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Factors affecting the evolution of virulence: nematode parasites of fig wasps as a case study

Published online by Cambridge University Press:  06 April 2009

E. A. Herre
E. A. Herre
Affiliation:
Smithsonian Tropical Research Institute, unit 0948, APO AA 34002-0948, U.S.A. or Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Republic of Panama
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Summary

The natural history of fig-pollinating wasps and their associated species-specific nematodes allows the measurement of many parameters which are relevant to testing hypotheses concerning host-parasite ecology and evolution. Within fig wasps species, it is possible to estimate lifetime reproductive success of foundress wasps as a function of presence or absence of nematode parasitism (virulence). Across species, there is a wide range of host population structures which, in turn, results in a range of opportunities for either horizontal or vertical nematode transmission. Therefore, estimates of virulence can be related to opportunities for transmission across a group of closely related hosts and their parasites. Further, the dynamics of the nematode infections over ecological and short-term evolutionary timescales can be monitored, giving added insight into the interpretation of the virulence estimates. Moreover, several scales of longer term evolutionary relationships are either known directly from fossil evidence or can be inferred from molecular data, providing deeper temporal context for the observed patterns. This combination of attributes permits detailed testing of hypotheses concerning the factors that potentially influence the evolution of virulence in host-parasite systems, and further, population and simulation models of the system that incorporate the parameter estimates can clarify the interpretation of how those factors act. There is little evidence suggesting that intermediate and long-term evolutionary relationships explain current levels of virulence. That is, it appears that virulence can change rapidly relative to speciation events, and that the nematodes do not tend to become ‘benign over time’. Instead, it appears that host population structure can influence the evolution of parasite virulence by affecting the relative opportunities for horizontal to vertical transmission, which, in turn, influences the relative costs and benefits of virulence to the nematodes. At one level, increased opportunities for horizontal transmission decouple the reproductive interests of the individual nematodes from those of the individual hosts that they are directly parasitizing, thereby reducing the cost of virulence to individual nematodes. At another level, increased opportunities of horizontal transmission also increases the relative frequency of hosts infected by multiple strains of nematodes. This promotes the evolution of more virulent forms by increasing the relative importance of within-host competition among nematode strains, thereby favouring strains that ‘eat more host sooner’. An interesting property of the fig-nematode systems is that the proportion of infected hosts does not change dramatically through time. This finding implies that there can be considerable negative effects on survival of infected hosts in addition to the previously documented reductions in fecundity of infected foundresses, because the latter are insufficient to account for the observed stability of wasp infection rates.

Keywords

parasitismvirulencefig waspsnematodespopulation structurephylogeny
Type
Research Article
Information
Parasitology , Volume 111 , Supplement S1: Ecology of wildlife host-parasite interactions , January 1995 , pp. S179 - S191
Copyright
Copyright © Cambridge University Press 1995

