A Model for the Coevolution of Immunity and Immune Evasion in Vector‐Borne Diseases with Implications for the Epidemiology of Malaria

We describe a model of host‐parasite coevolution, where the interaction depends on the investments by the host in its immune response and by the parasite in its ability to suppress (or evade) its host’s immune response. We base our model on the interaction between malaria parasites and their mosquito hosts and thus describe the epidemiological dynamics with the Macdonald‐Ross equation of malaria epidemiology. The qualitative predictions of the model are most sensitive to the cost of the immune response and to the intensity of transmission. If transmission is weak or the cost of immunity is low, the system evolves to a coevolutionarily stable equilibrium at intermediate levels of investment (and, generally, at a low frequency of resistance). At a higher cost of immunity and as transmission intensifies, the system is not evolutionarily stable but rather cycles around intermediate levels of investment. At more intense transmission, neither host nor parasite invests any resources in dominating its partner so that no resistance is observed in the population. These results may help to explain the lack of encapsulated malaria parasites generally observed in natural populations of mosquito vectors, despite strong selection pressure for resistance in areas of very intense transmission.

[1]  H J Bremermann,et al.  A competitive exclusion principle for pathogen virulence , 1989, Journal of mathematical biology.

[2]  Community dynamics, trade-offs, invasion criteria and the evolution of host resistance to microparasites. , 2001, Journal of theoretical biology.

[3]  J. Koella,et al.  On the use of mathematical models of malaria transmission. , 1991, Acta tropica.

[4]  H. Hurd,et al.  Plasmodium yoelii nigeriensis: the effect of high and low intensity of infection upon the egg production and bloodmeal size of Anopheles stephensi during three gonotrophic cycles , 1995, Parasitology.

[5]  L. Molineaux,et al.  The Garki project: Research on the epidemiology and control of malaria in the Sudan savanna of West Africa , 1980 .

[6]  F. Kafatos,et al.  Immunity to eukaryotic parasites in vector insects. , 1996, Current opinion in immunology.

[7]  H. Godfray,et al.  Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster , 1997, Nature.

[8]  M. Hochberg,et al.  Virulence and age at reproduction: new insights into host–parasite coevolution , 2001 .

[9]  Sylvain Gandon,et al.  Imperfect vaccines and the evolution of pathogen virulence , 2001, Nature.

[10]  P. Thrall,et al.  The cost of resistance and the maintenance of genetic polymorphism in host—pathogen systems , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[11]  R. Bowers The basic depression ratio of the host: the evolution of host resistance to microparasites , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[12]  J. Koella,et al.  Melanization of Plasmodium falciparum and C-25 Sephadex Beads by Field-Caught Anopheles gambiae (Diptera: Culicidae) from Southern Tanzania , 2002, Journal of medical entomology.

[13]  H. Ferguson,et al.  Why is the effect of malaria parasites on mosquito survival still unresolved? , 2002, Trends in parasitology.

[14]  S. Frank Statistical properties of polymorphism in host—parasite genetics , 1996, Evolutionary Ecology.

[15]  A. M. Ahmed,et al.  The costs of mounting an immune response are reflected in the reproductive fitness of the mosquito Anopheles gambiae , 2002 .

[16]  A. Sasaki,et al.  A model for the coevolution of resistance and virulence in coupled host–parasitoid interactions , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[17]  Odo Diekmann,et al.  On evolutionarily stable life histories, optimization and the need to be specific about density dependence , 1995 .

[18]  H. Godfray,et al.  COSTS OF COUNTERDEFENSES TO HOST RESISTANCE IN A PARASITOID OF DROSOPHILA , 2001, Evolution; international journal of organic evolution.

[19]  J. Kirchner,et al.  EVOLUTIONARY DYNAMICS OF PATHOGEN RESISTANCE AND TOLERANCE , 2000, Evolution; international journal of organic evolution.

[20]  E. Walker,et al.  Genetically manipulated vectors of human disease: a practical overview. , 2001, Trends in parasitology.

[21]  M. Boots,et al.  The Evolution of Costly Resistance in Host‐Parasite Systems , 1999, The American Naturalist.

[22]  B. Diamond,et al.  Revisiting and revising suppressor T cells. , 1992, Immunology today.

[23]  H J Bremermann,et al.  A game-theoretical model of parasite virulence. , 1983, Journal of theoretical biology.

[24]  P. Kaye Infectious diseases of humans: Dynamics and control , 1993 .

[25]  P. Schmid-Hempel,et al.  Survival for immunity: the price of immune system activation for bumblebee workers. , 2000, Science.

[26]  M. Parker Pathogens and sex in plants , 1994, Evolutionary Ecology.

[27]  J. Koella,et al.  Reduced efficacy of the immune melanization response in mosquitoes infected by malaria parasites , 2002, Parasitology.

[28]  A. Pain,et al.  Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells , 1999, Nature.

[29]  R. Sakai,et al.  Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. , 1986, Science.

[30]  M. van Baalen Coevolution of recovery ability and virulence. , 1998, Proceedings. Biological sciences.

[31]  S. Lal,et al.  Epidemiology and control of malaria , 1999, Indian journal of pediatrics.

[32]  Thompson,et al.  Weak sinks could cradle mutualistic symbioses – strong sources should harbour parasitic symbioses , 2000 .

[33]  K. McKean,et al.  Increased sexual activity reduces male immune function in Drosophila melanogaster , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[34]  B. Bloom,et al.  Suppressor T lymphocytes from lepromatous leprosy skin lesions. , 1986, Journal of immunology.

[35]  M. Siva-jothy,et al.  Decreased immune response as a proximate cost of copulation and oviposition in a damselfly , 1998 .

[36]  H. Hurd,et al.  Malaria‐induced reduction of fecundity during the first gonotrophic cycle of Anopheles Stephensi mosquitoes , 1995, Medical and veterinary entomology.

[37]  A GENETIC CORRELATION BETWEEN AGE AT PUPATION AND MELANIZATION IMMUNE RESPONSE OF THE YELLOW FEVER MOSQUITO AEDES AEGYPTI , 2002, Evolution; international journal of organic evolution.

[38]  B. Knols,et al.  Plasmodium falciparum sporozoites increase feeding-associated mortality of their mosquito hosts Anopheles gambiae s.l. , 2000, Parasitology.

[39]  Christophe Boëte,et al.  A theoretical approach to predicting the success of genetic manipulation of malaria mosquitoes in malaria control , 2002, Malaria Journal.

[40]  H. Hurd,et al.  The effects of natural Plasmodium falciparum infection on the fecundity and mortality of Anopheles gambiae s. l. in north east Tanzania , 1997, Parasitology.

[41]  S. Frank Coevolutionary genetics of hosts and parasites with quantitative inheritance , 2005, Evolutionary Ecology.