Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense

Evolution

Volumn 51, Issue 5, 1997, Pages 1435-1444

  Mauricio, Rodney ^a,b   Rausher, Mark D ^a  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Arabidopsis thaliana; Benefits; Coevolution; Costs; Glucosinolates; Herbivory; Natural selection; Resistance; Trichome

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 0030784809     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1558-5646.1997.tb01467.x     Document Type: Article

References (87)

1. ABBOTT, R. J., AND M. F. GOMES. 1987. Outcrossing rates in natural populations of Arabidopsis thaliana. Arabidopsis Inf. Serv. 25: 85-88.
2. ÅGREN, J., AND D. W. SCHEMSKE. 1994. Evolution of trichome number in a naturalized population of Brassica rapa. Am. Nat. 143:1-13.
3. ALEXANDER, H. M. 1992. Evolution of disease resistance in natural plant populations. Pp. 326-344 in R. S. Fritz and E. L. Simms, eds. Plant resistance to herbivores and pathogens. Univ. of Chicago Press, Chicago.
4. ARNOLD, S. J. 1981. Behavioral variation in natural populations. I. Phenotypic, genetic and environmental correlations between chemoreceptive responses to prey in the garter snake, Thamnophis elegans. Evolution 35:489-509.
5. BASKIN, J. M., AND C. C. BASKIN. 1972. Ecological life cycle and physiological ecology of seed germination of Arabidopsis thaliana. Can. J. Bot. 50:353-360.
6. BERENBAUM, M. R. 1978. Toxicity of a furanocoumarin to army-worms: a case of biosynthetic escape from insect herbivores. Science 201:532-534.
7. _. 1983. Coumarins and caterpillars: a case for coevolution. Evolution 37:163-179.
8. BERENBAUM, M. R., A. R. ZANGERL, AND J. K. NITAO. 1986. Constraints on chemical coevolution: wild parsnips and the parsnip webworm. Evolution 40:1215-1228.
9. BERNAYS, E. A. 1978. Tannins: an alternative viewpoint. Entomol. Exp. Appl. 24:44-53.
10. BERNAYS, E. A., AND M. GRAHAM. 1988. On the evolution of host specificity phytophagous arthropods. Ecology 69:886-892.
11. BLAU, P. A., P. FEENY, L. CONTARDO, AND D. S. ROBSON. 1978. Allylglucosinolate and herbivorous caterpillars: a contrast in toxicity and tolerance. Science 200:1296-1298.
12. BURDON, J. J. 1987. Diseases and plant population biology. Cambridge Univ. Press, Cambridge.
13. COOPER-DRIVER, G. A., AND T. SWAIN. 1976. Cyanogenic polymorphism in bracken in relation to herbivore predation. Nature (Lond.) 260:604.
14. DANGL, J. L., E. B. HOLUB, T. DEBENER, H. LEHNACKERS, C. RITTER, AND I. R. CRUTE. 1992. Genetic definition of loci involved in Arabidopsis-pathogen interactions. Pp. 393-418 in Koncz, C., N.-H. Chua, and J. Schell, eds. Methods in Arabidopsis Research. World Scientific, Singapore.
15. DIRZO, R., AND J. L. HARPER. 1982. Experimental studies on slug-plant interactions. III. Differences in the acceptability of individual plants of Trifolium repens to slugs and snails. J. Ecol. 70: 101-117.
16. DUDLEY, S. A. 1996. Differing selection on plant physiological traits in response to environmental water availability: a test of adaptive hypotheses. Evolution 50:92-102.
17. EHLERINGER, J. R., AND O. BJÖRKMAN. 1978. A comparison of photosynthetic characteristics of Encelia species possessing glabrous and pubescent leaves. Plant Physiol. 62:185-190.
18. EHLERINGER, J. R., O. BJÖRKMAN, AND H. A. MOONEY. 1976. Leaf pubescence: effects on absorption and photosynthesis in a desert shrub. Science 192:376-377.
