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Virulence determinants in a natural butterfly-parasite system

  • J. C. de ROODE (a1), L. R. GOLD (a1) and S. ALTIZER (a1)


Much evolutionary theory assumes that parasite virulence (i.e. parasite-induced host mortality) is determined by within-host parasite reproduction and by the specific parasite genotypes causing infection. However, many other factors could influence the level of virulence experienced by hosts. We studied the protozoan parasite Ophryocystis elektroscirrha in its host, the monarch butterfly, Danaus plexippus. We exposed monarch larvae to wild-isolated parasites and assessed the effects of within-host replication and parasite genotype on host fitness measures, including pre-adult development time and adult weight and longevity. Per capita replication rates of parasites were high, and infection resulted in high parasite loads. Of all host fitness traits, adult longevity showed the clearest relationship with infection status, and decreased continuously with increasing parasite loads. Parasite genotypes differed in their virulence, and these differences were maintained across ecologically relevant variables, including inoculation dose, host sex and host age at infection. Thus, virulence appears to be a robust genetic parasite trait in this system. Although parasite loads and genotypes had strong effects on virulence, inoculation dose, host sex and age at infection were also important. These results have implications for virulence evolution and emphasize the need for a detailed understanding of specific host-parasite systems for addressing theory.


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Ackery, P. R. and Vane-Wright, R. I. (1984). Milkweed Butterflies: their Cladistics and Biology. Cornell University Press, Ithaca, NY.
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.
Agresti, A. (1996). An Introduction to Categorical Data Analysis. John Wiley and Sons, New York.
Altizer, S. M. and Oberhauser, K. S. (1999). Effects of the protozoan parasite Ophryocystis elektroscirrha on the fitness of monarch butterflies (Danaus plexippus). Journal of Invertebrate Pathology 74, 7688.
Altizer, S. M., Oberhauser, K. S. and Brower, L. P. (2000). Associations between host migration and the prevalence of a protozoan parasite in natural populations of adult monarch butterflies. Ecological Entomology 25, 125139.
Altizer, S. M., Oberhauser, K. S. and Geurts, K. A. (2004). Transmission of the protozoan parasite, Ophryocystis elektroscirrha, in monarch butterfly populations: implications for prevalence and population-level impacts. In The Monarch Butterfly: Biology and Conservation (ed.Oberhauser, K. S. and Solensky, M.), pp. 203218. Cornell University Press, Ithaca, NY.
Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite population interactions. 1. Regulatory processes. Journal of Animal Ecology 47, 219247.
Anderson, R. M. and May, R. M. (1982). Coevolution of hosts and parasites. Parasitology 85, 411426.
Anderson, R. M. and May, R. M. (1992). Infectious Diseases of Humans – Dynamics and Control, Oxford University Press, Oxford.
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.
Bradley, C. A. and Altizer, S. (2005). Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts. Ecology Letters 8, 290300.
Brower, L. P. (1995). Understanding and misunderstanding the migration of the monarch butterfly (Nymphalidae) in North America: 1857–1995. Journal of the Lepidopterists' Society 49, 304385.
Brower, L. P., Fink, L. S., Brower, A. V., Leong, K., Oberhauser, K., Altizer, S., Taylor, O., Vickerman, D., Calvert, W. H., Van Hook, T., Alonsomejia, A., Malcolm, S. B., Owen, D. F. and Zalucki, M. P. (1995). On the dangers of interpopulational transfers of monarch butterflies. Bioscience 45, 540544.
Brunner, J. L., Richards, K. and Collins, J. P. (2005). Dose and host characteristics influence virulence of ranavirus infections. Oecologia 144, 399406.
