010). Are parasites “prudent” in space? Ecology Letters 13, 12451255.
Lipsitch, M., Herre, E. A. and Nowak, M. A. (1995 a). Host population structure and the evolution of virulence: a “law of diminishing returns”. Evolution 49, 743748.
Lipsitch, M., Nowak, M. A., Ebert, D. and May, R. M. (1995 b). The population dynamics of vertically and horizontally transmitted parasites. Proceedings of the Royal Society B: Biological Sciences 260, 321327.
Lipsitch, M., Siller, S. and Nowak, M. (1996). The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50, 17291741.
Lipsitch, M., Colijn, C., Cohen, T., Hanage, W. P. and Fraser, C. (2009). No coexistence for free: neutral null models for multistrain pathogens. Epidemics 1, 213.
Long, G. H. and Graham, A. L. (2011). Consequences of immunopathology for pathogen virulence evolution and public health: Malaria as a case study. Evolutionary Applications 4, 278291.
Luciani, F. and Alizon, S. (2009). The evolutionary dynamics of a rapidly mutating virus within and between hosts: the case of hepatitis C virus. PLoS Computational Biology 5, e1000565.
Lythgoe, K. A., Pellis, L. and Fraser, C. (2013). Is Hiv short-sighted? Insights from a multistrain nested model. Evolution (N. Y) 67, 27692782.
Mackinnon, M. J., Gandon, S. and Read, A. F. (2008). Virulence evolution in response to vaccination: the case of malaria. Vaccine 26, 4252.
Mackinnon, M. J. and Read, A. F. (2004). Immunity promotes virulence evolution in a malaria model. PLoS Biology 2, e230.
Magalon, H., Nidelet, T., Martin, G. and Kaltz, O. (2010). Host growth conditions influence experimental evolution of life history and virulence of a parasite with vertical and horizontal transmission. Evolution 64, 21262138.
Massey, R. C., Buckling, A. and Ffrench-Constant, R. (2004). Interference competition and parasite virulence. Proceedings of the Royal Society B: Biological Sciences 271, 785788.
May, R. M. and Nowak, M. A. (1995). Coinfection and the evolution of parasite virulence. Proceedings of the Royal Society B: Biological Sciences 261, 209215.
McLean, A. R. (1995). Vaccination, evolution and changes in the efficacy of vaccines: a theoretical framework. Proceedings of the Royal Society B: Biological Sciences 261, 389393.
Mennerat, A., Nilsen, F., Ebert, D. and Skorping, A. (2010). Intensive farming: evolutionary implications for parasites and pathogens. Evolutionary Biology 37, 5967.
Messenger, S. L., Molineux, I. J. and Bull, J. J. (1999). Virulence evolution in a virus obeys a trade-off. Proceedings of the Royal Society B: Biological Sciences 266, 397404.
Messinger, S. M. and Ostling, A. (2009). The consequences of spatial structure for the evolution of pathogen transmission rate and virulence. American Naturalist 174, 441454.
Messinger, S. M. and Ostling, A. (2013). The influence of host demography, pathogen virulence, and relationships with pathogen virulence on the evolution of pathogen transmission in a spatial context. Evolutionary Ecology 27, 353380.
Metcalf, C. J. E., Birger, R., Funk, S., Kouyos, R. D., Lloyd-Smith, J. O. and Jansen, V. A. A. (2015). Five challenges in evolution and infectious disease. Epidemics 10, 4044.
Mideo, N. (2009). Parasite adaptations to within-host competition. Trends in parasitology 25, 261268.
Mideo, N., Alizon, S. and Day, T. (2008). Linking within- and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends in Ecology & Evolution 23, 511517.
Mideo, N., Nelson, W. A., Reece, S. E., Bell, A. S., Read, A. F. and Day, T. (2011). Bridging scales in the evolution of infectious disease life histories: application. Evolution (N. Y) 65, 32983310.
Mikonranta, L., Friman, V. P. and Laakso, J. (2012). Life history trade-offs and relaxed selection can decrease bacterial virulence in environmental reservoirs. PLoS ONE 7, 19.
Mooi, F. R., Van Loo, I. H. M. and King, A. J. (2001). Adaptation of Bordetella pertussis to vaccination: a cause for its reemergence? Emerging Infectious Diseases 7, 526528.
