Evolution of latex and its constituent defensive chemistry in milkweeds (Asclepias): A phylogenetic test of plant defense escalation

Entomologia Experimentalis et Applicata

Volumn 128, Issue 1, 2008, Pages 126-138

  Agrawal, Anurag A ^a   Lajeunesse, Marc J ^a   Fishbein, Mark ^b  

^a Department of Obstetrics Gynecology   (United States)

^b PORTLAND STATE UNIVERSITY   (United States)

Author keywords

Asclepiadaceae; Cardenolide; Cardiac glycoside; Coevolution; Cysteine protease; Danaus plexippus; Lepidoptera; Macroevolution; Monarch butterfly; Nymphalidae; Phylogenetic analyses; Plant defense theory; Plant insect interactions

Indexed keywords

BUTTERFLY; CHEMICAL DEFENSE; COEVOLUTION; HERBIVORE; PHYLOGENETICS; PLANT DEFENSE; PLANT-HERBIVORE INTERACTION; PLANT-INSECT INTERACTION; SPECIES DIVERSITY; WEED;

APOCYNACEAE; ASCLEPIAS; DANAUS PLEXIPPUS; HEXAPODA; LEPIDOPTERA; NYMPHALIDAE;

EID: 46249128036     PISSN: 00138703     EISSN: 15707458     Source Type: Journal    
DOI: 10.1111/j.1570-7458.2008.00690.x     Document Type: Conference Paper

References (68)

