Evolution of an aphid-parasitoid interaction: Variation in resistance to parasitism among aphid populations specialized on different plants

Evolution

Volumn 53, Issue 5, 1999, Pages 1435-1445

  Hufbauer, Ruth A ^a   Via, Sara ^a,b  

^a Department of Obstetrics Gynecology   (United States)

^b Bldg 142   (United States)

Author keywords

Coevolution; Evolution of resistance; Herbivore; Parasitoid; Pea aphid; Population structure; Tritrophic interactions

Indexed keywords

BEHAVIOR; EVOLUTION; HOST PARASITE INTERACTION;

APHID; EVOLUTION; HERBIVORE; HOST-PARASITOID INTERACTION; PARASITE RESISTANCE;

ACYRTHOSIPHON PISUM; ANIMALIA; APHIDIDAE; APHIDIUS ERVI; FAVA; HEMIPTERA; HEXAPODA; HOMOPTERA; INSECTA; MEDICAGO SATIVA; PHASEOLUS (ANGIOSPERM); PISUM SATIVUM; TRIFOLIUM; VESPIDAE; VICIA FABA;

EID: 0032744087     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1558-5646.1999.tb05408.x     Document Type: Article

References (79)

1. Angalet, G. W., and R. Fuester. 1977. The Aphidius parasites of the pea aphid Acyrthosiphon pisum in the eastern half of the United States. Ann. Entomol. Soc. Am. 70:87-96.
2. Barton, N., and A. Clark. 1990. Population structure and process in evolution. Pp. 115-173 in K. Worhmann and S. K. Jain, eds. Population biology. Springer, New York.
3. Battaglia, D., F. Pennacchio, A. Romano, and A. Tranfaglia. 1995. The role of physical cues in the regulation of host recognition and acceptance behavior of Aphidius ervi Haliday (Hymenoptera: Braconidae). J. Insect Behavior 8:739-750.
4. Berdegue, M., J. T. Trumble, J. D. Hare, and R. A. Redak. 1996. Is it enemy-free space? The evidence for terrestrial insects and freshwater arthropods. Ecol. Entomol. 21:203-217.
5. Berenbaum, M. R., and A. R. Zangerl. 1998. Population-level adaptation to host-plant chemicals: the role of cytochrome P450 monooxygenases. Pp. 91-112 in S. Mopper and S. Y. Strauss, eds. Genetic structure and local adaptation in natural insect populations. Chapman and Hall, New York.
6. Bernays, E., and M. Graham. 1988. On the evolution of host specificity in phytophagous arthropods. Ecology 68:88-97.
7. Bradshaw, A. D. 1991. Genostasis and the limits to evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 333:289-305.
8. Carton, Y., and A. Nappi. 1991. The Drosophila immune reaction and the parasitoid capacity to evade it: genetic and coevolutionary aspects. Acta Oecol. 12:89-104.
9. Carver, M., and L. T. Woolcock. 1985. Interactions between Acyrthosiphon kondoi (Homoptera: Aphidoidea) and Aphelinus asychis (Hymenoptera: Chalcidoidea) and other parasites and hosts. Entomophaga 30:193-198.
10. Clark, T. L., and F. J. Messina. 1998. Plant architecture and the foraging success of ladybird beetles attacking the Russian wheat aphid. Entomol. Exp. Appl. 86:153-161.
11. Davies, D. H., and M. T. Siva-Jothy. 1991. Encapsulation in insects: polydnaviruses and encapsulation-promoting factors. Pp. 119-132 in A. P. Gupta, ed. Immunology of insects and other arthropods. CRC Press, Boca Raton, FL.
12. Dixon, A. F. G. 1985. Aphid ecology. Blackie and Sons, London.
13. Doutt, R. L. 1959. The biology of parasite Hymenoptera. Annu. Rev. Entomol. 4:161-182.
14. Du, Y.-J., G. M. Poppy, and W. Powell. 1996. Relative importance of semiochemicals from first and second trophic levels in host foraging behavior of Aphidius ervi. J. Chem. Ecol. 22:1591-1605.
