Challenging the trade-off model for the evolution of virulence: is virulence management feasible?

Progress in understanding the evolution of infectious diseases has inspired proposals to manage the evolution of pathogen (including parasite) virulence. A common view is that social interventions that lower pathogen transmission will indirectly select lower virulence because of a trade-off between transmission and virulence. Here, we argue that there is little theoretical justification and no empirical evidence for this plan. Although a trade-off model might apply to some pathogens, the mechanism appears too weak for rapid selection of substantial changes in virulence. Direct selection against virulence itself might be a more rewarding approach to managing the evolution of virulence.

[1]  M. Hochberg.  ESTABLISHING GENETIC CORRELATIONS INVOLVING PARASITE VIRULENCE , 1998, Evolution; international journal of organic evolution.

[2]  A. Gibbs,et al.  Molecular Basis of Virus Evolution , 2005 .

[3]  A. Read,et al.  Selection for high and low virulence in the malaria parasite , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[4]  R. Weiss,et al.  Virulence and pathogenesis. , 2002, Trends in microbiology.

[5]  M. Baalen,et al.  The scope for virulence management: a comment on Ewald's view on the evolution of virulence. , 1995, Trends in microbiology.

[6]  D. Falconer,et al.  Introduction to Quantitative Genetics. , 1962 .

[7]  Paul W. Ewald.  Imperfect Vaccines and the Evolution of Pathogen Virulence , 2004 .

[8]  Maurice W. Sabelis,et al.  The Dynamics of Multiple Infection and the Evolution of Virulence , 1995, The American Naturalist.

[9]  P. Thrall,et al.  SEXUALLY TRANSMITTED DISEASES IN ANIMALS: ECOLOGICAL AND EVOLUTIONARY IMPLICATIONS , 1996, Biological reviews of the Cambridge Philosophical Society.

[10]  L. H. Taylor,et al.  VIRULENCE OF MIXED‐CLONE AND SINGLE‐CLONE INFECTIONS OF THE RODENT MALARIA PLASMODIUM CHABAUDI , 1998, Evolution; international journal of organic evolution.

[11]  M. Carrington,et al.  Association of HLA profiles with early plasma viral load, CD4+ cell count and rate of progression to AIDS following acute HIV‐1 infection , 1998, AIDS.

[12]  J. Bull,et al.  MOLECULAR GENETICS OF ADAPTATION IN AN EXPERIMENTAL MODEL OF COOPERATION , 1992, Evolution; international journal of organic evolution.

[13]  Janice Moore.  Parasites and the Behavior of Animals , 2002 .

[14]  D. Ebert,et al.  The evolution of parasitic diseases. , 1996, Parasitology today.

[15]  B. Levin,et al.  Selection and evolution of virulence in bacteria: an ecumenical excursion and modest suggestion , 1990, Parasitology.

[16]  D. Ebert.  Experimental evolution of parasites. , 1998, Science.

[17]  Steven A. Frank,et al.  Models of Parasite Virulence , 1996, The Quarterly Review of Biology.

[18]  S. Nee,et al.  Microbial evolution (Communication arising): Antitoxin vaccines and pathogen virulence , 2002, Nature.

[19]  M A Nowak,et al.  Superinfection and the evolution of parasite virulence. , 1994, Proceedings. Biological sciences.

[20]  T. Day.  PARASITE TRANSMISSION MODES AND THE EVOLUTION OF VIRULENCE , 2001, Evolution; international journal of organic evolution.

[21]  A. Read,et al.  GENETIC RELATIONSHIPS BETWEEN PARASITE VIRULENCE AND TRANSMISSION IN THE RODENT MALARIA PLASMODIUM CHABAUDI , 1999, Evolution; international journal of organic evolution.

[22]  F. M. Stewart,et al.  Epidemiology, evolution, and future of the HIV/AIDS pandemic. , 2001, Emerging infectious diseases.

[23]  Martin A Nowak,et al.  THE EVOLUTION OF VIRULENCE IN PATHOGENS WITH VERTICAL AND HORIZONTAL TRANSMISSION , 1996, Evolution; international journal of organic evolution.

[24]  HOMAS,et al.  VIRAL LOAD AND HETEROSEXUAL TRANSMISSION OF HUMAN IMMUNODEFICIENCY VIRUS TYPE 1 VIRAL LOAD AND HETEROSEXUAL TRANSMISSION OF HUMAN IMMUNODEFICIENCY VIRUS TYPE 1 , 2000 .

[25]  R M May,et al.  Coevolution of hosts and parasites , 1982, Parasitology.

[26]  L. H. Taylor,et al.  Determinants of transmission success of individual clones from mixed-clone infections of the rodent malaria parasite, Plasmodium chabaudi. , 1998, International journal for parasitology.

