Antagonistic, stage-specific selection on defensive chemical sequestration in a toxic butterfly

Evolution

Volumn 62, Issue 7, 2008, Pages 1610-1617

  Fordyce, James A ^a   Nice, Chris C ^b  

^a UNIVERSITY OF TENNESSEE   (United States)

^b TEXAS STATE UNIVERSITY   (United States)

Author keywords

Aristolochic acid; Battus philenor; Gregarious feeding; Natural selection; Trade offs

Indexed keywords

ARISTOLOCHIC ACID;

ALKALOID; ANTAGONISM; ARTIFICIAL DIET; BUTTERFLY; CHEMICAL DEFENSE; FAT; HOST PLANT; LARVAL DEVELOPMENT; NATURAL SELECTION; PREDATOR; SURVIVORSHIP; TOXIC ORGANISM; TRADE-OFF;

ANIMAL; ARISTOLOCHIA; ARTICLE; BUTTERFLY; CHEMISTRY; DIET; FEMALE; FOOD CHAIN; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; LIPID METABOLISM; METABOLISM;

ANIMALS; ARISTOLOCHIA; ARISTOLOCHIC ACIDS; BUTTERFLIES; DIET; FEMALE; FOOD CHAIN; LARVA; LIPID METABOLISM; SELECTION (GENETICS); VARIATION (GENETICS);

NORTH AMERICA; TEXAS; UNITED STATES;

ARISTOLOCHIA; ARISTOLOCHIA TOMENTOSA; BATTUS PHILENOR; PAPILIONOIDEA;

EID: 48949118194     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2008.00388.x     Document Type: Article

References (65)

1. Alonso-Mejía, A., and L. P. Brower. 1994. From model to mimic - age-dependent unpalatability in monarch butterflies. Experientia 50 : 176 181.
2. Bates, H. W. 1862. Contributions to an insect fauna of the Amazon Valley. Lepidoptera: Heliconidae. Trans. Linn. Soc. Lond. 23 : 495 566.
3. Berenbaum, M. R., and A. R. Zangerl. 1998. Chemical phenotype matching between a plant and its insect herbivore. Proc. Natl. Acad. Sci. USA 95 : 13743 13748.
4. Boggs, C. L. 1997. Reproductive allocation from reserves and income in butterfly species with differing adult diets. Ecology 78 : 181 191.
5. Bowers, M. D. 1993. Aposematic caterpillars: life-styles of the warningly colored and unpalatable. Pp. 331 371 in N. E. Stamp and T. M. Casey, eds. Caterpillars: ecological and evolutionary constraints on foraging. Chapman and Hall, London, UK.
6. Brower, J. V. Z. 1958a. Experimental studies of mimicry in some North American butterflies. Part II. Battus philenor and Papilio troilus, P. polyxenes and P. glaucus. Evolution 12 : 123 136.
7. Brower, J. V. Z. 1958b. Experimental studies of mimicry in some North American butterflies. Part III. Danaus gilippus berenice and Limenitis archippus floridensis. Evolution 12 : 273 285.
8. Brower, L. P., and J. V. Z. Brower. 1962. The relative abundance of model and mimic butterflies in natural populations of the Battus philenor mimicry complex. Ecology 43 : 154 158.
9. Camara, M. D. 1997a. Physiological mechanisms underlying the costs of chemical defence in Junonia coenia Hubner (Nymphalidae): a gravimetric and quantitative genetic analysis. Evol. Ecol. 11 : 451 469.
10. Camara, M. D. 1997b. Predator responses to sequestered plant toxins in buckeye caterpillars: are tritrophic interactions locally variable J. Chem. Ecol. 23 : 2093 2106.
11. Chen, Z., and D. Zhu. 1987. Aristolochia Alkaloids. Pp. 29 65 in A. Brossi, ed. The Alkaloids: chemistry and pharmacology. Academic Press, Inc., San Diego.
12. Clancy, K. M., and P. W. Price. 1987. Rapid herbivore growth enhances enemy attack: sublethal plant defenses remain a paradox. Ecology 68 : 733 737.
13. Codella, S. G., Jr., and R. C. Lederhouse. 1989. Intersexual comparison of mimetic protection in the black swallowtail butterfly, Papilio polyxenes: experiments with captive blue jay predators. Evolution 43 : 410 420.
14. Duffey, S. S. 1980. Sequestration of plant natural-products by insects. Ann. Rev. Entomol. 25 : 447 477.
15. Dyer, L. A., and M. D. Bowers. 1996. The importance of sequestered iridoid glycosides as a defense against an ant predator. J. Chem. Ecol. 22 : 1527 1539.
16. Engler-Chaouat, H. S., and L. E. Gilbert. 2007. De novo synthesis vs. sequestration: negatively correlated metabolic traits and the evolution of host plant specialization in cyanogenic butterflies. J. Chem. Ecol. 33 : 25 42.
17. Feeny, P. 1976. Plant apparency and chemical defense. Pp. 1 40 in J. W. Wallace and R. L. Mansell, eds. Biochemical interaction between plants and insects. Plenum Press, New York.
18. Feyereisen, R. 1999. Insect P450 enzymes. Ann. Rev. Entomol. 44 : 507 533.
19. Fordyce, J. A. 2001. The lethal plant defense paradox remains: inducible host-plant aristolochic acids and the growth and defense of the pipevine swallowtail. Entomol. Exp. Appl. 100 : 339 346.
20. Fordyce, J. A. 2003. Aggregative feeding of pipevine swallowtall larvae enhances hostplant suitability. Oecologia 135 : 250 257.
21. Fordyce, J. A. 2005. Clutch size plasticity in the Lepidoptera. Pp. 125 144 in T. N. Ananthakrishnan and D. W. Whitman, eds. Insects and phenotypic plasticity. Science Publishers, Inc., Enfield, NH.
22. Fordyce, J. A. 2006. The evolutionary consequences of ecological interactions mediated through phenotypic plasticity. J. Exp. Biol. 209 : 2377 2383.
23. Fordyce, J. A., and A. A. Agrawal. 2001. The role of plant trichomes and caterpillar group size on growth and defence of the pipevine swallowtail Battus philenor. J. Anim. Ecol. 70 : 997 1005.
24. Fordyce, J. A., and C. C. Nice. 2004. Geographic variation in clutch size and a realized benefit of aggregative feeding. Evolution 58 : 447 450.
25. Fordyce, J. A., and A. M. Shapiro. 2003. Another perspective on the slow-growth/high-mortality hypothesis: chilling effects on swallowtail larvae. Ecology 84 : 263 268.
26. Fordyce, J. A., Z. H. Marion, and A. M. Shapiro. 2005. Phenological variation in chemical defense of the pipevine swallowtail, Battus philenor. J. Chem. Ecol. 31 : 2835 2846.
27. Fordyce, J. A., C. C. Nice, and A. M. Shapiro. 2006. A novel trade-off of insect diapause affecting a sequestered chemical defense. Oecologia 149 : 101 106.
28. Gamberale, G., and B. S. Tullberg. 1998. Aposematism and gregariousness: the combined effect of group size and coloration on signal repellence. Proc. R. Soc. Lond. B 265 : 889 894.
29. Glendinning, J. I. 2002. How do herbivorous insects cope with noxious secondary plant compounds in their diet Entomol. Exp. Appl. 104 : 15 25.
30. Haase, E. 1893. Untersuchungen über die Mimicry auf Grundlage eines natürlichen Systems der Papilioniden. Verlag von Erwin Nägele, Stuttgart.
31. Harborne, J. B. 1993. Introduction of ecological biochemistry. Academic Press, London.
32. Hatle, J. D., and J. H. Spring. 1998. Inter-individual variation in sequestration (as measured by energy dispersive spectroscopy) predicts efficacy of defensive secretion in lubber grasshoppers. Chemoecology 8 : 85 90.
33. +-ATPase. J. Chem. Ecol. 22 : 1921 1937.
34. Jeffords, M. R., J. G. Sternburg, and G. P. Waldbauer. 1979. Batesian mimicry: field demonstration of the survival value of pipevine swallowtail and monarch color patterns. Evolution 33 : 275 286.
35. Karlsson, B. 1995. Resource-allocation and mating systems in butterflies. Evolution 49 : 955 961.
36. Malcolm, S. B., and M. P. Zalucki. 1996. Milkweed latex and cardenolide induction may resolve the lethal plant defence paradox. Entomol. Exp. Appl. 80 : 193 196.
37. Malcolm, S. B., B. J. Cockrell, and L. P. Brower. 1989. Cardenolide fingerprint of monarch butterflies reared on common milkweed, Asclepias syriaca L. J. Chem. Ecol. 15 : 819 854.
38. Moranz, R., and L. P. Brower. 1998. Geographic and temporal variation of cardenolide-based chemical defenses of queen butterfly (Danaus gilippus) in northern Florida. J. Chem. Ecol. 24 : 905 932.
39. Müller, F. 1878. Ituna and Thyrdia: a remarkable case of mimicry in butterflies. Proc. Entomol. Soc. Lond. 1879 : 20 29.
40. Müller, C., and U. Wittstock. 2005. Uptake and turn-over of glucosinolates sequestered in the sawfly Athalia rosae. Insect Biochem. Mol. 35 : 1189 1198.
41. Müller, C., B. J. Zwaan, H. de Vos, and P. M. Brakefield. 2003. Chemical defence in a sawfly: genetic components of variation in relevant life-history traits. Heredity 90 : 468 475.
42. Nelson, C. J., J. N. Seiber, and L. P. Brower. 1981. Seasonal and intraplant variation of cardenolide content in the California milkweed, Asclepias eriocarpa, and implications for plant defense. J. Chem. Ecol. 7 : 981 1010.
43. Nice, C. C., and J. A. Fordyce. 2006. How caterpillars avoid overheating: behavioral and phenotypic plasticity of pipevine swallowtail larvae. Oecologia 146 : 541 548.
44. Nishida, R. 2002. Sequestration of defensive substances from plants by Lepidoptera. Annu. Rev. Entomol. 47 : 57 92.
45. Nishida, R., J. D. Weintraub, P. Feeny, and H. Fukami. 1993. Aristolochic acids from Thottea spp. (Aristolochiaceae) and the osmeterial secretions of Thottea feeding troidine swallowtail larvae (Papilionidae). J. Chem. Ecol. 19 : 1587 1594.
46. Ode, P. J. 2006. Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu. Rev. Entomol. 51 : 163 185.
47. Platt, A. P., R. P. Coppinger, and L. P. Brower. 1971. Demonstration of selective advantage of mimetic Limenitis butterflies presented to caged avian predators. Evolution 25 : 692 701.
48. 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.
49. Racheli, T., and L. Pariset. 1992. II genere Battus tassonomia e storia naturale. Fragm. Entomol. (Roma) (Suppl.) 23 : 1 163.
50. Rausher, M. D. 1979. Egg recognition: its advantage to a butterfly. Anim. Behav. 27 : 1034 1040.
51. Rayor, L. S., L. J. Mooney, and J. A. Renwick. 2007. Predatory behavior of Polistes dominulus wasps in response to cardenolides and glucosinolates in Pieris napi caterpillars. J. Chem. Ecol. 33 : 1177 1185.
52. Ritland, D. B. 1994. Variation in palatability of queen butterflies (Danaus gilippus) and implications regarding mimicry. Ecology 75 : 732 746.
53. Rothschild, M., T. Reichstein, J. von Euw, R. Aplin, and R. R. M. Harman. 1970. Toxic lepidoptera. Toxicon 8 : 293 299.
54. Rowell-Rahier, M., and J. M. Pasteels. 1992. Third trophic level influences of plant allelochemics. Pp. 243 277 in G. Rosenthal and M. R. Berenbaum, eds. Herbivores: their interactions with secondary plant metabolites. Academic Press, New York.
55. Sillén-Tullberg, B. 1988. Evolution of gregariousness in aposematic butterfly larvae: a phylogenetic analysis. Evolution 42 : 293 305.
56. Sime, K. 2002. Chemical defence of Battus philenor larvae against attack by the parasitoid Trogus pennator. Ecol. Entomol. 27 : 337 345.
57. Sime, K. R., P. P. Feeny, and M. M. Haribal. 2000. Sequestration of aristolochic acids by the pipevine swallowtail, Battus philenor (L.): evidence and ecological implications. Chemoecology 10 : 169 178.
58. Slater, J. W. 1877. On the food of gaily-coloured caterpillars. Trans. Entomol. Soc. Lond. 1877 : 205 209.
59. Stamp, N. E. 1980. Egg deposition patterns in butterflies: why do some species cluster their eggs rather than deposit them singly Am. Nat. 115 : 367 380.
60. Stamp, N. E. 1986. Physical constraints of defense and response to invertebrate predators by pipevine caterpillars (Battus philenor: Papilionidae). J. Lepid. Soc. 40 : 191 205.
61. Theodoratus, D. H., and M. D. Bowers. 1999. Effects of sequestered iridoid glycosides on prey choice of the prairie wolf spider Lycosa carolinensis. J. Chem. Ecol. 25 : 283 295.
62. Tullberg, B. S., and A. F. Hunter. 1996. Evolution of larval gregariousness in relation to repellent defences and warning coloration in tree-feeding macrolepidoptera: a phylogenetic analysis based on independent contrasts. Biol. J. Linn. Soc. 57 : 253 276.
63. Urzua, A., and H. Priestap. 1985. Aristolochic acids from Battus polydamas. Biochem. Syst. Ecol. 13 : 169 170.
64. Williams, I. S. 1999. Slow-growth, high-mortality - a general hypothesis, or is it Ecol. Entomol. 24 : 490 495.
65. Zalucki, M. P., L. P. Brower, and A. Alonso-M. 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. Ecol. Entomol. 26 : 212 224.