Mooi, F. R., Van Loo, I. H. M., Van Gent, M., He, Q., Bart, M. J., Heuvelman, K. J., De Greeff, S. C., Diavatopoulos, D., Teunis, P., Nagelkerke, N. and Mertsola, J. (2009). Bordetella pertussis strains with increased toxin production associated with pertussis resurgence. Emerging Infectious Diseases 15, 12061213.
Morozov, A. and Best, A. (2012). Predation on infected host promotes evolutionary branching of virulence and pathogens’ biodiversity. Journal of Theoretical Biology 307, 2936.
Morozov, A. Y. and Adamson, M. W. (2011). Evolution of virulence driven by predator-prey interaction: possible consequences for population dynamics. Journal of Theoretical Biology 276, 181191.
Mosquera, J. and Adler, F. R. (1998). Evolution of virulence: a unified framework for coinfection and superinfection. Journal of Theoretical Biology 195, 293313.
Nidelet, T., Koella, J. C. and Kaltz, O. (2009). Effects of shortened host life span on the evolution of parasite life history and virulence in a microbial host-parasite system. BMC Evolutionary Biology 9, 65.
Nowak, M. A. and May, R. M. (1994). Superinfection and the evolution of parasite virulence. Proceedings of the Royal Society B: Biological Sciences 255, 8189.
Octavia, S., Maharjan, R. P., Sintchenko, V., Stevenson, G., Reeves, P. R., Gilbert, G. L. and Lan, R. (2011). Insight into evolution of \emph{Bordetella pertussis} from comparative genomic analysis: evidence of vaccine-driven selection. Molecular Biology and Evolution 28, 707715.
Ogbunugafor, C. B., Alto, B. W., Overton, T. M., Bhushan, A., Morales, N. M. and Turner, P. E. (2013). Evolution of increased survival in RNA viruses specialized on cancer-derived cells. American Naturalist 181, 585–95.
O'Keefe, K. J. and Antonovics, J. (2002). Playing by different rules: the evolution of virulence in sterilizing pathogens. American Naturalist 159, 597605.
Pagán, I., Montes, N., Milgroom, M. G. and García-Arenal, F. (2014). Vertical transmission selects for reduced virulence in a plant virus and for increased resistance in the host. PLoS Pathogens 10, 2325.
Payne, R., Muenchhoff, M., Mann, J., Roberts, H. E., Matthews, P., Adland, E., Hempenstall, A., Huang, K. H., Brockman, M., Brumme, Z., Sinclair, M., Miura, T., Frater, J., Essex, M., Shapiro, R., Walker, B. D., Ndung'u, T., McLean, A. R., Carlson, J. M. and Goulder, P. J. R. (2014). Impact of HLA-driven HIV adaptation on virulence in populations of high HIV seroprevalence. Proceedings of the National Academy of Sciences of the United States of America 111, E5393E5400.
Pedersen, A. B. and Fenton, A. (2007). Emphasizing the ecology in parasite community ecology. Trends in Ecology & Evolution 22, 133139.
Pollitt, E. J. G., West, S. A., Crusz, S. A., Burton-Chellew, M. N. and Diggle, S. P. (2014). Cooperation, quorum sensing, and evolution of virulence in Staphylococcus aureus. Infection and Immunity 82, 10451051.
Raberg, L., de Roode, J. C., Bell, A. S., Stamou, P., Gray, D. and Read, A. F. (2006). The role of immune-mediated apparent competition in genetically diverse malaria infections. American Naturalist 168, 4153.
Read, A. F. (1994). The evolution of virulence. Trends in Microbiology 2, 7376.
Read, A. F., Baigent, S. J., Powers, C., Kgosana, L. B., Blackwell, L., Smith, L. P., Kennedy, D. A., Walkden-Brown, S. W. and Nair, V. K. (2015). Imperfect vaccination can enhance the transmission of highly virulent pathogens. PLoS Biology
Read, A. F. and Taylor, L. H. (2001). The ecology of genetically diverse infections. Science 292, 10991102.
Read, J. M. and Keeling, M. J. (2006). Disease evolution across a range of spatio-temporal scales. Theoretical Population Biology 70, 201213.
Rumbaugh, K. P., Trivedi, U., Watters, C., Burton-Chellew, M. N., Diggle, S. P. and West, S. A. (2012). Kin selection, quorum sensing and virulence in pathogenic bacteria. Proceedings of the Royal Society B: Biological Sciences 279, 35843588.
