Host-parasite genetic interactions and virulence-transmission relationships in natural populations of monarch butterflies

Evolution

Volumn 64, Issue 2, 2010, Pages 502-514

  De Roode, Jacobus C ^a   Altizer, Sonia ^b  

^a EMORY UNIVERSITY   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

Coevolution; G G interaction; Local adaptation; Ophryocystis elektroscirrha; Tolerance

Indexed keywords

BUTTERFLY; GENOTYPE; HOST-PARASITE INTERACTION; LOCAL ADAPTATION; MORTALITY; NATURAL SELECTION; PROTOZOAN; SYMPATRY; TOLERANCE; VIRULENCE;

ANIMAL; ARTICLE; BUTTERFLY; EVOLUTION; GENETICS; HOST PARASITE INTERACTION; PARASITOLOGY; VIRULENCE;

ANIMALS; BUTTERFLIES; EVOLUTION; HOST-PARASITE INTERACTIONS; VIRULENCE;

BACTERIA (MICROORGANISMS); DANAUS PLEXIPPUS; OPHRIOCYSTIS ELEKTROSCIRRHA; PROTOZOA;

EID: 75149120749     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2009.00845.x     Document Type: Article

References (88)

1. Alizon, S., A. Hurford, N. Mideo, and M. Van Baalen. 2009. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J. Evol. Biol. 22 : 245 259.
2. Alonso-Mejia, A., E. Rendon-Salinas, E. Montesinos-Patino, and L. P. Brower. 1997. Use of lipid reserves by monarch butterflies overwintering in Mexico: implications for conservation. Ecol. Appl. 7 : 934 947.
3. Altizer, S. M., and K. S. Oberhauser. 1999. Effects of the protozoan parasite Ophryocystis elektroscirrha on the fitness of monarch butterflies (Danaus plexippus). J. Invertebr. Pathol. 74 : 76 88.
4. Altizer, S., D. Harvell, and E. Friedle. 2003. Rapid evolutionary dynamics and disease threats to biodiversity. Trends Ecol. Evol. 18 : 589 596.
5. Anderson, R. M., and R. M. May. 1982. Coevolution of hosts and parasites. Parasitology 85 : 411 426.
6. Antia, R., B. R. Levin, and R. M. May. 1994. Within-host population dynamics and the evolution and maintenance of microparasite virulence. Am. Nat. 144 : 457 472.
7. Barrett, R. D. H., R. C. MacLean, and G. Bell. 2005. Experimental evolution of Pseudomonas fluorescens in simple and complex environments. Am. Nat. 166 : 470 480.
8. Bell, G., and J. Maynard Smith. 1987. Short-term selection for recombination among mutually antagonistic species. Nature 328 : 66 68.
9. Bremermann, H. J., and J. Pickering. 1983. A game-theoretical model of parasite virulence. J. Theor. Biol. 100 : 411 426.
10. Brower, L. P. 1995. Understanding and misunderstanding the migration of the monarch butterfly (Nymphalidae) in North America: 1857-1995. J. Lepidopt. Soc. 49 : 304 385.
11. Brower, L. P. 1999. Biological necessities for monarch butterfly overwintering in relation to the oyamel forest ecosystem in Mexico. Pp. 11 28 in J. Hoth, L. Merino, K. Oberhauser, I. Pisanty, S. Price, and T. Wilkinson, eds. The 1997 North American Conference on the Monarch Butterfly. Commission for Environmental Cooperation, Montreal.
12. Bull, J. J. 1994. Virulence. Evolution 48 : 1423 1437.
13. Burdon, J. J., and P. H. Thrall. 1999. Spatial and temporal patterns in coevolving plant and pathogen associations. Am. Nat. 153 : S15 S33.
14. Carius, H. J., T. J. Little, and D. Ebert. 2001. Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 55 : 1136 1145.
15. Cleaveland, S., G. R. Hess, A. P. Dobson, M. K. Laurenson, H. I. McCallum, M. R. Roberts, and R. Woodroffe. 2002. The role of pathogens in biological conservation. Pp. 139 150 in P. J. Hudson, A. Rizzoli, B. T. Grenfell, H. Heesterbeek, and A. P. Dobson, eds. The ecology of wildlife diseases. Oxford Univ. Press.
16. Daszak, P., A. A. Cunningham, and A. D. Hyatt. 2000. Emerging infectious diseases of wildlife - threats to biodiversity and human health. Science 287 : 443 449.