15. Duffy, S. S., K. A. Bloem, and B. C. Campbell. 1986. Consequences of sequestration of plant natural products in plant-insect-parasitoid interactions. Pp. 31-60 in D. J. Boethel and R. D. Eikenbary, eds. Interactions of plant resistance and parasitoids and predators of insects. Ellis Harwood, Chichester, UK.
16. Ebert, D. 1994. Virulence and local adaptation of a horizontally transmitted parasite. Science 265:1084-1086.
17. Eigenbrode, S. D., S. Moodie, and T. Castagnola. 1995. Predators mediate host plant resistance to a phytophagous pest in cabbage with glossy leaf wax. Entomol. Exp. Appl. 77:335-342.
18. Feder, J. L. 1995. The effects of parasitoids on sympatric host races of Rhagoletis pomonella (Diptera: Tephritidae). Ecology 76:801-813.
19. Feder, J. L., S. H. Berlocher, and S. B. Opp. 1998. Sympatric hostrace formation and speciation in Rhagoletis (Diptera: Tephritidae): a tale of two species for Charles D. Pp. 407-442 in S. Mopper and S. Y. Strauss, eds. Genetic structure and local adaptation in natural insect populations. Chapman and Hall, New York.
20. Feeny, P. 1976. Plant apparency and chemical defense. Recent Adv. Phytochem. 10:1-40.
21. _. 1992. The evolution of chemical ecology: contributions from the study of herbivorous insects. Pp. 1-44 in G. A. Rosenthal and M. R. Berenbaum, eds. Herbivores: their interactions with secondary plant metabolites. 2d ed. Vol. 2. Evolutionary and ecological processes. Academic Press, Inc., San Diego, CA.
22. Fryer, G. 1986. Enemy-free space: a new name for an ancient ecological concept. Biol. J. Linn. Soc. 27:287-292.
23. Godfray, H. C. J. 1993. Parasitoids. Princeton Univ. Press, Princeton, NJ.
24. Gonzalez, D., K. S. Hagen, P. Stary, G. W. Bishop, D. W. Davis, and K. S. Pike. 1995. Pea aphid and blue alfalfa aphid. Pp. 129-135 in J. R. Nechols, L. A. Andrew, J. W. Beardsley, R. D. Goeden, and D. G. Jackson, eds. Biological control in the western United States. Univ. of California Division of Agriculture and Natural Resources publication no. 3361.
25. Grevstad, F. S., and B. W. Klepetka. 1992. The influence of plant architecture on the foraging efficiencies of a suite of ladybird beetles feeding on aphids. Oecologia 92:399-404.
26. Halfhill, J. E., P. E. Featherson, and A. G. Dicke. 1972. History of Praon and Aphidius parasites of the pea aphid in the Pacific Northwest. Environ. Entomol. 1:402-405.
27. Hastings, A., and S. Harrison. 1994. Metapopulation dynamics and genetics. Annu. Rev. Ecol. Syst. 25:167-188.
28. Henter, H. J. 1992. The ecological genetics of interactions between the pea aphid (Acyrthosiphon pisum) and the parasitoid Aphidius ervi. Ph.D. diss., Cornell University, Ithaca, NY.
29. _. 1995. The potential for coevolution in a host-parasitoid system. II. Genetic variation within a population of wasps in the ability to parasitize an aphid host. Evolution 49:439-445.
30. Henter, H. J., and S. Via. 1995. The potential for coevolution in a host-parasitoid system. I. Genetic variation within an aphid population in susceptibility to a parasitic wasp. Evolution 49:427-438.
31. Holt, R. D., and M. E. Hochberg. 1997. When is biological control evolutionarily stable? Ecology 78:1673-1683.
32. Huffaker, C. B. 1958. Experimental studies on predation: dispersion factors and predator-prey oscillations. Hilgardia 27:343-383.
33. Itami, J. K., T. P. Craig, and J. D. Horner. 1998. Factors affecting gene flow between the host races of Eurosta solidaginis. Pp. 375-407 in S. Mopper and S. Y. Strauss, eds. Genetic structure and local adaptation in natural insect populations. Chapman and Hall, New York.