Bull, J. J., Molineux, I. J. and Rice, W. R. (1991). Selection of benevolence in a host-parasite system. Evolution 45, 875882.
Burnet, M. and White, D. O. (1972). The Natural History of Infectious Disease, Cambridge University Press, Cambridge.
Carius, H. J., Little, T. J. and Ebert, D. (2001). Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 55, 11361145.
Cory, J. S. and Myers, J. H. (2004). Adaptation in an insect host-plant pathogen interaction. Ecology Letters 7, 632639.
Crawley, M. J. (2002). Statistical Computing: An Introduction to Data Analysis using S-Plus, John Wiley and Sons, Chichester.
Davis, A. K., Farrey, B. D. and Altizer, S. (2005). Variation in thermally induced melanism in monarch butterflies (Lepidoptera: Nymphalidae) from three American populations. Journal of Thermal Biology 30, 410421.
Day, T. (2002). On the evolution of virulence and the relationship between various measures of mortality. Proceedings of the Royal Society of London, B 269, 13171323.
Dezfuli, B. S., Volponi, S., Beltrami, I. and Poulin, R. (2002). Intra- and interspecific density-dependent effects on growth in helminth parasites of the cormorant, Phalacrocorax carbo sinensis. Parasitology 124, 537544.
Diffley, P., Scott, J. O., Mama, K. and Tsen, T. N. (1987). The rate of proliferation among African trypanosomes is a stable trait that is directly related to virulence. American Journal of Tropical Medicine and Hygiene 36, 533540.
Dybdahl, M. F. and Storfer, A. (2003). Parasite local adaptation: Red Queen versus Suicide King. Trends in Ecology and Evolution 18, 523530.
Ebert, D. (1999). The evolution and expression of parasite virulence. In Evolution in Health and Disease (ed.Stearns, S. C.), pp. 161172. Oxford University Press, Oxford.
Ebert, D., Zschokke-Rohringer, C. D. and Carius, H. J. (2000). Dose effects and density-dependent regulation of two microparasites of Daphnia magna. Oecologia 122, 200209.
Ewald, P. W. (1983). Host-parasite relations, vectors, and the evolution of disease severity. Annual Review of Ecology and Systematics 14, 465485.
Frank, S. A. (1996). Models of parasite virulence. The Quarterly Review of Biology 71, 3778.
Grech, K., Watt, K. and Read, A. F. (2006). Host-by-parasite interactions for virulence and resistance in a malaria model system. Journal of Evolutionary Biology 19, 16201630.
Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S. and Samuel, M. D. (2002). Climate warming and disease risks for terrestrial and marine biota. Science 296, 21582162.
Herre, E. A. (1993). Population structure and the evolution of virulence in nematode parasites of fig wasps. Science 259, 14421445.
Hodgson, D. J., Hitchman, R. B., Vanbergen, A. J., Hails, R. S., Possee, R. D. and Cory, J. S. (2004). Host ecology determines the relative fitness of virus genotypes in mixed-genotype nucleopolyhedrovirus infections. Journal of Evolutionary Biology 17, 10181025.
Hughes, W. O. H., Petersen, K. S., Ugelvig, L. V., Pedersen, D., Thomsen, L., Poulsen, M. and Boomsma, J. J. (2004). Density-dependence and within-host competition in a semelparous parasite of leaf-cutting ants. BMC Evolutionary Biology 4, 45.
Imhoof, B. and Schmid-Hempel, P. (1998). Single-clone and mixed-clone infections versus host environment in Crithidia bombi infecting bumblebees. Parasitology 117, 331336.
Jaenike, J. (1996). Population-level consequences of parasite aggregation. Oikos 76, 155160.
Keymer, A. E. (1982). Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84, 573587.
Knight, A. (1998). A population study of monarch butterflies in North-Central and South Florida. Ph.D. thesis, University of Florida, Gainesville.
Krist, A. C., Jokela, J., Wiehn, J. and Lively, C. M. (2004). Effects of host condition on susceptibility to infection, parasite developmental rate, and parasite transmission in a snail-trematode interaction. Journal of Evolutionary Biology 17, 3340.