17. De Roode, J. C., L. R. Gold, and S. Altizer. 2007. Virulence determinants in a natural butterfly-parasite system. Parasitology 134 : 657 668.
18. De Roode, J. C., A. B. Pedersen, M. D. Hunter, and S. Altizer. 2008a. Host plant species affects virulence in monarch butterfly parasites. J. Anim. Ecol. 77 : 120 126.
19. De Roode, J. C., A. J. Yates, and S. Altizer. 2008b. Virulence- transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proc. Natl. Acad. Sci. USA 105 : 7489 7494.
20. De Roode, J. C., J. Chi, R. M. Rarick, and S. Altizer. 2009. Strength in numbers: high parasite burdens increase transmission of a protozoan parasite of monarch butterflies (Danaus plexippus). Oecologia 161 : 67 75.
21. Dieckmann, U., J. A. J. Metz, M. A. Sabelis, and K. Sigmund. 2002. Adaptive dynamics of infectious diseases: in pursuit of virulence management. Cambridge Univ. Press, Cambridge, UK.
22. Diffley, P., J. O. Scott, K. Mama, and T. N. Tsen. 1987. The rate of proliferation among African trypanosomes is a stable trait that is directly related to virulence. Am. J. Trop. Med. Hyg. 36 : 533 540.
23. Dybdahl, M. F., and A. Storfer. 2003. Parasite local adaptation: Red Queen versus Suicide King. Trends Ecol. Evol. 18 : 523 530.
24. Ebert, D. 1999. The evolution and expression of parasite virulence. Pp. 161 172 in S. C. Stearns, ed. Evolution in health and disease. Oxford Univ. Press, Oxford, UK.
25. Ebert, D., and J. J. Bull. 2003. Challenging the trade-off model for the evolution of virulence: is virulence management feasible? Trends Microbiol 11 : 15 20.
26. Ewald, P. W. 1994. Evolution of infectious disease. Oxford Univ. Press, Oxford, UK.
27. Fenner, F., and F. N. Ratcliffe. 1965. Myxomatosis. Cambridge Univ. Press, Oxford, UK.
28. Fineblum, W. L., and M. D. Rausher. 1995. Tradeoff between resistance and tolerance to herbivore damage in a morning glory. Nature 377 : 517 520.
29. Frank, S. A. 1996. Models of parasite virulence. Q. Rev. Biol. 71 : 37 78.
30. Fraser, C., T. D. Hollingsworth, R. Chapman, F. de Wolf, and W. P. Hanage. 2007. Variation in HIV-1 set-point viral load: epidemiological analysis and an evolutionary hypothesis. Proc. Natl. Acad. Sci. USA 104 : 17441 17446.
31. Galvani, A. P. 2003. Epidemiology meets evolutionary ecology. Trends Ecol. Evol. 18 : 132 139.
32. Gandon, S. 2002. Local adaptation and the geometry of host-parasite coevolution. Ecol. Letters 5 : 246 256.
33. Gandon, S., and Y. Michalakis. 2000. Evolution of parasite virulence against qualitative or quantitative host resistance. Proc. R. Soc. Lond. B. 267 : 985 990.
34. Gandon, S., M. J. Mackinnon, S. Nee, and A. F. Read. 2001. Imperfect vaccines and the evolution of pathogen virulence. Nature 414 : 751 756.
35. Graham, A. L., J. E. Allen, and A. F. Read. 2005. Evolutionary causes and consequences of immunopathology. Annu. Rev. Ecol. Evol. Syst. 36 : 373 397.
36. Grech, K., K. Watt, and A. F. Read. 2006. Host-by-parasite interactions for virulence and resistance in a malaria model system. J. Evol. Biol. 19 : 1620 1630.
37. Greischar, M. A., and B. Koskella. 2007. A synthesis of experimental work on parasite local adaptation. Ecol. Letts. 10 : 418 434.
38. Hamilton, W. D. 1980. Sex versus non-sex versus parasite. Oikos 35 : 282 290.
39. Hamilton, W. D., R. Axelrod, and R. Tanese. 1990. Sexual reproduction as an adaptation to resist parasites. Proc. Natl. Acad. Sci. USA 87 : 3566 3573.
40. Imhoof, B., and P. Schmid-Hempel. 1998. Patterns of local adaptation of a protozoan parasite to its bumblebee host. Oikos 82 : 59 65.
41. Jensen, K. H., T. J. Little, A. Skorping, and D. Ebert. 2006. Empirical support for optimal virulence in a castrating parasite. PLoS Biol. 4 : e197.
42. Kaltz, O., and J. A. Shykoff. 1998. Local adaptation in host-parasite systems. Heredity 81 : 361 370.