1. Adamowicz SJ Purvis A (2006) From more to fewer? Testing an allegedly pervasive trend in the evolution of morphological structure. Evolution 60 : 1402 1416.
2. Agrawal AA (2004) Resistance and susceptibility of milkweed: competition, root herbivory, and plant genetic variation. Ecology 85 : 2118 2133.
3. Agrawal AA (2005) Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores. Evolutionary Ecology Research 7 : 651 667.
4. Agrawal AA (2007) Macroevolution of plant defense strategies. Trends in Ecology and Evolution 22 : 103 109.
5. Agrawal AA Fishbein M (2006) Plant defense syndromes. Ecology 87 : S132 S149.
6. Agrawal AA Malcolm SB (2002) Once upon a milkweed. Natural History 111 : 48 53.
7. Agrawal AA Van Zandt PA (2003) Ecological play in the coevolutionary theatre: genetic and environmental determinants of attack by a specialist weevil on milkweed. Journal of Ecology 91 : 1049 1059.
8. Alroy J (2000) Understanding the dynamics of trends within evolving lineages. Paleobiology 26 : 319 329.
9. Arribere MC, Cortadi AA, Gattuso MA, Bettiol MP, Priolo NS Caffini NO (1998) Comparison of Asclepiadaceae latex proteases and characterization of Morrenia brachystephana Griseb. cysteine peptidases. Phytochemical Analysis 9 : 267 273.
10. Baker RH Wilkinson GS (2001) Phylogenetic analysis of sexual dimorphism and eye-span allometry in stalk-eyed flies (Diopsidae). Evolution 55 : 1371 1385.
11. Berenbaum M (1983) Coumarins and caterpillars - a case for coevolution. Evolution 37 : 163 179.
12. Blau PA, Feeny P, Contardo L Robson DS (1978) Allylglucosinolate and herbivorous caterpillars: a contrast in toxicity and tolerance. Science 200 : 1296 1298.
13. Bollwinkel CW (1969) A revision of the South American Species of Asclepias L. Southern Illinois University, Carbondale, IL, USA.
14. Brower LP, McEvoy PB, Williamson KL Flannery MA (1972) Variation in cardiac glycoside content of monarch butterflies from natural populations in eastern North America. Science 177 : 426 429.
15. Da Costa CP Jones CM (1971) Cucumber beetle resistance and mite susceptibility controlled by the bitter gene in Cucumis sativus L. Science 172 : 1145 1146.
16. Dixon CA, Erickson JM, Kellett DN Rothschild M (1978) Some adaptations between Danaus plexippus and its food plant, with notes on Danaus chrysippus and Euploea core (Insecta: Lepidoptera). Journal of Zoology 185 : 437 467.
17. Dussourd DE (1997) Plant exudates trigger leaf-trenching by cabbage loopers, Trichoplusia ni (Noctuidae). Oecologia (Berlin) 112 : 362 369.
18. Dussourd DE Denno RF (1991) Deactivation of plant defense: correspondence between insect behavior and secretory canal architecture. Ecology 72 : 1383 1396.
19. Dussourd DE Denno RF (1994) Host range of generalist caterpillars: trenching permits feeding on plants with secretory canals. Ecology 75 : 69 78.
20. Dussourd DE Eisner T (1987) Vein-cutting behavior: insect counterploy to the latex defense of plants. Science 237 : 898 900.
21. Ehrlich PR Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18 : 586 608.
22. Farrell BD, Dussourd DE Mitter C (1991) Escalation of plant defense: do latex and resin canals spur plant diversification. American Naturalist 138 : 881 900.
23. Farrell BD Mitter C (1998) The timing of insect-plant diversification: might Tetraopes (Coleoptera: Cerambycidae) and Asclepias (Asclepiadaceae) have co-evolved? Biological Journal of the Linnean Society 63 : 553 577.
24. Feeny PP (1976) Plant apparency and chemical defense. Biochemical Interaction between Plants and Insects (ed. by JW Wallace RL Mansell pp. 1 40. Plenum, New York, NY, USA.
25. Felsenstein J (1985) Phylogenies and the comparative method. American Naturalist 125 : 1 15.
26. Fine PVA, Miller ZJ, Mesones I, Irazuzta S, Appel HM et al 2006) The growth-defense trade-off and habitat specialization by plants in Amazonian forests. Ecology 87 : S150 S162.
27. Futuyma DJ (1987) On the role of species in anagenesis. American Naturalist 130 : 465 473.
28. Futuyma DJ (1989) Speciational trends and the role of species in macroevolution. American Naturalist 134 : 318 321.
29. Grant V (1963) The Origin of Adaptation. Columbia University Press, New York, NY, USA.
30. Grant V (1989) The theory of speciational trends. American Naturalist 133 : 604 612.
31. Harvey PH Pagel MD (1991) The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford, UK.
32. Hibbett DS (2004) Trends in morphological evolution in homobasidiomycetes inferred using maximum likelihood: a comparison of binary and multistate approaches. Systematic Biology 53 : 889 903.
33. Holzinger F Wink M (1996) Mediation of cardiac glycoside insensitivity in the monarch butterfly (Danaus plexippus): role of an amino acid substitution in the ouabain binding site of Na+/K+-ATPase. Journal of Chemical Ecology 22 : 1921 1937.
34. Konno K, Hirayama C, Nakamura M, Tateishi K, Tamura Y et al 2004) Papain protects papaya trees from herbivorous insects: role of cysteine proteases in latex. Plant Journal 37 : 370 378.
35. Labeyrie E Dobler S (2004) Molecular adaptation of Chrysochus leaf beetles to toxic compounds in their food plants. Molecular Biology and Evolution 21 : 218 221.
