Skip to main content
SpringerLink
Log in

Co-evolution between Hosts and Infectious Disease Agents and its Effects on Virulence

  • Conference paper
Population Biology of Infectious Diseases

Part of the book series: Dahlem Workshop Reports ((DAHLEM LIFE,volume 25))

Abstract

Protozoan parasites have evolved several mechanisms to overcome vertebrate host defenses. These include intracellular location, antigenic variation, antigen-specific immunosuppression, and nonspecific immunosuppression. In response to the challenge of infectious diseases, mammalian hosts have developed several mechanisms for limiting parasitic infections. Some of these are conventional immune responses, involving the formation of specific antibodies, T-lymphocytes that can kill infected cells, and T-lymphocytes that can activate macrophages in such a way that they limit the multiplication of parasites. Other mechanisms of resistance have also evolved, including inherited variations in hemoglobin and erythrocyte enzymes and structure that can limit their capacity to support parasite replication. As a result of selection through parasitic disease, stable polymorphisms have developed.

The transmission of parasites by arthropods introduces a further level of complexity and necessity for co-evolution of the parasites and both hosts, ensuring the survival of all of them in nature. When hosts and parasites have lived together for a long time, as in the case of African parasites and wild animals, the hosts have developed efficient mechanisms of resistance and the infections are of low virulence. When the time of coexistence is intermediate, as in the case of indigenous domestic livestock, the same parasites produce infections of intermediate virulence, whereas in newly introduced hosts they produce highly virulent infections. Such graded responses strongly suggest that co-evolution can result in attenuated infections.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allison, A.C. 1954. The distribution of the sickle-cell trait in East Africa and elsewhere, and its apparent relationship to the incidence of subtertian malaria. Trans. R. Soc. Trop. Med. Hyg. 48: 312–338.

    Article  PubMed  CAS  Google Scholar 

  2. Allison, A.C. 1954. Protection afforded by the sickle-cell trait against subtertian malarial infection. Brit. Med. J. 1: 290–294.

    Article  PubMed  CAS  Google Scholar 

  3. Allison, A.C. 1954. Notes on sickle-cell polymorphism. Ann. Hum. Genet. 19: 39–51.

    Article  PubMed  CAS  Google Scholar 

  4. Allison, A.C. 1960. Glucose-6-phosphate dehydrogenase deficiency in red blood cells of East Africans. Nature 186: 531–532.

    Article  PubMed  CAS  Google Scholar 

  5. Allison, A.C. 1964. Polymorphism and natural selection in human populations. Cold Spr. Harb. Symp. Quant. Biol. 29: 137–149.

    CAS  Google Scholar 

  6. Allison, A.C. 1981. Cellular immune response in theileriosis. In Advances in the Control of Theileriosis, eds. A.D. Irvin, M.P. Cunningham, and A.S. Young. The Hague: M. Nyhoff.

    Google Scholar 

  7. Allison, A.C., and Clyde, D.F. 1961. Malaria in African children with deficient erythrocyte glucose-6-phos-phate dehydrogenase. Brit. Med. J. 1: 1366–1348.

    Article  Google Scholar 

  8. Ashcroft, M.T.; Burtt, E.; and Fairburn, H. 1959. The experimental infection of some African wild animals with Trypanosoma rhodesiense, T. Brucei and T. congolense. Ann. Trop. Med. Parasitol. 53: 147–161.

    PubMed  CAS  Google Scholar 

  9. Beaven, G.H.; Ellis, M.J.; and White, J.C. 1961. Studies on human foetal haemoglobin. III. The hereditary haemoglobinopathies and thalassaemias. Brit. J. Haematol. 7: 169–186.

    Article  CAS  Google Scholar 

  10. Bienzle, U.; Ayeni, O.; Lucas, A.O.; and Luzzatto, L. 1972. Glucose-6-phosphate dehydrogenase and malaria. Greater resistance of females heterozygous for enzyme deficiency and males with non-deficient variant. Lancet i: 107–110.

    Article  Google Scholar 

  11. Bodmer, W.F. 1972. Evolutionary significance of the H-LA system. Nature 237: 139–145.

    Article  PubMed  CAS  Google Scholar 

  12. Brown, K.N. 1977. Antigenic variation. In Immunity in Parasitic Diseases, vol. 72, pp. 59–70. Paris: Colloque Inserm.

    Google Scholar 

  13. Cavalli-Sforza, L., and Bodmer, W.F. 1971. The Genetics of Human Populations. San Francisco: Freeman.

    Google Scholar 

  14. Clark, I.A., and Allison, A.C. 1974. Babesia microti and Plasmodium berghei yoelii infections in nude mice. Nature 252: 328–329.