43. Kaltz, O., S. Gandon, Y. Michalakis, and J. A. Shykoff. 1999. Local maladaptation in the anther-smut fungus Microbotryum violaceum to its host plant Silene latifolia: evidence from a cross-inoculation experiment. Evolution 53 : 395 407.
44. Koskela, T., S. Puustinen, V. Salonen, and P. Mutikainen. 2002. Resistance and tolerance in a host plant-holoparasitic plant interaction: genetic variation and costs. Evolution 56 : 899 908.
45. Lafferty, K., and L. Gerber. 2002. Good medicine for conservation biology: the intersection of epidemiology and conservation theory. Conserv. Biol. 16 : 593 604.
46. Laine, A. L. 2007. Pathogen fitness components and genotypes differ in their sensitivity to nutrient and temperature variation in a wild plant-pathogen association. J. Evol. Biol. 20 : 2371 2378.
47. Laine, A. L. 2008. Temperature-mediated patterns of local adaptation in a natural plant-pathogen metapopulation. Ecol. Letts. 11 : 327 337.
48. Lambrechts, L., J. Halbert, P. Durand, L. C. Gouagna, and J. C. Koella. 2005. Host genotype by parasite genotype interactions underlying the resistance of anopheline mosquitoes to Plasmodium falciparum. Malaria J. 4 : 3.
49. Lambrechts, L., S. Fellous, and J. C. Koella. 2006. Coevolutionary interactions between host and parasite genotypes. Trends Parasitol. 22 : 12 16.
50. Lefèvre, T., M. Sanchez, F. Ponton, D. Hughes, and F. Thomas. 2007. Virulence in resistance in malaria: who drives the outcome of infection? Trends Parasitol 23 : 299 302.
51. Levin, B. R. 1996. The evolution and maintenance of virulence in microparasites. Emerg. Infect. Dis. 2 : 93 102.
52. Levin, S., and D. Pimentel. 1981. Selection of intermediate rates of increase in parasite-host systems. Am. Nat. 117 : 308 315.
53. Lipsitch, M., and E. R. Moxon. 1997. Virulence and transmissibility of pathogens: what is the relationship? Trends Microbiol 5 : 31 37.
54. Lively, C. M. 1989. Adaptation by a parasitic trematode to local populations of its snail host. Evolution 43 : 1663 1671.
55. Lively, C. M. 1999. Migration, virulence, and the geographic mosaic of adaptation by parasites. Am. Nat. 153 : S34 S47.
56. Lively, C. M., and M. F. Dybdahl. 2000. Parasite adaptation to locally common host genotypes. Nature 405 : 679 681.
57. Mackinnon, M. J., and A. F. Read. 1999. Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53 : 689 703.
58. Mackinnon, M. J., and A. F. Read. 2004. Immunity promotes virulence evolution in a malaria model. PLoS Biol. 2 : E230.
59. Mackinnon, M. J., S. Gandon, and A. F. Read. 2008. Virulence evolution in response to vaccination: the case of malaria. Vaccine 26 : C42 C52.
60. Malcolm, S. B., and L. P. Brower. 1989. Evolutionary and ecological implications of cardenolide sequestration in the monarch butterfly. Experientia 45 : 284 295.
61. Manning, S. D., M. E. J. Woolhouse, and J. Ndamba. 1995. Geographic compatibility of the freshwater snail Bulinus globosus and schistosomes from the Zimbabwe Highveld. Int. J. Parasitol. 25 : 37 42.
62. Margolis, E., and B. R. Levin. 2008. The evolution of bacteria-host interactions: virulence and the immune over-response. Pp. 3 12 in F. Baquero, C. Nombela, G. H. Cassell, and A. Gutierrez, eds. Evolutionary biology of bacterial and fungal pathogens. ASM Press, Washington.
63. Mauricio, R., M. D. Rausher, and D. S. Burdick. 1997. Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78 : 1301 1311.
64. McCoy, K. D., T. Boulinier, S. Schjorring, and Y. Michalakis. 2002. Local adaptation of the ectoparasite Ixodes uriae to its seabird host. Evol. Ecol. Res. 4 : 441 456.
65. McLaughlin, R. E., and J. Myers. 1970. Ophryocystis elektroscirrha sp. n., a neogregarine pathogen of monarch butterfly Danaus plexippus (L.) and the Florida queen butterfly D. gilippus berenice Cramer. J. Protozool. 17 : 300 305.