36. Lankau RA (2007) Specialist and generalist herbivores exert opposing selection on a chemical defense. New Phytologist 175 : 176 184.
37. Lewinsohn TM (1991) The geographical distribution of plant latex. Chemoecology 2 : 64 68.
38. Liggieri C, Arribere MC, Trejo SA, Canals F, Aviles FX Priolo NS (2004) Purification and biochemical characterization of asclepain c I from the latex of Asclepias curassavica L. Protein Journal 23 : 403 411.
39. Maddison DR Maddison WP (2005) MacClade, version 4.08. Sinauer Associates, Sunderland, MA, USA.
40. Malcolm SB (1995) Milkweeds, monarch butterflies and the ecological significance of cardenolides. Chemoecology 5/6 : 101 117.
41. Martins EP Hansen TF (1997) Phylogenies and the comparative method : A general approach to incorporating phylogenetic information into the analaysis of interspecific data. American Naturalist, 149 : 646 667.
42. McNamara KJ (1990) Evolutionary Trends. University of Arizona Press, Tucson, AZ, USA.
43. van der Meijden E (1996) Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies. Entomologia Experimentalis et Applicata 80 : 307 310.
44. van der Meijden E, Wijn M Verkaar HJ (1988) Defense and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51 : 355 363.
45. Moen DS (2006) Cope's rule in cryptodiran turtles: do the body sizes of extant species reflect a trend of phyletic size increase? Journal of Evolutionary Biology 19 : 1210 1221.
46. Mooers AØ, Vamosi SM Schluter D (1999) Using phylogenies to test macroevolutionary hypotheses of trait evolution in cranes (Gruinae). American Naturalist 154 : 249 259.
47. Moore LV Scudder GGE (1986) Ouabain-resistant Na,K-ATPases and cardenolide tolerance in the large milkweed bug, Oncopeltus fasciatus. Journal of Insect Physiology 32 : 27 33.
48. Nelson CJ, Seiber JN Brower LP (1981) Seasonal and intraplant variation of cardenolide content in the California milkweed Asclepias eriocarpa, and implications for plant defense. Journal of Chemical Ecology 7 : 981 1010.
49. Omland KE (1997) Examining two standard assumptions of ancestral reconstructions: repeated loss of dichromatism in dabbling ducks (Anatini). Evolution 51 : 1636 1646.
50. Pechan T, Cohen A, Williams WP Luthe DS (2002) Insect feeding mobilizes a unique plant defense protease that disrupts the peritrophic matrix of caterpillars. Proceedings of the National Academy of Sciences of the United States of America 99 : 13319 13323.
51. Purvis A Garland T (1993) Polytomies in comparative analyses of continuous characters. Systematic Biology 42 : 569 575.
52. Rohlf FJ (2006) A comment on phylogenetic correction. Evolution 60 : 1509 1515.
53. Ronquist F Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 : 1572 1574.
54. Sanderson MJ (2002) Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Molecular Biology and Evolution 19 : 101 109.
55. Sanderson MJ (2003) r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19 : 301 302.
56. Shukla OP Krishna Murti CR (1971) The biochemistry of plant latex. Journal of Scientific and Industrial Research (India) 30 : 640 662.
57. Simms EL Triplett J (1994) Costs and benefits of plant responses to disease: resistance and tolerance. Evolution 48 : 1973 1985.
58. Stepek G, Buttle DJ, Duce IR, Lowe A Behnke JM (2005) Assessment of the anthelmintic effect of natural plant cysteine proteinases against the gastrointestinal nematode, Heligmosomoides polygyrus, in vitro. Parasitology 130 : 203 211.
59. Steward JL Keeler KH (1988) Are there trade-offs among antiherbivore defenses in Ipomoea (Convolvulaceae)? Oikos 53 : 79 86.
60. Swofford DL Maddison WP (1987) Reconstructing ancestral character states under Wagner parsimony. Mathematical Biosciences 87 : 199 229.
61. Trejo SA, Lopez LMI, Cimino CV, Caffini NO Natalucci CL (2001) Purification and characterization of a new plant endopeptidase isolated from latex of Asclepias fruticosa L. (Asclepiadaceae). Journal of Protein Chemistry 20 : 469 477.
62. Van Zandt PA Agrawal AA (2004) Specificity of induced plant responses to specialist herbivores of the common milkweed, Asclepias syriaca. Oikos 104 : 401 409.
63. Vaughan GL Jungreis AM (1977) Insensitivity of lepidopteran tissues to ouabain - physiological mechanisms for protection from cardiac-glycosides. Journal of Insect Physiology 23 : 585 589.
64. Vermeij GJ (1994) The evolutionary interaction among species: selection, escalation, and coevolution. Annual Review of Ecology and Systematics 25 : 219 236.
65. Whittall JB Hodges SA (2007) Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447 : 706 712.
66. Woodson RE (1954) The North American species of Asclepias L. Annals of the Missouri Botanical Garden 41 : 1 211.
67. Zalucki MP Malcolm SB (1999) Plant latex and first-instar monarch larval growth and survival on three North American milkweed species. Journal of Chemical Ecology 25 : 1827 1842.
68. Zalucki MP, Brower LP Alonso A (2001) Detrimental effects of latex and cardiac glycosides on survival and growth of first-instar monarch butterfly larvae Danaus plexippus feeding on the sandhill milkweed Asclepias humistrata. Ecological Entomology 26 : 212 224.