    Article  PubMed  CAS  Google Scholar 

  15. Coatney, G.R.; Collins, W.E.; McWarren, W.; and Contacos, P.G. 1977. The Primate Malarias, pp. 1–366. Washington, DC: US Government Printing Office.

    Google Scholar 

  16. Cohen, S.; McGregor, I.A.; and Carrington, S. 1961. Gamma-globulin and acquired immunity to human malaria. Nature 192: 733–737.

    Article  PubMed  CAS  Google Scholar 

  17. Cross, G.A.M. 1975. Identification, purification and properties of clone-specific glycoprotein antigens constituting the surface coat of Trypanosoma brucei. Parasitology 71: 393–417.

    Article  PubMed  CAS  Google Scholar 

  18. Eaton, J.W.; Eckman, J.R.; Berger, E.; and Jacob, H.S. 1976. Suppression of malaria infection by oxidant-sensitive host erythrocytes. Nature 264: 758–760.

    Article  PubMed  CAS  Google Scholar 

  19. Etkin, N.L., and Eaton, J.W. 1975. Malaria-induced erythrocyte oxidant sensitivity. In Erythrocyte Structure and Function, ed. G.J. Brewer, pp. 219–234. New York: A.R. Liss, Inc.

    Google Scholar 

  20. Eugui, E.M., and Allison, A.C. 1980. Differences in susceptibility of various mouse strains to haemoprotozoan infections: possible correlation with natural killer activity. Parasite Immunol. 2: 277–299.

    Article  PubMed  CAS  Google Scholar 

  21. Eyles, D.E.; Laing, A.B.G.; McWarren, W.; and Sandosham, A.A. 1962. Malaria parasites in Malayan leaf monkeys of the genus Presbytis. Med. J. Malaya 17: 85–86.

    Google Scholar 

  22. Freeman, R.R.; Trejdosiewicz, A.G.; and Cross, G.A.M. 1980. Protective monoclonal antibodies recognizing stage-specific merozoite antigens of a rodent malarial parasite. Nature 284: 366–368.

    Article  PubMed  CAS  Google Scholar 

  23. Friedman, M.J. 1978. Erythrocytic mechanism of sickle-cell resistance to malaria. Proc. Natl. Acad. Sci. USA 75: 1994–1997.

    Article  PubMed  CAS  Google Scholar 

  24. Friedman, M.J. 1979. Oxidant damage mediates variant red-cell resistance to malaria. Nature 280: 245–247.

    Article  PubMed  CAS  Google Scholar 

  25. Friedman, M.J.; Roth, E.F.; Nagel, R.L.; and Trager, W. 1979. Plasmodium falciparum: Physiological interactions with the human sickle cell. Exp. Parasitol. 47: 73–80.

    Article  PubMed  CAS  Google Scholar 

  26. Friedman, M.J.; Roth, E.F.; Nagel, R.L.; and Trager, W. 1979. The role of hemoglobins C, S, and NBALT in the inhibition of malaria parasite development in vitro. Am. J. Trop. Med. Hyg. 28: 777–780.

    PubMed  CAS  Google Scholar 

  27. Gilles, H.M.; Fletcher, K.A.; Hendrickse, R.G.; Lindner, R.; Reddy, S.; and Allan, N. 1967. Glucose-6-phosphate dehydrogenase deficiency, sickling and malaria in African children in South Western Nigeria. Lancet i: 138–140.

    Article  CAS  Google Scholar 

  28. Götz, P.; Boman, A.; and Boman, H.G. 1981. Interactions between insect immunity and an insect-pathogenic nematode with symbiotic bacteria. Proc. R. Soc. Lond. B 212: 333–350.

    Article  Google Scholar 

  29. Griffin, L., and Allonby, E.W. 1979. Trypanotolerance in breeds of sheep and goats with an experimental infection of Trypanosoma congolense. Vet. Parasitol. 5: 97–105.

    Article  Google Scholar 

  30. Grosskinsky, C.M., and Askonas, B.A. 1981. Macrophages as primary target cells and mediators of immune dysfunction in African trypanosomiasis. Infect. Immun. 33: 149–155.

    PubMed  CAS  Google Scholar 

  31. Grun, J.I., and Weidanz, W.P. 1981. Immunity to Plasmodium chabaudi adami in the B cell deficient mouse. Nature 290: 143–145.

    Article  PubMed  CAS  Google Scholar 

  32. Hitzeroth, H.W., and Bender, K. 1980. Erythrocyte G-6-PD and 6-PGD genetic polymorphism in Southern African Negroes, with a note on G-6-PD and the malaria hypothesis. Hum. Genet. 54: 233–242.