19. EHRLICH, P. R., AND P. H. RAVEN. 1964. Butterflies and plants: a study in coevolution. Evolution 18:586-608.
20. ENDLER, J. A. 1986. Natural selection in the wild. Princeton Univ. Press, Princeton, NJ.
21. FAGERSTROM, T., S. LARSSON, AND O. TENOW. 1987. On optimal defence in plants. Funct. Ecol. 1:73-81.
22. FEENY, P. 1970. Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:565-581.
23. FRAENKEL, G. S. 1959. The raison d'être of secondary plant substances. Science 129:1466-1470.
24. FUTUYMA, D. J. 1983. Evolutionary interactions among herbivorous insects and plants. Pp. 207-231 in D. J. Futuyma and M. Slatkin, eds. Coevolution. Sinauer, Sunderland, MA.
25. GOMES, M. F., AND R. J. ABBOTT. 1987. Genotypic diversity in British populations of Arabidopsis thaliana based on a survey of isozyme variation. Arabidopsis Inf. Serv. 23:25-30.
26. GULMON, S. L., AND H. A. MOONEY. 1986. Costs of defense and their effects on plant productivity. Pp. 681-698 in T. J. Givnish, ed. On the economy of plant form and function. Cambridge Univ. Press, Cambridge.
27. HAIRSTON, N. G., F. E. SMITH, AND L. B. SLOBODKIN. 1960. Community structure, populations control, and competition. Am. Nat. 94:421-425.
28. HASLAM, E. 1986. Secondary metabolism - fact or fiction. Nat. Prod. Rep. 3:217-249.
29. HEANEY, R. K., AND G. R. FENWICK. 1981. A micro-column method for the rapid determination of total glucosinolate content of cruciferous material. Z. Pflanzenzücht. 87:89-95.
30. HOGGE, L. R., D. W. REED, E. W. UNDERBILL, AND G. W. HAUGHN. 1988. HPLC separation of glucosinolates from leaves and seeds of Arabidopsis thaliana and their identification using thermospray liquid chromatography/mass spectrometry. J. Chromatogr. Sci. 26:551-556.
31. JANZEN, D. H. 1980. When is it coevolution? Evolution 34:611-612.
32. JERMY, T. 1976. Insect-host-plant relationship-co-evolution or sequential evolution? Symp. Biol. Hung. 16:109-113.
33. _. 1984. Evolution of insect/host plant relationships. Am. Nat. 124:609-630.
34. JOHNSON, H. B. 1975. Plant pubescence: an ecological perspective. Bot. Rev. 41:233-258.
35. JONES, C. G., AND R. D. FIRN. 1991. On the evolution of plant secondary chemical diversity. Phil. Trans. R. Soc. Lond. B 333: 273-280.
36. JONES, D. A. 1979. Chemical defense: primary or secondary function? Am. Nat. 113:445-451.
37. JONES, M. E. 1971. The population genetics of Arabidopsis thaliana. I. The breeding system. Heredity 27:39-50.
38. JUNIPER, B. E., AND T. R. E. SOUTHWOOD. 1986. Insects and the plant surface. Edward Arnold, London.
39. KARABOURNIOTIS, G., K. PAPADOPOULOS, M. PAPAMARKOU, AND Y. MANETAS. 1992. Ultraviolet-B radiation absorbing capacity of leaf hairs. Physiol. Plant. 86:414-418.
40. KILIAN, A., AND M. MALUSZYNSKI. 1987. Genetic variability of Arabidopsis thaliana populations from regions of different pollution level. Arabidopsis Inf. Serv. 25:57-66.
41. KILIAN, A., A. ROSTANSKI, AND M. MALUSZYNSKI. 1985. Analysis of the variability of Arabidopsis thaliana natural populations in Poland. Arabidopsis Inf. Serv. 22:77-86.