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References

REFERENCES

Allison, A. C. (1982). Coevolution between hosts and infectious disease agents and its effect on virulence. In Dahlem Workshop Reports, Life Sciences Research Report 25, Population Biology of Infectious Diseases. pp. 245. (eds Anderson, R. M. and May, R. M.) Berlin: Springer Verlag.Google Scholar
Anderson, R. M. & May, R. M. (1991). Infectious Diseases of Humans. Oxford: Oxford University Press.Google Scholar
Axelrod, R. & Hamilton, W. D. (1981). The evolution of cooperation. Science 211, 1390–6.CrossRefGoogle ScholarPubMed
Berg, C. C. (1989). Classification and distribution of Ficus. Experientia 45, 605–11.CrossRefGoogle Scholar
Berg, C. C. & Wiebes, J. T. (1992). African Fig Trees and Fig Wasps. Amsterdam, North-Holland.Google Scholar
Bremmermann, H. J. (1980). Sex and polymorphism as strategies in host-pathogen interactions. Journal of Theoretical Biology 87, 671–702.CrossRefGoogle Scholar
Bremmermann, H. J. & Pickering, J. (1983). A game theoretical model of parasite virulence. Journal of Theoretical Biology 100, 411–26.CrossRefGoogle Scholar
Bull, J. J. (1994). The evolution of virulence. Evolution 48, 1423–37.Google Scholar
Bull, J. J., Molineux, I. J. & Rice, W. H. (1991). Selection of benevolence in a host-parasite system. Evolution 45, 875–82.Google Scholar
Clayton, D. H. & Tompkins, D. M. (1994). Ectoparasite virulence is linked to mode of transmission. Proceedings of the Royal Society Series B 256, 211–17.Google ScholarPubMed
Compton, S. G. (1993). One way to be a fig. African Entomologist 1, 151–8.Google Scholar
Collinson, M. E. (1989). The fossil history of the Moraceae. In Evolution, Systematics, and Fossil History of the Hamanielidae. (ed. Crane, P. R. & Blackmore, S.) Oxford: Clarendon Press.Google Scholar
Corner, E. J. H. (1940). Wayside Trees of Malaya. Singapore Government Printing Office.Google Scholar
Corner, E. J. H. (1985). Ficus (Moraceae) and Hymenoptera (Chalcidoidea): Figs and their pollinators. Biological Journal of the Linnaean Society 25, 187–95.CrossRefGoogle Scholar
Ebert, D. (1994). Virulence and local adaptation of a horizontally transmitted parasite. Science 265, 1084–6.CrossRefGoogle ScholarPubMed
Ebert, D. & Herre, E. A. (1995). The evolution of virulence and disease symptoms. Parasitology Today. (in press).Google Scholar
Ewald, P. W. (1987). Transmission modes and the evolution of the parasitism-mutualism continuum. Annals of the New York Academy of Sciences 503, 295–306.CrossRefGoogle ScholarPubMed
Fine, P. E. M. (1975). Vectors and vertical transmission: an epidemiological perspective. Annals of the New York Academy of Sciences 266, 173–94.CrossRefGoogle Scholar
Frank, S. A. (1985). Hierarchical selection theory and sex ratios. II. On applying the theory, and testing with fig wasps. Evolution 39, 949–64.CrossRefGoogle ScholarPubMed
Frank, S. A. (1992). A kin selection model for the evolution of virulence. Proceedings of the Royal Society B 250, 195–7.Google ScholarPubMed
Galil, J. & Eisikowitch, D. (1968). Flowering cycles and fruit types of Ficus sycomorus in Israel. New Phytologist 67, 745–58.CrossRefGoogle Scholar
Giblin-Davis, R. M., Center, B. J., Nadel, H., Frank, H. & Ramirez, W. (1995). Nematodes associated with fig wasps, Pegoscapus spp. (Agaonidae), and syconia of Native Florida Figs (Ficus spp.) Journal of Nematology. 27, 1–14.Google Scholar
Haldane, J. B. S. (1949). Disease and Evolution. La Ricerca Scientifica supplimental 19, 68–76.Google Scholar
Hamilton, W. D. (1980). Sex versus non-sex versus parasite. Oikos 35, 282–90.CrossRefGoogle Scholar