Leong, K. L., Yoshimura, M. A., Kaya, H. K. and Williams, H. (1997 a). Instar susceptibility of the monarch butterfly (Danaus plexippus) to the neogregarine parasite, Ophryocystis elektroscirrha. Journal of Invertebrate Pathology 69, 7983.
Leong, K. L. H., Yoshimura, M. A. and Kaya, H. K. (1997 b). Occurrence of a neogregarine protozoan, Ophryocystis elektroscirrha McLaughlin and Myers, in populations of monarch and queen butterflies. Pan-Pacific Entomologist 73, 4951.
Levin, B. R. (1996). The evolution and maintenance of virulence in microparasites. Emerging Infectious Diseases 2, 93102.
Lipsitch, M., Siller, S. and Nowak, M. A. (1996). The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50, 17291741.
Mackinnon, M. J., Gaffney, D. J. and Read, A. F. (2002). Virulence of malaria parasites: host genotype by parasite genotype interactions. Infection, Genetics and Evolution 1, 287296.
Mackinnon, M. J. and Read, A. F. (1999). Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53, 689703.
McLaughlin, R. E. and Myers, J. (1970). Ophryocystis elektroscirrha sp. n., a neogregarine pathogen of monarch butterfly Danaus plexippus (L.) and the Florida queen butterfly D. gilippus berenice Cramer. Journal of Protozoology 17, 300305.
Nagano, C. D., Sakai, W. H., Malcolm, S. B., Cockrell, B. J., Donahue, J. P. and Brower, L. P. (1993). Spring migration of monarch butterflies in California. In Biology and Conservation of the Monarch Butterfly (ed.Zalucki, M. P.), pp. 217232. Natural History Museum of Los Angeles County, Los Angeles CA.
Oberhauser, K. S. (1997). Fecundity, lifespan and egg mass in butterflies: effects of male-derived nutrients and female size. Functional Ecology 11, 166175.
Osnas, E. E. and Lively, C. M. (2004). Parasite dose, prevalence of infection and local adaptation in a host-parasite system. Parasitology 128, 223228.
Poulin, R. and Combes, C. (1999). The concept of virulence: interpretations and implications. Parasitology Today 15, 474475.
Poulin, R. and Morand, S. (2000). The diversity of parasites. The Quarterly Review of Biology 75, 277293.
Read, A. F. (1994). The evolution of virulence. Trends in Microbiology 2, 7376.
Stearns, S. C. and Ebert, D. (2001). Evolution in health and disease: work in progress. Quarterly Review of Biology 76, 417432.
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.
Tanada, Y. and Kaya, H. K. (1993). Insect Pathology. Academic Press, San Diego.
Timms, R., Colegrave, N., Chan, B. H. K. and Read, A. F. (2001). The effect of parasite dose on disease severity in the rodent malaria Plasmodium chabaudi. Parasitology 123, 111.
Turner, C. M., Aslam, N. and Dye, C. (1995). Replication, differentiation, growth and the virulence of Trypanosoma brucei infections. Parasitology 111, 289300.
Van Beek, N. A. M., Wood, H. A. and Hughes, P. R. (1988). Quantitative aspects of nuclear polyhedrosis virus infections in Lepidopterous larvae: the dose-survival time relationship. Journal of Invertebrate Pathology 51, 5863.
Vickerman, D., Michels, A. and Burrowes, P. A. (1999). Levels of infection of migrating monarch monarch butterflies, Danaus plexippus (Lepidoptera: Nymphalidae) by the parasite Ophryocystis elektroscirrha (Neogregarinidae: Ophryocystidae), and evidence of a new mode of spore transmission between adults. Journal of the Kansas Entomological Society 72, 124128.
Wiklund, C. and Kaitala, A. (1995). Sexual selection for large male size in a polyandrous butterfly – the effect of body size on male versus female reproductive success in Pieris napi. Behavioral Ecology 6, 613.
Zimmer, C. (2001). Parasite Rex: Inside the Bizarre World of Nature's Most Dangerous Creatures, Simon and Schuster, New York.


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Virulence determinants in a natural butterfly-parasite system

  • J. C. de ROODE (a1), L. R. GOLD (a1) and S. ALTIZER (a1)


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