[27]  Rustom Antia,et al.  WITHIN‐HOST POPULATION DYNAMICS AND THE EVOLUTION OF MICROPARASITES IN A HETEROGENEOUS HOST POPULATION , 2002, Evolution; international journal of organic evolution.

[28]  S. Pagani,et al.  Evidence of increased carriage of Corynebacterium spp. in healthy individuals with low antibody titres against diphtheria toxoid , 2000, Epidemiology and Infection.

[29]  C. Dennis.  The bugs of war , 2001, Nature.

[30]  George C. Williams,et al.  The Dawn of Darwinian Medicine , 1991, The Quarterly Review of Biology.

[31]  Martin A. Nowak,et al.  Superinfection and the evolution of parasite virulence , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[32]  D. Ebert.  Virulence and Local Adaptation of a Horizontally Transmitted Parasite , 1994, Science.

[33]  V. T. Contreras,et al.  Trypanosoma cruzi: metacyclogenesis in vitro--I. Changes in the properties of metacyclic trypomastigotes maintained in the laboratory by different methods. , 1994, Memorias do Instituto Oswaldo Cruz.

[34]  T. Day.  Virulence evolution via host exploitation and toxin production in spore-producing pathogens , 2002 .

[35]  A. Galazka.  The changing epidemiology of diphtheria in the vaccine era. , 2000, The Journal of infectious diseases.

[36]  Sam P. Brown,et al.  Does multiple infection select for raised virulence? , 2002, Trends in microbiology.

[37]  Rustom Antia,et al.  Within-Host Population Dynamics and the Evolution and Maintenance of Microparasite Virulence , 1994, The American Naturalist.

[38]  C. Calisher,et al.  Transmission of an arenavirus in white-throated woodrats (Neotoma albigula), southeastern Colorado, 1995-1999. , 2001, Emerging infectious diseases.

[39]  D. Ebert,et al.  THE INFLUENCE OF HOST DEMOGRAPHY ON THE EVOLUTION OF VIRULENCE OF A MICROSPORIDIAN GUT PARASITE , 1997, Evolution; international journal of organic evolution.

[40]  J. Jaenike.  SUBOPTIMAL VIRULENCE OF AN INSECT‐PARASITIC NEMATODE , 1996, Evolution; international journal of organic evolution.

[41]  E. Herre.  Population Structure and the Evolution of Virulence in Nematode Parasites of Fig Wasps , 1993, Science.

[42]  J. Bull,et al.  SELECTION OF BENEVOLENCE IN A HOST–PARASITE SYSTEM , 1991, Evolution; international journal of organic evolution.

[43]  J. Bull,et al.  Virulence evolution in a virus obeys a trade off , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[44]  C. M. Pease,et al.  A critique of methods for measuring life history trade‐offs , 1988 .

[45]  R. Lenski,et al.  TRADEOFF BETWEEN HORIZONTAL AND VERTICAL MODES OF TRANSMISSION IN BACTERIAL PLASMIDS , 1998, Evolution; international journal of organic evolution.

[46]  S. Elena.  Evolutionary history conditions the timing of transmission in vesicular stomatitis virus. , 2001, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[47]  R. May,et al.  The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. , 1994, Journal of theoretical biology.

[48]  B. R. Levin,et al.  The evolution and maintenance of virulence in microparasites. , 1996, Emerging infectious diseases.

[49]  D. Ebert,et al.  Optimal killing for obligate killers: the evolution of life histories and virulence of semelparous parasites , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[50]  F. M. Stewart,et al.  The intrinsic rate of increase of HIV/AIDS: epidemiological and evolutionary implications. , 1996, Mathematical biosciences.

[51]  T. Day.  Virulence evolution and the timing of disease life-history events , 2003 .

[52]  J. Bull,et al.  Short-sighted evolution and the virulence of pathogenic microorganisms. , 1994, Trends in microbiology.

[53]  P. Ewald,et al.  Host-Parasite Relations, Vectors, and the Evolution of Disease Severity , 1983 .

[54]  S. Plotkin,et al.  Microbial evolution: antitoxin vaccines and pathogen virulence. , 2002, Nature.

[55]  F. Adler,et al.  Virulence management in biocontrol agents , 2002 .

[56]  M. Lipsitch,et al.  Virulence and transmissibility of pathogens: what is the relationship? , 1997, Trends in microbiology.

[57]  U. Mackenstedt,et al.  Reduction of transmission stages concomitant with increased host immune responses to hypervirulent Sarcocystis singaporensis, and natural selection for intermediate virulence. , 2001, International journal for parasitology.

[58]  K. Mendis,et al.  Quantifying genetic and nongenetic contributions to malarial infection in a Sri Lankan population. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Jenn K Thompson,et al.  Genes necessary for expression of a virulence determinant and for transmission of Plasmodium falciparum are located on a 0.3-megabase region of chromosome 9. , 1993, Proceedings of the National Academy of Sciences of the United States of America.