42. KOCH, E., AND A. SLUSARENKO. 1990. Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2:437-445.
43. LAMB, R. J. 1980. Hairs protect pods of mustard (Brassica hirta "Gisilba") from flea beetle damage. Can. J. Plant Sci. 60:1439-1440.
44. LANDE, R., AND S. J. ARNOLD. 1983. The measurement of selection on correlated characters. Evolution 37:1210-1226.
45. LAWRENCE, M. J. 1976. Variations in natural populations of Arabidopsis thaliana (L). Heynh. Pp. 167-190 in J. G. Vaughan, A. J. MacLeod, and B. M. G. Jones, eds. The biology and chemistry of the Cruciferae. Academic Press, London.
46. LEVIN, D. A. 1973. The role of trichomes in plant defenses. Q. Rev. Biol. 48:3-15.
47. MARQUIS, R. J. 1992. The selective impact of herbivores. Pp. 301-325 in R. S. Fritz and E. L. Simms, eds. Plant resistance to herbivores and pathogens. Univ. of Chicago Press, Chicago.
48. MAURICIO, R. 1998. Costs of resistance to natural enemies in field populations of the annual plant, Arabidopsis thaliana. Am. Nat. In press.
49. MAURICIO, R., AND L. E. MOJONNIER. 1997. Reducing bias in the measurement of selection. Trends Ecol. Evol. In press.
50. 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.
51. MEINZER, F., AND G. GOLDSTEIN. 1985. Some consequences of leaf pubescence in the Andean giant rosette plant Espeletia timotensis. Ecology 66:512-520.
52. MITCHELL-OLDS, T., AND R. G. SHAW. 1987. Regression analysis of natural selection: statistical inference and biological interpretation. Evolution 41:1149-1161.
53. MORGAN, O. D. 1971. A study of four weed hosts of Sclerotinia species in alfalfa fields. Plant Dis. Rep. 55:1087-1089.
54. MULLER, C. H. 1969. The "co-" in coevolution. Science 164:197-198.
55. NIELSHN, J. K. 1978. Host plant discrimination within Cruciferae: feeding responses of four leaf beetles (Coleoptera: Chrysomelidae) to glucosinolates, cucurbitacins and cardenolides. Entomol. Exp. Appl. 24: 41-54.
56. NÚÑEZ-FAREÁN, J., AND R. DIRZO. 1994. Evolutionary ecology of Datura stramonium L. in central Mexico: natural selection for resistance to herbivorous insects. Evolution 48:423-436.
57. PARKER, M. A. 1990. The pleiotropy theory for polymorphism of disease resistance genes in plants. Evolution 44:1872-1875.
58. RATCLIFFE, D. 1961. Adaptation to habitat in a group of annual plants. J. Ecol. 49:187-203.
59. RAUSHER, M. D. 1981. Host plant selection by Battus philenor butterflies: the roles of predation, nutrition, and plant chemistry. Ecol. Monogr. 51:1-20.
60. _. 1984. Tradeoffs in performance on different hosts: evidence from within-and between-site variation in the beetle Delovala guttata. Evolution 38:582-595.
61. _. 1992a. Natural selection and the evolution of plant-insect interactions. Pp. 20-88 in B. D. Roitberg and M. S. Isman, eds. Insect chemical ecology: an evolutionary approach. Routledge, Chapman and Hall, New York.
62. _. 1992b. The measurement of selection on quantitative traits: biases due to environmental covariances between traits and fitness. Evolution 46:616-626.
63. RAUSHER, M. D., AND E. L. SIMMS. 1989. The evolution of resistance to herbivory in Ipomoea purpurea. I. Attempts to detect selection. Evolution 43:563-572.
64. RENWICK, J. A. A., AND C. D. RADKE. 1983. Chemical recognition of host plants for oviposition by the cabbage butterfly, Pieris rapae (Lepidoptera: Pieridae). Environ. Entomol. 12: 446-450.
65. RHOADES, D. F. 1977. Integrated antiherbivore, antidesiccant and ultraviolet screening properties of creosotebush resin. Biochem. Syst. Ecol. 5:281-290.