Hamilton, W. D. (1982). Pathogens as causes of genetic diversity in their host populations. In Dahlem Workshop Reports, Life Sciences Research Report 25, Population Biology of Infectious Diseases. (ed. Anderson, R. M. & May, R. M.) pp. 269–297. Berlin: Springer Verlag.Google Scholar
Hamilton, W. D. & Zuk, M. (1982). Heritable true fitness and bright birds: A role for parasites? Science 218, 384–7.Google Scholar
Herre, E. A. (1985). Sex ratio adjustment in fig wasps. Science 228, 896–8.CrossRefGoogle ScholarPubMed
Herre, E. A. (1987). Optimality, plasticity, and selective regime in fig wasp sex ratios. Nature 329, 627–9.CrossRefGoogle Scholar
Herre, E. A. (1988). Sex ratio adjustment in thirteen species of Panamanian fig wasps. Ph.D. thesis, University of lowa.Google Scholar
Herre, E. A. (1989). Coevolution of reproductive characteristics in twelve species of new world figs and their pollinator wasps. Experientia 45, 637–47.CrossRefGoogle Scholar
Herre, E. A. (1993). Population structure and the evolution of virulence in nematode parasites of fig wasps. Science 259, 1442–5.Google ScholarPubMed
Herre, E. A. (1996). An overview of studies on a community of Panamanian figs. Journal of Biogeography. (in press).CrossRefGoogle Scholar
Herre, E. A., Machado, C. A., Bermingham, E., Nason, J. D., Windsor, D. M., Mccafferty, S. S., Van Houten, W. & Bachmann, K. (1996 a). Molecular phylogenies of figs and their pollinating wasps. Journal of Biogeography. (in press).CrossRefGoogle Scholar
Herre, E. A., West, S. A., Cook, J. M., Compton, S. G. & Kjellberg, F. (1996 b). Fig Wasp Mating Systems: Pollinators and Parasites, Sex Ratio Adjustment and Male Polymorphism, Population Structure and its Consequences. In Social Competition and Cooperation in Insects and Arachnids I. Evolution of Mating Systems. (ed. Choe, J. C., Crespi, B.) Chicago: University of Chicago Press.Google Scholar
Holmes, J. C. (1982). Impact of infectious diseases on the population growth and geographical distributions of animals. In Dahlem Workshop Reports, Life Sciences Workshop Report 25, Population Biology of Infectious Diseases. (ed. Anderson, R. M., & May, R. M.) pp. 37–53. Berlin: Springer Verlag.Google Scholar
Hossaert-Mckey, M., Gibernau, M. & Frey, J. E. (1994). Chemosensory attraction of fig wasps to substances produced by receptive figs. Entomologia Experimentalis et Applicata 70, 185–91.CrossRefGoogle Scholar
Jaenike, J. (1978). An hypothesis to account for the maintenance of sex within populations. Evolutionary Theory 3, 191–4.Google Scholar
Janzen, D. H. (1979). How to be a fig. Annual Review of Ecology and Systematics 10, 13–51.CrossRefGoogle Scholar
Levin, S. A. & Pimentel, D. (1981). Selection of intermediate rates of increase in parasite-host systems. American Naturalist 117, 308–15.CrossRefGoogle Scholar
Lipsitch, M., Nowak, M. A., Ebert, D. & May, R. M. (1995). The population dynamics of vertically and horizontally transmitted parasites. Proceedings of the Royal Society B 260, 321–7.Google ScholarPubMed
Machado, C. A., Herre, E. A., Mccafferty, S. S. & Bermingham, E. (1996). Molecular phylogenies of fig pollinating and non-pollinating wasps and the implications for the origin and the evolution of the fig-fig wasp mutualism. Journal of Biogeography (in press).CrossRefGoogle Scholar
Mangin, K. L., Lipsitch, M. & Ebert, D. (1995). Virulence and transmission mode of two microsporidia in Daphnia magna. Parasitology 111, 133–42.CrossRefGoogle Scholar
May, R. M. & Anderson, R. M. (1983). Epidemiology and genetics in the coevolution of parasites and hosts. Proceedings of the Royal Society B 219, 281–313.Google ScholarPubMed