    Article  PubMed  CAS  Google Scholar 

  33. Hoeijmakers, J.H.J.; Fraseh, A.C.C.; Bernards, A.; Borst, P.; and Cross, G.A.M. 1980. Novel expression linked copies of the genes for variant surface antigens in trypanosomes. Nature 284: 78–80.

    Article  PubMed  CAS  Google Scholar 

  34. Holder, A.A., and Freeman, R.R. 1981. Immunization against blood-stage rodent malaria using purified parasite antigens. Nature 294: 361–364.

    Article  PubMed  CAS  Google Scholar 

  35. Irvin, A.D.; Cunningham, M.P.; and Young, A.S., eds. 1981. Advances in the Control of Theileriosis. The Hague: Martinus Nijhoff.

    Google Scholar 

  36. Kidson, C., and Gorman, F.J. 1962. A challenge to the concept of selection by malaria in glucose-6-phosphate dehydrogenase deficiency. Nature 196: 49–51.

    Article  PubMed  CAS  Google Scholar 

  37. Livingstone, F.B. 1971. Malaria and human polymorphisms. Ann. Rev. Genet. 5: 33–64.

    Article  Google Scholar 

  38. Luse, A., and Miller, L.H. 1971. Plasmodium falciparum malaria: ultrastructure of parasitized erythrocytes in cardiac vessels. Am. J. Trop. Med. Hyg. 20: 650–655.

    Google Scholar 

  39. Luzzatto, L. 1974. Genetic factors in malaria. Bull. WHO 50: 195–202.

    PubMed  CAS  Google Scholar 

  40. Luzzatto, L.; Nwachuku-Jarrett, E.S.; and Reddy, S. 1970. Increased sickling of parasitized erythrocytes as mechanism of resistance against malaria in the sickle-cell trait. Lancet i: 319–322.

    Article  Google Scholar 

  41. Martin, S.K.; Miller, L.H.; Alling, D.; Okoye, V.C.; Esan, G.J.F.; Osunkoya, B.O.; and Deane, M. 1979. Severe malaria and glucose-6-phosphate dehydrogenase deficiency: a reappraisal of the malaria G-6-PD hypothesis. Lancet i: 524–526.

    Article  Google Scholar 

  42. Miller, L.H.; Aikawa, M.; Johnson, J.G.; and Shiroishi, T. 1979. Interaction between cytochalasin B-treated malarial parasites and erythrocytes. Attachment and junction formation. J. Exp. Med. 149: 172–184.

    Article  PubMed  CAS  Google Scholar 

  43. Miller, L.H.; Mason, S.J.; Dvorak, J.A.; McGinnis, M.H.; and Rothman, I.K. 1975. Erythrocyte receptors for (Plasmodium knowlesi) malaria: The Duffy blood group determinants. Science 189: 561–563.

    Article  PubMed  CAS  Google Scholar 

  44. Miller, L.H.; McGinniss, M.H.; Holland, P.V.; and Sigmon, P. 1978. The Duffy blood group phenotype in American blacks infected with Plasmodium vivax in Vietnam. Am. J. Trop. Med. Hyg. 27: 1069–1072.

    PubMed  CAS  Google Scholar 

  45. Moll, G.; Lohding, A.; and Young, A.S. 1981. The epidemiology of theileriosis in the trans-Mara division, Kenya. In Advances in the Control of Theileriosis, eds. A.D. Irvin, M.P. Cunningham, and A.S. Young, pp. 56–59. The Hague: Martinus Nyhoff.

    Chapter  Google Scholar 

  46. Motulsky, A.G. 1960. Metabolic polymorphisms and the role of infectious diseases in human evolution. Hum. Biol. 32: 28–62.

    PubMed  CAS  Google Scholar 

  47. Mourant, A.E.; Kopec, A.C.; and Domaniewska-Sobczak, K. 1976. The Distribution of the Human Blood Groups and Other Polymorphisms, 2nd ed. Oxford University Press.

    Google Scholar 

  48. Murray, M.; Morrison, W.I.; Murray, P.K.; Clifford, J.D.; and Trail, J.C.M. 1979. Trypanotolerance — a review. Wld. Anim. Rev. 31: 2–12.

    Google Scholar 

  49. Nagel, R.L.; Raventos-Suarez, C.; Fabry, M.E.; Tanowitz, H.; Sicard, D.; and Labie, D. 1981. Impairment of the growth of Plasmodium falciparum in HbEE erythrocytes. J. Clin. Invest. 68: 303–305.