34. Jarosz, A. M., and J. J. Burdon. 1991. Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini. II. Local and regional variation in patterns of resistance and racial structure. Evolution 45:1618-1627.
35. Jeffries, M. J., and J. H. Lawton. 1984. Enemy free space and the structure of ecological communities. Biol. J. Linn. Soc. 23:269-286.
36. Jervis, M. A. 1997. Parasitoids as limiting and selective factors: can biological control be evolutionarily stable? Trends Ecol. Evol. 12:378-379.
37. Karban, R. 1989. Fine-scale adaptation of herbivorous thrips to individual host plants. Nature 340:60-61.
38. Kester, K. M., and P. Barbosa. 1991. Behavioral and ecological constraints imposed by plants on insect parasitoids: implications for biological control. Biol. Control 1:94-106.
39. Kraaijeveld, A. R., and J. J. M. Van Alphen. 1995. Geographical variation in encapsulation ability of Drosophila melanogaster larvae and evidence for parasitoid-specific components. Evol. Ecol. 9:10-17.
40. Kraaijeveld, A. R., J. J. M. Van Alphen, and H. C. J. Godfray. 1998. The coevolution of host resistance and parasitoid virulence. Parasitology 116:829-845.
41. Lamb, R. J., and P. J. Pointing. 1972. Sexual morph determination in the aphid Acyrthosiphon pisum. J. Insect Physiol. 18:2029-2042.
42. Littell, R. C., G. A. Milliken, W. W. Stroup, and R. D. Wolfinger. 1996. SAS system for mixed models. SAS Institute, Inc,. Cary, NC.
43. Lively, C. M. 1989. Adaptation by a parasitic trematode to local populations of its snail host. Evolution 43:1663-1671.
44. Loader, C., and H. Damman. 1991. Nitrogen content of food plants and vulnerability of Pieris rapae to natural enemies. Ecology 72:1586-1590.
45. Losey, J. E., and R. F. Denno. 1998. The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behavior. Ecol. Entomol. 23:53-61.
46. Mackauer, M., and A. Campbell. 1972. The establishment of three exotic parasites (Hymenoptera: Aphidiidae) in British Columbia. J. Entomol. Soc. BC 69:54-58.
47. Mopper, S., and S. Y. Strauss. 1998. Genetic structure and local adaptation in natural insect populations. Chapman and Hall, New York.
48. Mopper, S., M. Beck, D. Simberloff, and P. Stiling. 1995. Local adaptation and agents of selection in a mobile insect. Evolution 49:810-815.
49. Neter, J., W. Wasserman, and M. H. Kutner. 1990. Applied linear statistical models. Irwin, Boston, MA.
50. Nicholson, A. J., and V. A. Bailey. 1935. The balance of animal populations. Proc. Zool. Soc. Lond. B Biol. Sci. 3:551-598.
51. Obrycki, J. J. 1986. The influence of foliar pubescence on entomophagous species. Pp. 61-83 in D. J. Boethel and R. D. Eikenbary, eds. Interactions of plant resistance and parasitoids and predators of insects. Ellis Harwood, Chichester, UK.
52. Parker, M. A. 1985. Local population differentiation for compatibility in an annual legume and its host specific fungal pathogen. Evolution 39:713-723.
53. Pellmyr, O., and J. N. Thompson. 1992. Multiple occurrences of mutualism in the yucca moth lineage. Proc. Natl. Acad. Sci. USA 88:2927-2929.
54. Powell, W., and A. F. Wright. 1992. The influence of host food plants on host recognition by four aphidiine parasitoids (Hymenoptera: Braconidae). Bull. Entomol. Res. 81:449-453.
55. Price, P. W. 1986. Ecological aspects of host plant resistance and biological control: interactions among three trophic levels. Pp. 11-30 in D. J. Boethel and R. D. Eikenbary, eds. Interactions of plant resistance and parasitoids and predators of insects. Ellis Harwood, Chichester, UK.