66. _. 1979. Evolution of plant chemical defenses against herbivory. Pp. 3-54 in G. A. Rosenthal and D. H. Janzen, eds. Herbivores: their interaction with secondary plant metabolites. Academic Press, San Diego, CA.
67. ROSENTHAL, G. A., AND M. BERENBAUM. 1991. Herbivores, their interactions with secondary plant metabolites. 2d ed. Vol. 1. The chemical participants. Academic Press. San Diego, CA.
68. ROUGHGARDEN, J. 1979. Theory of population genetics and evolutionary ecology: an introduction. Macmillan, New York.
69. SAS INSTITUTE. 1988. SAS/GRAPH user's guide. Vers. 6.03 ed. Statistical Analysis Systems Institute, Inc., Cary, NC.
70. _. 1989. SAS/STAT user's guide. Vers. 6.03 ed. Statistical Analysis Systems Institute, Inc., Cary, NC.
71. SCHLUTER, D., AND M. L. NYCHKA. 1994. Exploring fitness surfaces. Am. Nat. 143: 597-616.
72. SCHMITT, T. M., M. E. HAY, AND N. LINDQUIST. 1995. Constraints on chemically mediated coevolution: multiple functions for seaweed secondary metabolites. Ecology 76:107-123.
73. SIEGLER, D., AND P. W. PRICE. 1976. Secondary compounds in plants: primary functions. Am. Nat. 110:101-105.
74. SIMMS, E. L., AND M. D. RAUSHER. 1987. Costs and benefits of plant resistance to herbivory. Am. Nat. 130:570-581.
75. _. 1989. The evolution of resistance to herbivory in Ipomoea purpurea. II. Natural selection by insects and costs of resistance. Evolution 43:573-585.
76. _. 1993. Patterns of selection on phytophage resistance in Ipomoea purpurea. Evolution 47:970-976.
77. SNAPE, J. W., AND M. J. LAWRENCE. 1971. The breeding system of Arabidopsis thaliana. Heredity 27:299-302.
78. THOMAS, C. D., D. NG, M. C. SINGER. J. L. B. MALLET, C. PARMESAN, AND H. L. BILLINGTON. 1987. Incorporation of a European weed into the diet of a North American herbivore. Evolution 41:892-901.
79. THOMPSON, J. N. 1994. The coevolutionary process. Univ. of Chicago Press, Chicago.
80. TRAYNIER, R. M. M., AND R. J. W. TRUSCOTT. 1991. Potent natural egg-laying stimulant for cabbage butterfly Pieris rapae. J. Chem. Ecol. 17:1371-1380.
81. TRNENÁ, L., M. SKÁROVA, J. RELICHOVÁ, AND I. CETL. 1987. High outcrossing rates in a partially fertile line and their significance in the genetic structure of populations in Arabidopsis thaliana (L.) Heynh. Arabidopsis Inf. Serv. 23:31-40.
82. TSUJI, J., AND S. C. SOMERVILLE. 1992. First report of natural infection of Arabidopsis thaliana by Xanthomonas campestris pv. campestris. Plant Dis. 76:539.
83. VAUGHAN, J. G., A. J. MACLEOD, AND B. M. G. JONES. 1976. The biology and chemistry of the Cruciferae. Academic Press, London.
84. VIA, S. 1984. The quantitative genetics of polyphagy in an insect herbivore. II. Genetic correlations in larval performance within and among host plants. Evolution 38:896-905.
85. WADE, M. J., AND S. KALISZ. 1990. The causes of natural selection. Evolution 44:1947-1955.
86. WHITTAKER, R. H., AND P. FEENY. 1971. Allelochemics: chemical interactions between species. Science 171:757-770.
87. WINK, M., AND L. WITTE. 1985. Quinolizidine alkaloids as nitrogen source for lupin seedlings and cell cultures. Z. Naturforsch. Sect. C Biosci. 40:767-775.