Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-27T11:41:03.343Z Has data issue: false hasContentIssue false

Virulence determinants in a natural butterfly-parasite system

Published online by Cambridge University Press:  04 December 2006

J. C. de ROODE*
Affiliation:
Department of Environmental Studies, Emory University, Atlanta, GA 30322, USA
L. R. GOLD
Affiliation:
Department of Environmental Studies, Emory University, Atlanta, GA 30322, USA
S. ALTIZER
Affiliation:
Department of Environmental Studies, Emory University, Atlanta, GA 30322, USA
*
*Corresponding author: Tel: +1 706 542 3485. E-mail: jaapderoode@hotmail.com

Summary

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.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2006

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ackery, P. R. and Vane-Wright, R. I. (1984). Milkweed Butterflies: their Cladistics and Biology. Cornell University Press, Ithaca, NY.Google Scholar
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.CrossRefGoogle Scholar
Agresti, A. (1996). An Introduction to Categorical Data Analysis. John Wiley and Sons, New York.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. (1982). Coevolution of hosts and parasites. Parasitology 85, 411426.CrossRefGoogle ScholarPubMed
Anderson, R. M. and May, R. M. (1992). Infectious Diseases of Humans – Dynamics and Control, Oxford University Press, Oxford.Google Scholar
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.CrossRefGoogle Scholar
Bradley, C. A. and Altizer, S. (2005). Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts. Ecology Letters 8, 290300.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
Brunner, J. L., Richards, K. and Collins, J. P. (2005). Dose and host characteristics influence virulence of ranavirus infections. Oecologia 144, 399406.CrossRefGoogle ScholarPubMed
Bull, J. J., Molineux, I. J. and Rice, W. R. (1991). Selection of benevolence in a host-parasite system. Evolution 45, 875882.Google Scholar
Burnet, M. and White, D. O. (1972). The Natural History of Infectious Disease, Cambridge University Press, Cambridge.Google Scholar
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.Google Scholar
Cory, J. S. and Myers, J. H. (2004). Adaptation in an insect host-plant pathogen interaction. Ecology Letters 7, 632639.CrossRefGoogle Scholar
Crawley, M. J. (2002). Statistical Computing: An Introduction to Data Analysis using S-Plus, John Wiley and Sons, Chichester.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Dybdahl, M. F. and Storfer, A. (2003). Parasite local adaptation: Red Queen versus Suicide King. Trends in Ecology and Evolution 18, 523530.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
Ewald, P. W. (1983). Host-parasite relations, vectors, and the evolution of disease severity. Annual Review of Ecology and Systematics 14, 465485.CrossRefGoogle Scholar
Frank, S. A. (1996). Models of parasite virulence. The Quarterly Review of Biology 71, 3778.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Herre, E. A. (1993). Population structure and the evolution of virulence in nematode parasites of fig wasps. Science 259, 14421445.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Imhoof, B. and Schmid-Hempel, P. (1998). Single-clone and mixed-clone infections versus host environment in Crithidia bombi infecting bumblebees. Parasitology 117, 331336.CrossRefGoogle ScholarPubMed
Jaenike, J. (1996). Population-level consequences of parasite aggregation. Oikos 76, 155160.CrossRefGoogle Scholar
Keymer, A. E. (1982). Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84, 573587.CrossRefGoogle ScholarPubMed
Knight, A. (1998). A population study of monarch butterflies in North-Central and South Florida. Ph.D. thesis, University of Florida, Gainesville.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
Levin, B. R. (1996). The evolution and maintenance of virulence in microparasites. Emerging Infectious Diseases 2, 93102.CrossRefGoogle ScholarPubMed
Lipsitch, M., Siller, S. and Nowak, M. A. (1996). The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50, 17291741.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Mackinnon, M. J. and Read, A. F. (1999). Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53, 689703.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.Google Scholar
Oberhauser, K. S. (1997). Fecundity, lifespan and egg mass in butterflies: effects of male-derived nutrients and female size. Functional Ecology 11, 166175.CrossRefGoogle Scholar
Osnas, E. E. and Lively, C. M. (2004). Parasite dose, prevalence of infection and local adaptation in a host-parasite system. Parasitology 128, 223228.CrossRefGoogle Scholar
Poulin, R. and Combes, C. (1999). The concept of virulence: interpretations and implications. Parasitology Today 15, 474475.CrossRefGoogle ScholarPubMed
Poulin, R. and Morand, S. (2000). The diversity of parasites. The Quarterly Review of Biology 75, 277293.CrossRefGoogle ScholarPubMed
Read, A. F. (1994). The evolution of virulence. Trends in Microbiology 2, 7376.CrossRefGoogle ScholarPubMed
Stearns, S. C. and Ebert, D. (2001). Evolution in health and disease: work in progress. Quarterly Review of Biology 76, 417432.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
Tanada, Y. and Kaya, H. K. (1993). Insect Pathology. Academic Press, San Diego.Google Scholar
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.CrossRefGoogle ScholarPubMed
Turner, C. M., Aslam, N. and Dye, C. (1995). Replication, differentiation, growth and the virulence of Trypanosoma brucei infections. Parasitology 111, 289300.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
Zimmer, C. (2001). Parasite Rex: Inside the Bizarre World of Nature's Most Dangerous Creatures, Simon and Schuster, New York.Google Scholar