66. Mead-Briggs, A. R., and J. A. Vaughan. 1975. Differential transmissibility of Myxoma virus strains of differing virulence grades by rabbit flea Spilopsyllus cuniculi (Dale). J. Hyg. (Lond). 75 : 237 247.
67. Messenger, S. L., I. J. Molineux, and J. J. Bull. 1999. Virulence evolution in a virus obeys a trade-off. Proc. R. Soc. Lond. B 266 : 397 404.
68. Miller, M. R., A. White, and M. Boots. 2005. The evolution of host resistance: tolerance and control as distinct strategies. J. Theor. Biol. 236 : 198 207.
69. Miller, M. R., A. White, and M. Boots. 2006. The evolution of parasites in response to tolerance in their hosts: the good, the bad, and apparent commensalism. Evolution 60 : 945 956.
70. Nuismer, S. L., and S. Gandon. 2008. Moving beyond common-garden and transplant designs: insight into the causes of local adaptation in species interactions. Am. Nat. 171 : 658 668.
71. Parker, M. A. 1985. Local population differentiation for compatibility in an annual legume and its host-specific fungal pathogen. Evolution 39 : 713 723.
72. Rausher, M. D. 2001. Co-evolution and plant resistance to natural enemies. Nature 411 : 857 864.
73. Restif, O., and J. C. Koella. 2003. Shared control of epidemiological traits in a coevolutionary model of host-parasite interactions. Am. Nat. 161 : 827 836.
74. Roy, B. A., and J. W. Kirchner. 2000. Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54 : 51 63.
75. Salvaudon, L., V. Heraudet, and J. A. Shykoff. 2005. Parasite-host fitness trade-offs change with parasite identity: genotype-specific interactions in a plant-pathogen system. Evolution 59 : 2518 2524.
76. Salvaudon, L., V. Heraudet, and J. A. Shykoff. 2007. Genotype-specific interactions and the trade-off between host and parasite fitness. BMC Evol. Biol. 7 : 189.
77. Sasaki, A., and Y. Iwasa. 1991. Optimal growth schedule of pathogens within a host: switching between lytic and latent cycles. Theor. Popul. Biol. 39 : 201 239.
78. Simms, E. L., and J. Triplett. 1994. Costs and benefits of plant responses to disease - resistance and tolerance. Evolution 48 : 1973 1985.
79. Stowe, K. A., R. J. Marquis, C. G. Hochwender, and E. L. Simms. 2000. The evolutionary ecology of tolerance to consumer damage. Ann. Rev. Ecol. Syst. 31 : 565 595.
80. Thompson, J. N. 1999. Specific hypotheses on the geographic mosaic of coevolution. Am. Nat. 152 : S1 S14.
81. Thompson, J. N., and J. J. Burdon. 1992. Gene-for-gene coevolution between plants and parasites. Nature 360 : 121 125.
82. Thrall, P. H., J. J. Burdon, and J. D. Bever. 2002. Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction. Evolution 56 : 1340 1351.
83. Tiffin, P., and M. D. Rausher. 1999. Genetic constraints and selection acting on tolerance to herbivory in the common morning glory Ipomoea purpurea. Am. Nat. 154 : 700 716.
84. Turner, C. M., N. Aslam, and C. Dye. 1995. Replication, differentiation, growth and the virulence of Trypanosoma brucei infections. Parasitology 111 : 289 300.
85. Urquhart, F. A., and N. R. Urquhart. 1978. Autumnal migration routes of the eastern population of the monarch butterfly (Danaus p. plexippus L.; Danaidae; Lepidoptera) in North America to the overwintering site in the Neovolcanic Plateau of Mexico. Can. J. Zool. 56 : 1759 1764.
86. Van Baalen, M., and M. W. Sabelis. 1995. The dynamics of multiple infection and the evolution of virulence. Am. Nat. 146 : 881 910. (Pubitemid 3025116)
87. Windsor, D. A. 1998. Most of the species on Earth are parasites. Int. J. Parasitol. 28 : 1939 1941.
88. Woodson, R. E. 1954. The North American species of Asclepias L. Ann. Mo. Bot. Gard. 41 : 1 211.