May, R. M. & Nowak, M. A. (1994). Superinfection, metapopulation dynamics, and the evolution of diversity. Journal of Theoretical Biology B 170, 95–114.CrossRefGoogle ScholarPubMed
Maynard, J. Smith & Szathmary, E. (1995). The Major Transitions of Evolution. Oxford: Freeman/Spectrum.Google Scholar
Nason, J. D., Herre, E. A., & Hamrick, J. L. (1996). Long distance dispersal of pollen by fig wasps. Journal of Biogeography. (in press).Google Scholar
Nowak, M. A. & May, R. M. (1994). Superinfection and the evolution of virulence. Proceedings of the Royal Society B 255, 81–9.Google Scholar
Parker. (1985). Local population differentiation for compatibility in an annual legume and its host-specific fungal pathogen. Evolution 39, 713–23.CrossRefGoogle Scholar
Patel, A., Hossaert-Mckey, M. & Mckey, D. (1993). Ficus-pollinator research in India: Past, present, and future. Current Science 65, 243–53.Google Scholar
Poinar, G. O. Jr (1979). Parasitodiplogaster sycophilon gen. n., sp. n. Diplogasteridae: Nematoda), a parasite of Elizabethiella stuckenbergi Grandi (Agaonidae: Hymenoptera) in Rhodesia. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen 82, 375–81.Google Scholar
Poinar, G. O. Jr, & Herre, E. A. (1991). Speciation and adaptive radiation in the fig wasp nematode, Parasitodiplogaster (Diplogasteridae: Rhabditida), in Panama. Revue de Nematologie 14, 361–74.Google Scholar
Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton: Princeton University Press.Google ScholarPubMed
Price, P. W., Westoby, M., Rice, B., Atsatt, P. R., Fritz, R. S., Thompson, J. N. & Mobley, K. (1986). Parasite mediation in ecological interactions. Annual Review of Ecology and Systematics 17, 487–505.Google Scholar
Ramirez, B. W. (1969). Fig wasps: mechanism of pollen transfer. Science 163, 580–81.CrossRefGoogle Scholar
Ramirez, B. W. (1974). Coevolution of Ficus and Agaonidae. Annals of the Missouri Botanical Garden 61, 770–80.Google Scholar
Read, A. F. (1994). The evolution of virulence. Trends in Microbiology 2, 73–6.CrossRefGoogle ScholarPubMed
Toft, C. A. & Aeschlimann, A. (1991). Introduction: Coexistence or Conflict? In Parasite Host Associations: Coexistence or Conflict. (ed. Toft, C. A., Aeschlimann, A. & Bolis, L.) Oxford: Oxford Science Publications, pp. 1–12.CrossRefGoogle Scholar
Van Noort, S., Ware, A. B. & Compton, S. G. (1989). Pollinator-specific volatile attractants released from the figs of Ficus burtt-davyi. South African Journal of Science 85, 323–4.Google Scholar
Wade, M. J. (1985). Soft selection, hard selection, kin selection, and group selection. American Naturalist 125, 61–73.CrossRefGoogle Scholar
Ware, A. B., Perry, T. K., Compton, S. G. & Van Noort, S. (1993). Fig volatiles: their role in attracting pollinators and maintaining pollinator specificity. Plant Systematics and Evolution 186, 147–56.CrossRefGoogle Scholar
West, S. & Herre, E. A. (1994). The ecology of the New World fig parasitizing wasps Idarnes and implications for the evolution of the Fig-pollinator mutualism. Proceedings of the Royal Society London B 258, 67–72.Google Scholar
Wiebes, J. T. (1979). Co-evolution of figs and their insect pollinators. Annual Review of Ecology and Systematics 10, 1–12.CrossRefGoogle Scholar
Wiebes, J. T. (1982). The phylogeny of the agaonidae (Hymenoptera, Chalcidoidea). Netherlands Journal of Zoology 32, 395–411.Google Scholar
Wiebes, J. T. (1995). Agaonidae (Hymenoptera Chalcidoidea) and Ficus (Moraceae): fig wasps and their figs, xv (Meso-American Pegoscapus). Proceedings of the Koninklijke Nederlandes Akademie van Wetenschappen 98, 167–83.Google Scholar
Yamamura, N. (1993). Vertical transmission and evolution of mutualism from parasitism. Theor. Pop. Biol. 44, 95–109.Google Scholar