56. _. 1991. Evolutionary theory of host and parasitoid interactions. Biol. Control 1:83-93.
57. Price, P. W., C. E. Bouton, P. Gross, B. A. McPheron, J. N. Thompson, and A. E. Weis. 1980. Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst. 11:41-65.
58. Read, D. P., P. P. Feeny, and R. B. Root. 1970. Habitat selection by the aphid parasite Diaeretiella rapae (Hymenoptera Braconidae) and hyperparasite Charips brassicae (Hymenoptera: Cynipidae). Can. Entomol. 102:1567-1578.
59. Sandstrom, J. 1994a. High variation in host adaptation among clones of the pea aphid, Acyrthosiphon pisum, on peas, Pisum sativum. Entoml. Exp. Appl. 71:245-256.
60. _. 1994b. Performance of pea aphid (Acyrthosiphon pisum) clones on host plants and synthetic diets mimicking the same plants' phloem amino acid composition. J. Insect Physiol. 40:1051-1057.
61. _. 1996. Temporal changes in host adaptation in the pea aphids, Acyrthosiphon pisum. Ecol. Entomol. 21:56-62.
62. SAS Institute. 1997. SAS/STAT software: changes and enhancements through release 6.12. SAS Institute, Inc., Cary, NC.
63. Stiling, P., and A. M. Rossi. 1996. Complex effects of genotype and environment on insect herbivores and their natural enemies on coastal plants. Ecology 77:2212-2218.
64. Storfer, A., and A. Sih. 1998. Gene flow and ineffective antipredator behavior in a stream-breeding salamander. Evolution 52:558-565.
65. Strand, M. R., and L. L. Pech. 1995. Immunological basis for compatibility in parasitoid-host relationships. Annu. Rev. Entomol. 40:31-56.
66. Stubblebine, W. H., and J. H. Langenheim. 1977. Effects of Hymenaea courbaril leaf resin on the generalist herbivore Spodoptera exigua (beet armyworm). J. Chem Ecol. 3:633-647.
67. Thompson, J. N. 1994. The Coevolutionary Process. Univ. of Chicago Press, Chicago.
68. Thorpe, K. W., and P. Barbosa. 1986. Effects of consumption of high and low nicotine tobacco by Manduca sexta (Lepidoptera: Sphingidae) on survival of gregarious endoparasitoid Cotesia congregata (Hymenoptera: Braconidae). J. Chem. Ecol. 12:1329-1337.
69. Vet, L. E., and M. Dicke. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37:141-172.
70. Via, S. 1991a. The genetic structure of host plant adaptations in a spatial patchwork: demographic variability among reciprocally transplanted pea aphid clones. Evolution 45:827-852.
71. _. 1991b. Specialized host plant performance of pea aphids clones is not altered by experience. Ecology 72:1420-1427.
72. _. 1994. Population structure and local adaptation in a clonal herbivore. Pp. 58-85 in L. Real, ed. Ecological genetics. Princeton Univ. Press, Princeton, NJ.
73. _. 1999. Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 53:1446-1457.
74. Via, S., and A. J. Shaw. 1996. Short-term evolution in the size and shape of pea aphids. Evolution 50:163-173.
75. Vinson, S. B. 1981. Habitat location. Pp. 51-77 in D. A. Nordlund, R. L. Jones, and W. J. Lewis, eds. Semiochemicals, their role in pest control. Wiley, New York.
76. _. 1990. How parasitoids deal with the immune system of their hosts: an overview. Arch. Insect Biochem. Physiol. 13:3-27.
77. Vinson, S. B., and G. F. Iwantsch. 1980. Host suitability for insect parasitoids. Annu. Rev Entomol. 25:397-419.
78. Wright, S. 1940. Breeding structure of populations in relation to speciation. Am. Nat. 74:232-48.
79. _. 1978. Evolution and the genetics of populations. IV. Variability within and among populations. Univ. of Chicago Press, Chicago.