    Article  PubMed  Google Scholar 

  50. Pasvol, G.; Weatherall, D.J.; and Wilson, R.J.M. 1977. Effects of foetal haemoglobin on susceptibility of red cells to Plasmodium falciparum. Nature 270: 171–173.

    Article  PubMed  CAS  Google Scholar 

  51. Pasvol, G.; Weatherall, D.J.; and Wilson, R.J.M. 1978. Cellular mechanism for the protective effect of hemoglobin S against P. falciparum malaria. Nature 274: 701–703.

    Article  PubMed  CAS  Google Scholar 

  52. Pays, E.; Van Meiervenne, N.; Le Ray, D.; and Steinert, M. 1981. Gene duplication and transposition linked to antigenic variation in Trypanosoma brucei. Proc. Natl. Acad. Sci. USA 78: 2673–2677.

    Article  PubMed  CAS  Google Scholar 

  53. Potocnjak, P.; Yoshida, N.; Nussenzweig, R.S.; and Nussenzweig, V. 1980. Monovalent fragments (Fab) of monoclonal antibodies to a sporozoite surface antigen (Pb 44) protect mice against malarial infections. J. Exp. Med. 151: 1504–1513.

    Article  PubMed  CAS  Google Scholar 

  54. Quin, T.C., and Wyler, P.J. 1979. Intravascular clearance of parasitized erythrocytes in rodent malaria. J. Clin. Invest. 63: 1187–1194.

    Article  Google Scholar 

  55. Rank, R.G., and Weidanz, W.P. 1976. Nonsterilizing immunity in avian malaria: an antibody-independent phenomenon. Proc. Soc. Exp. Biol. Med. 151: 257–259.

    PubMed  CAS  Google Scholar 

  56. Roberts, D.W., and Weidanz, W.P. 1979. T-cell immunity to malaria in the B-cell deficient mouse. Am. J. Trop. Med. Hyg. 28: 1–3.

    PubMed  CAS  Google Scholar 

  57. Steinert, R.; Hultmark, D.; Engström, A.; Bennich, H.; and Boman, H. 1951. Sequence and specificity of two anti-bacterial proteins involved in insect immunity. Nature 292: 246–248.

    Article  Google Scholar 

  58. Warren, W.Mc.C., and Collins, W.E. 1981. Vector-parasite interactions and the epidemiology of malaria. Parasitological Topics, a Presentation Volume to P.C.C. Carnham, F.R.S. on the Occasion of his 80th Birthday. Society of Protozoologists, Special Publication No. 1, pp. 266–274.

    Google Scholar 

  59. Weinbaum, F.I.; Evans, C.B.; and Tigelaar, R.E. 1976. Immunity to Plasmodium berghei yoelii in mice. I. The course of infection in T-cell and B-cell deficient mice. J. Immunol. 117: 1999–2005.

    PubMed  CAS  Google Scholar 

  60. Wilson, R.J.M. 1977. Circulating antigens of parasites. In Immunity in Parasitic Diseases, vol.72, pp. 87–101. Paris: Colloque Inserm.

    Google Scholar 

  61. Young, A.S.; Brown, C.G.D.; Burridge, M.J.; Grootenhuis, J.G.; Kanhai, G.K.; Purnell, R.E.; and Stagg, D.A. 1978. The incidence of theilerial parasites in East African buffalo (Syncerus caffer). Tropenmed. Parasit. 29: 281–288.

    CAS  Google Scholar 

  62. Zinkernagel, R.M. 1979. Review: Cellular immune responses to intracellular parasites: role of the major histocompatability gene complex and thymus in determining immune responsiveness and susceptibility to disease. Parasite Immunol. I: 91–109.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Biological Sciences, Syntex Research, Palo Alto, CA, 94304, USA

    A. C. Allison

Authors
  1. A. C. Allison
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Dept. of Pure and Applied Biology, Imperial College, London University, London, SW7 2BB, England

    R. M. Anderson

  2. Biology Dept., Princeton University, Princeton, NJ, 08544, USA

    R. M. May

Rights and permissions

Reprints and permissions

Copyright information

© 1982 D. Bernhard, Dahlem Konferenzen, Berlin

About this paper

Cite this paper

Allison, A.C. (1982). Co-evolution between Hosts and Infectious Disease Agents and its Effects on Virulence. In: Anderson, R.M., May, R.M. (eds) Population Biology of Infectious Diseases. Dahlem Workshop Reports, vol 25. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-68635-1_13

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-68635-1_13

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-68637-5

  • Online ISBN: 978-3-642-68635-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation