Host plants and immatures as mate-searching cues in Heliconius butterflies

Animal Behaviour

Volumn 80, Issue 2, 2010, Pages 231-239

  Estrada, Catalina ^a   Gilbert, Lawrence E ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Butterfly; Heliconius; Host fidelity; Host plant; Male mate searching; Plant volatile; Pupal mating; Sexual behaviour

Indexed keywords

BUTTERFLY; HOST PLANT; HOST-PARASITE INTERACTION; LARVA; MATE GUARDING; PHYTOCHEMISTRY; PLANT DEFENSE; PUPA; REPRODUCTIVE STRATEGY;

HELICONIUS; HELICONIUS CHARITHONIA; HEXAPODA; PAPILIONOIDEA;

EID: 77954759251     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2010.04.023     Document Type: Article

References (79)

1. Andersson S., Dobson H.E.M. Behavioral foraging responses by the butterfly Heliconius melpomene to Lantana camara floral scent. Journal of Chemical Ecology 2003, 29:2303-2318.
2. Beccaloni G.W., Viloria A.L., Hall S.K., Robinson G.S. Catalogue of the Hostplants of the Neotropical Butterflies 2008, Sociedad Entomológica Aragonesa, Zaragoza.
3. Bell W.J. Searching behavior patterns in insects. Annual Review of Entomology 1990, 35:447-467.
4. Beltrán M., Jiggins C.D., Brower A.V.Z., Bermingham E., Mallet J.L.B. Do pollen feeding, pupal mating and larval gregariousness have a single origin in Heliconius butterflies? Inferences from multilocus DNA sequence data. Biological Journal of the Linnean Society 2007, 92:221-239.
5. Benson W.W. Resource partitioning in passion vine butterflies. Evolution 1978, 32:493-518.
6. Benson W.W., Brown K.S., Gilbert L.E. Coevolution of plants and herbivores: passion flower butterflies. Evolution 1975, 29:659-680.
7. Borch H., Schmid F. On Ornithoptera priamus caelestis Rothschild, demophanes Fruhstorfer and boisduvali Montrouzier (Papilionidae). Journal of the Lepidopterist's Society 1973, 27:196-205.
8. Braby M.F., Trueman J.W.H. Evolution of larval host plant associations and adaptive radiation in pierid butterflies. Journal of Evolutionary Biology 2006, 19:1677-1690.
9. Brown K.S. The biology of Heliconius and related genera. Annual Review of Entomology 1981, 26:427-457.
10. Brown K.S.J., Benson W.W. Evolution in modern Amazonian non-forest islands: Heliconius hermathena. Biotropica 1977, 9:95-117.
11. Cocroft R.B., Rodríguez R.L., Hunt R.E. Host shifts, the evolution of communication, and speciation in the Enchenopa binotata species complex of treehoppers. The Evolutionary Biology of Herbivorous Insects: Specialization, Speciation and Radiation 2008, 88-100. University of California Press, Berkeley. K.J. Tilmon (Ed.).
12. Cunningham J., Moore C., Zalucki M., Cribb B. Insect odour perception: recognition of odour components by flower foraging moths. Proceedings of the Royal Society B 2006, 273:2035-2040.
13. Deinert E.I. Sexual selection in Heliconius hewitsoni, a pupal mating butterfly. Ecology and Evolution Taking Flight: Butterflies as Model Study Systems 2003, 91-108. University of Chicago Press, Chicago. C.L. Boggs, P.R. Ehrlich, W.B. Watt (Eds.).
14. Deinert E.I., Longino J.T., Gilbert L.E. Mate competition in butterflies. Nature 1994, 370:23-24.
15. Deng J., Wei H., Huang Y., Du J. Enhancement of attraction to sex pheromones of Spodoptera exigua by volatile compounds produced by host plants. Journal of Chemical Ecology 2004, 30:2037-2045.
16. Dennis R.L.H., Shreeve T.G. Hostplant-habitat structure and the evolution of butterfly mate-locating behavior. Zoological Journal of the Linnean Society 1988, 94:301-318.
17. Drès M., Mallet J.L.B. Host races in plant-feeding insects and their importance in sympatric speciation. Philosophical Transactions of the Royal Society of London, Series B 2002, 357:471-492.
18. Dukas R. Evolutionary biology of insect learning. Annual Review of Entomology 2008, 53:145-160.
19. Ehrlich P.R., Gilbert L.E. Population structure and dynamics of the tropical butterfly Heliconius ethilla. Biotropica 1973, 5:69-82.
20. Ehrlich P.R., Raven P.H. Butterflies and plants: a study in coevolution. Evolution 1964, 18:586-608.
21. Elgar M.A., Pierce N.E. Mating success and fecundity in an ant-tended lycaenid butterfly. Reproductive Success: Studies of Selection and Adaptation in Contrasting Breeding Systems 1988, 59-75. University of Chicago Press, Chicago. T.H. Clutton-Block (Ed.).
22. Emelianov I., Drès M., Baltensweiler W., Mallet J.L.B. Host-induced assortative mating in host races of the larch budmoth. Evolution 2001, 55:2002-2010.
23. Estrada, C. 2009. Sexual behavior, intraspecific signaling and the evolution of mimicry among closely related species. Ph.D. thesis, University of Texas at Austin.
24. Estrada C., Jiggins C.D. Patterns of pollen feeding and habitat preference among Heliconius species. Ecological Entomology 2002, 27:448-456.
25. Estrada C., Yildizhan S., Schulz S., Gilbert L.E. Sex-specific chemical cues from immatures facilitate the evolution of mate guarding in Heliconius butterflies. Proceedings of the Royal Society B 2010, 277:407-413.
26. Feder J.L. The apple maggot fly, Ragoletis pomonella: flies in the face of conventional wisdom about speciation?. Endless Forms: Species and Speciation 1998, 130-144. Oxford University Press, New York. D.J. Howard, S.H. Berlocher (Eds.).
27. Feder J.L., Opp S.B., Wlazlo B., Reynolds K., Spisak S. Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly. Proceedings of the National Academy of Sciences, U.S.A. 1994, 91:7990-7994.
28. Forister M.L. Influence of host plant phenology on Mitoura nelsoni (Lepidoptera: Lycaenidae). Annals of the Entomological Society of America 2005, 98:295-301.
29. Funk D.J. Isolating a role for natural selection in speciation: host adaptation and sexual isolation in Neochlamisus bebbianae leaf beetles. Evolution 1998, 52:1744-1759.
30. Geervliet J.B.F., Posthumus M.A., Vet L.E.M., Dicke M. Comparative analysis of headspace volatiles from different caterpillar-infested or uninfested food plants of Pieris species. Journal of Chemical Ecology 1997, 23:2935-2954.
31. Gilbert L.E. Postmating female odor in Heliconius butterflies: a male-contributed antiaphrodisiac?. Science 1976, 193:419-420.
32. Gilbert L.E. Development of theory in the analysis of insect-plant interaction. Analysis of Ecological Systems 1978, 117-153. Ohio State University Press, Columbus. D.J. Horn, G.R. Stairs, R.D. Mitchell (Eds.).
33. Gilbert L.E. Biodiversity of a Central American Heliconius community: patterns, process, and problems. Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions 1991, 403-427. J. Wiley, New York. P.W. Price, T.M. Lewinsohn, G.W. Fernandes, W.W. Benson (Eds.).
34. Gilbert L.E., Singer M.C. Butterfly ecology. Annual Review of Ecology and Systematics 1975, 6:365-397.
35. Ginzel M.D., Hanks L.M. Role of host plant volatiles in mate location for three species of longhorned beetles. Journal of Chemical Ecology 2005, 31:213-217.
36. Gompert Z., Fordyce J.A., Forister M.L., Shapiro A.M., Nice C.C. Homoploid hybrid speciation in an extreme habitat. Science 2006, 314:1923-1925.
37. Jiggins C.D., Naisbit R.E., Coe R.L., Mallet J.L.B. Reproductive isolation caused by colour pattern mimicry. Nature 2001, 411:302-305.
38. Jiggins C.D., Estrada C., Rodrigues A. Mimicry and the evolution of premating isolation in Heliconius melpomene Linnaeus. Journal of Evolutionary Biology 2004, 17:680-691.
39. Landolt P., Phillips T.W. Host plant influences on sex pheromone behavior of phytophagous insects. Annual Review of Entomology 1997, 42:371-391.
40. Linn C., Feder J.L., Nojima S., Dambroski H.R., Berlocher S.H., Roelofs W. Fruit odor discrimination and sympatric host race formation in Rhagoletis. Proceedings of the National Academy of Sciences, U.S.A. 2003, 100:11490-11493.
41. Mallet J.L.B., Gilbert L.E. Why are there so many mimicry rings? Correlation between habitat, behavior and mimicry in Heliconius butterflies. Biological Journal of the Linnean Society 1995, 55:159-180.
42. Mendoza-Cuenca L., Macías-Ordóñez R. Female synchrony may drive disruptive sexual selection on male mating phenotypes in a Heliconius butterfly. Behavioral Ecology 2010, 21:144-152.
43. Mullen S.P. Wing pattern evolution and the origins of mimicry among North American admiral butterflies (Nymphalidae: Limenitis). Molecular Phylogenetics and Evolution 2006, 39:747-758.
44. Nice C.C., Shapiro A.M. Population genetic evidence of restricted gene flow between host races in the butterfly genus Mitoura (Lepidoptera: Lycaenidae). Annals of the Entomological Society of America 2001, 94:257-267.
45. Nice C.C., Fordyce J.A., Shapiro A.M., Ffrench-Constant R. Lack of evidence for reproductive isolation among ecologically specialised lycaenid butterflies. Ecological Entomology 2002, 27:702-712.
46. Papaj D.R., Newsom G.M. A within species warning function for an aposematic signal. Proceedings of the Royal Society B 2005, 272:2519-2523.
47. Papaj D.R., Prokopy R.J. Ecological and evolutionary aspects of learning in phytophagous insects. Annual Review of Entomology 1989, 34:315-350.
48. Papke R.S., Kemp D.J., Rutowski R.L. Multimodal signalling: structural ultraviolet reflectance predicts male mating success better than pheromones in the butterfly Colias eurytheme L. (Pieridae). Animal Behaviour 2007, 73:47-54.
49. Paré P.W., Tumlinson J.H. Plant volatiles as a defense against insect herbivores. Plant Physiology 1999, 121:325-332.
50. Peña C., Wahlberg N. Prehistorical climate change increased diversification of a group of butterflies. Biology Letters 2008, 4:274-278.
51. Pliske T.E., Edgar J.A., Culvenor C.C.J. The chemical basis of attraction of ithomiine butterflies to plants containing pyrrolizidine alkaloids. Journal of Chemical Ecology 1976, 2:255-262.
52. Pratt G.F. Evolution of Euphilotes (Lepidoptera: Lycaenidae) by seasonal and host shift. Biological Journal of the Linnean Society 1994, 51:387-416.
53. Prokopy R.J., Owens E.D. Visual detection of plants by herbivorous insects. Annual Review of Entomology 1983, 28:337-364.
54. Rausher M.D. Search image for leaf shape in a butterfly. Science 1978, 200:1071-1073.
55. Reddy G.V.P., Guerrero A. Interactions of insect pheromones and plant semiochemicals. Trends in Plant Science 2004, 9:253-261.
56. Ruther J., Reinecke A., Thiemann K., Tolasch T., Francke W., Hilker M. Mate finding in the forest cockchafer, Melolontha hippocastani, mediated by volatiles from plants and females. Physiological Entomology 2000, 25:172.
57. Rutowski R.L. The evolution of male mate-locating behavior in butterflies. American Naturalist 1991, 138:1121-1139.
58. Schluter D. Ecology and the origin of species. Trends in Ecology & Evolution 2001, 16:372-380.
59. Scott J.A. Mate-locating behavior of western North American butterflies. Journal of Research in Lepidoptera 1975, 14:1-40.
60. Smiley J.T. Plant chemistry and the evolution of host specificity: new evidence from Heliconius and Passiflora. Science 1978, 201:745-747.
61. Sokal R.R., Rohlf J. Biometry 1969, W.H. Freeman, San Francisco.
62. Soroker V., Talebaev S., Harari A.R., Wesley S.D. The role of chemical cues in host and mate location in the pear psylla Cacopsylla bidens (Homoptera: Psyllidae). Journal of Insect Behavior 2004, 17:613-626.
63. Summers K., Symula R., Clough M., Cronin T. Visual mate choice in poison frogs. Proceedings of the Royal Society B 1999, 266:2141-2145.
64. Thomas Y., Bethenod M., Pelozuelo L., Frerot B., Bourguet D. Genetic isolation between two sympatric host-plant races of the European corn borer, Ostrinia nubilalis Hubner. I. Sex pheromone, moth emergence timing, and parasitism. Evolution 2003, 57:261-273.
65. Thornhill R., Alcock J. The Evolution of Insect Mating Systems 1983, Harvard University Press, Cambridge, Massachusetts.
66. Tooker J.F., Koening W.A., Hanks L.M. Altered host plant volatiles are proxies for sex pheromones in the gall wasp Antistrophus rufus. Proceedings of the National Academy of Sciences, U.S.A. 2002, 99:15486-15491.
67. Turlings T.C., Loughrin J.H., McCall P.J., Röse U.S., Lewis W.J., Tumlinson J.H. How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proceedings of the National Academy of Sciences, U.S.A. 1995, 92:4169-4174.
68. Turner J.R.G. Experiments on the demography of tropical butterflies. II. Longevity and home-range behaviour in Heliconius erato. Biotropica 1971, 3:21-31.
69. Via S. Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 1999, 53:1446-1457.
70. Visser J.H., Straten S., Maarse H. Isolation and identification of volatiles in the foliage of potato, Solanum tuberosum, a host plant of the Colorado beetle, Leptinotarsa decemlineata. Journal of Chemical Ecology 1979, 5:13-25.
71. Weingartner E., Wahlberg N., Nylin S. Dynamics of host plant use and species diversity in Polygonia butterflies (Nymphalidae). Journal of Evolutionary Biology 2006, 19:483-491.
72. Weiss M.R. Innate colour preferences and flexible colour learning in the pipevine swallowtail. Animal Behaviour 1997, 53:1043-1052.
73. Weiss M., Papaj D.R. Colour learning in two behavioural contexts: how much can a butterfly keep in mind?. Animal Behaviour 2003, 65:425-434.
74. Weller S.J., Jacobson N.L., Conner W.E. The evolution of chemical defences and mating systems in tiger moths (Lepidoptera: Arctiidae). Biological Journal of the Linnean Society 1999, 68:557-578.
75. Wheat C.W., Vogel H., Wittstock U., Braby M.F., Underwood D., Mitchell-Olds T. The genetic basis of a plant-insect coevolutionary key innovation. Proceedings of the National Academy of Sciences, U.S.A. 2007, 104:20427-20431.
76. Wiernasz D. Male choice on the basis of female melanin pattern in Pieris butterflies. Animal Behaviour 1995, 49:45-51.
77. Wiklund C. Sexual selection and the evolution of butterfly mating systems. Butterflies: Ecology and Evolution Taking Flight 2003, 67-90. University of Chicago Press, Chicago. C.L. Boggs, W.B. Watt, P.R. Ehrlich (Eds.).
78. Yang Z., Bengtsson M., Witzgall P. Host plant volatiles synergize response to sex pheromone in codling moth, Cydia pomonella. Journal of Chemical Ecology 2004, 30:619-629.
79. Yockteng R., Nadot S. Phylogenetic relationships among Passiflora species based on the glutamine synthetase nuclear gene expressed in chloroplast (ncpGS). Molecular Phylogenetics and Evolution 2004, 31:379-396.