Sasaki, A. and Iwasa, Y. (1991). Optimal growth schedule of pathogens with a host: switching between lytic and latent cycles. Theoretical Population Biology 39, 201239.
Schmid-Hempel, P. (2011). Evolutionary Parasitology. Oxford University Press, Oxford, UK.
Schmid-Hempel, P. and Frank, S. A. (2007). Pathogenesis, virulence, and infective dose. PLoS Pathogens 3, 13721373.
Schneider, D. S. and Ayres, J. S. (2008). Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Natural Reviews Immunology 8, 889895.
Shim, E. and Galvani, A. P. (2009). Evolutionary repercussions of avian culling on host resistance and influenza virulence. PLoS ONE 4, 18.
Smithers, S. R. and Terry, R. J. (1969). Immunity in schistosomiasis. Annals of the New York Academy of Sciences 160, 826840.
Soubeyrand, B. and Plotkin, S. A. (2002). Antitoxin vaccines and pathogen virulence. Nature 417, 609610.
Stewart, A. D., Logsdon, J. M. and Kelley, S. E. (2005). An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution 59, 730739.
Sundberg, L. R., Kunttu, H. M. T. and Valtonen, E. T. (2014). Starvation can diversify the population structure and virulence strategies of an environmentally transmitting fish pathogen. BMC Microbiology 14, 67.
Turner, P., Cooper, V. and Lenski, R. (1998). Tradeoff between horizontal and vertical modes of transmission in bacterial plasmids. Evolution 52, 315329.
Turner, P. E. and Chao, L. (1999). Prisoner's dilemma in an RNA virus. Nature 398, 441443.
Vale, P. F., Fenton, A. and Brown, S. P. (2014). Limiting damage during infection: lessons from infection tolerance for Novel Therapeutics. PLoS Biology 12, e1001769.
van Baalen, M. (2002). Contact networks and the evolution of virulence. In Adapt. Dyn. Infect. Dis. Purs. Virulence Manag. (ed. Dieckmann, U., Metz, J. A. J., Sabelis, M. W. and Sigmund, K.), pp. 85103. Cambridge University Press, Cambridge, UK.
van Baalen, M. and Sabelis, M. W. (1995 a). The dynamics of multiple infection and the evolution of virulence. American Naturalist 146, 881.
van Baalen, M. and Sabelis, M. W. (1995 b). The scope for virulence management: a comment on Ewald's view on the evolution of virulence. Trends in Microbiology 3, 414416.
van Boven, M., Mooi, F. R., Schellekens, J. F. P., de Melker, H. E. and Kretzschmar, M. (2005). Pathogen adaptation under imperfect vaccination: implications for pertussis. Proceedings of the Royal Society B: Biological Sciences 272, 16171624.
Walther, B. A. and Ewald, P. W. (2004). Pathogen survival in the external environment and the evolution of virulence. Biological Review of the Cambridge Philosophical Society 79, 849869.
Wasik, B. R., Bhushan, A., Ogbunugafor, C. B. and Turner, P. E. (2015). Delayed transmission selects for increased survival of vesicular stomatitis virus. Evolution 69, 117125.
West, S. A. and Buckling, A. (2003). Cooperation, virulence and siderophore production in bacterial parasites. Proceedings of the Royal Society B: Biological Sciences 270, 3744.
Wild, G., Gardner, A. and West, S. A. (2009). Adaptation and the evolution of parasite virulence in a connected world. Nature 459, 983986.
Williams, P. D. and Day, T. (2001). Interactions between sources of mortality and the evolution of parasite virulence. Proceedings of the Royal Society B: Biological Sciences 268, 23312337.
Williams, P. D. and Day, T. (2008). Epidemiological and evolutionary consequences of targeted vaccination. Molecular Ecology 17, 485499.
Witter, R. L. (1997). Increased virulence of Marek's disease virus field isolates. Avian Diseases 41, 149163.

Keywords

The adaptive evolution of virulence: a review of theoretical predictions and empirical tests

  • CLAYTON E. CRESSLER (a1) (a2), DAVID V. McLEOD (a1), CARLY ROZINS (a1), JOSÉE VAN DEN HOOGEN (a1) and TROY DAY (a1) (a2) (a3)...

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