Phenotypic plasticity in sexual communication signal of a noctuid moth

Journal of Evolutionary Biology

Volumn 23, Issue 12, 2010, Pages 2731-2738

  Groot, A T ^a   Classen A ^a   Staudacher, H ^a   Schal, C ^b   Heckel, D G ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Communication interference; Early adult experience; Environmental effects; Experience hypothesis; Heliothis subflexa; Heliothis virescens; Intraspecific variation; Sex pheromone production

Indexed keywords

SEX PHEROMONE;

ADAPTATION; ADULT; GENETIC ANALYSIS; INTRASPECIFIC VARIATION; MOTH; OLFACTORY CUE; PHENOTYPIC PLASTICITY; SEX PHEROMONE; SEXUAL SELECTION; SIGNAL;

ADAPTATION; ANIMAL; ANIMAL COMMUNICATION; ARTICLE; ASSOCIATION; CHEMISTRY; DRUG EFFECT; FEMALE; METABOLISM; MOTH; PHENOTYPE; PHYSIOLOGY; SEXUAL BEHAVIOR; STIMULATION;

ADAPTATION, PHYSIOLOGICAL; ANIMAL COMMUNICATION; ANIMALS; CUES; FEMALE; MOTHS; PHENOTYPE; SEX ATTRACTANTS; SEXUAL BEHAVIOR, ANIMAL; STIMULATION, CHEMICAL;

HELIOTHIS SUBFLEXA; HELIOTHIS VIRESCENS; LEPIDOPTERA; NOCTUIDAE;

EID: 78449247477     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2010.02124.x     Document Type: Article

References (65)

1. Agrawal, A.A. 2001. Ecology - Phenotypic plasticity in the interactions and evolution of species. Science 294: 321-326.
2. Aitchison, J. 1986. The Statistical Analysis of Compositional Data. The Blackburn Press, New Jersey.
3. Anderson, P., Sadek, M.M. & Hansson, B.S. 2003. Pre-exposure modulates attraction to sex pheromone in a moth. Chem. Senses 28: 285-291.
4. Andersson, J., Borg-Karlson, A.K., Vongvanich, N. & Wiklund, C. 2007. Male sex pheromone release and female mate choice in a butterfly. J. Exp. Biol. 210: 964-970.
5. Bailey, N.W. & Zuk, M. 2008. Acoustic experience shapes female mate choice in field crickets. Proc. R. Soc. Lond. B Biol. Sci. 275: 2645-2650.
6. Bashir, T., Hodges, R.J., Birkinshaw, L.A., Hall, D.R. & Farman, D.I. 2003. Phenotypic plasticity of Rhyzopertha dominica pheromone signaling: The effects of different hosts and presence of conspecific females on male produced aggregation pheromone. J. Chem. Ecol. 29: 945-959.
7. Blows, M.W. & Higgie, M. 2002. Evolutionary experiments on mate recognition in the Drosophila serrata species complex. Genetica 116: 239-250.
8. Brooks, R., Hunt, J., Blows, M.W., Smith, M.J., Bussiere, L.F. & Jennions, M.D. 2005. Experimental evidence for multivariate stabilizing sexual selection. Evolution 59: 871-880.
9. Butlin, R. & Trickett, A.J. 1997. Can population genetic simulations help to interpret pheromone evolution?. In: Insect Pheromone Research: New Directions (R.T. Cardé & A.K. Minks, eds), pp. 548-562. Chapman and Hall, New York.
10. Cossé, A.A., Campbell, M.G., Glover, T.J., Linn, C.E., Todd, J.L., Baker, T.C. & Roelofs, W.L. 1995. Pheromone behavioral responses in unusual male European corn borer hybrid progeny not correlated to electrophysiological phenotypes of their pheromone-specific antennal neurons. Experientia 51: 809-816.
11. Coyne, J.A. & Orr, H.A. 1997. "Patterns of speciation in Drosophila" revisited. Evolution 51: 295-303.
12. Coyne, J.A., Barton, N.H. & Turelli, M. 1997. Perspective: a critique of Sewall Wright's shifting balance theory of evolution. Evolution 51: 643-671.
13. Crispo, E. 2008. Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow. J. Evol. Biol. 21: 1460-1469.
14. Denotter, C.J., Schuil, H.A. & Sandervanoosten, A. 1978. Reception of host plant odors and female sex pheromone in Adoxophyes orana (Lepidoptera, Tortricidae) - Electrophysiology and Morphology. Entomol. Exp. Appl. 24: 570-578.
15. Foster, S. 2009. Sugar feeding via trehalose haemolymph concentration affects sex pheromone production in mated Heliothis virescens moths. J. Exp. Biol. 212: 2789-2794.
16. Gries, G., Schaefer, P.W., Gries, R., Liska, J. & Gotoh, T. 2001. Reproductive character displacement in Lymantria monacha from northern Japan? J. Chem. Ecol. 27: 1163-1176.
17. Groning, J. & Hochkirch, A. 2008. Reproductive interference between animal species. Q. Rev. Biol. 83: 257-282.
18. Groot, A., Gemeno, C., Brownie, C., Gould, F. & Schal, C. 2005. Male and female antennal responses in Heliothis virescens and H. subflexa to conspecific and heterospecific sex pheromone compounds. Environ. Entomol. 34: 256-263.
19. Groot, A.T., Horovitz, J.L., Hamilton, J., Santangelo, R.G., Schal, C. & Gould, F. 2006. Experimental evidence for interspecific directional selection on moth pheromone communication. Proc. Natl Acad. Sci. USA 103: 5858-5863.
20. Groot, A.T., Santangelo, R.G., Ricci, E., Brownie, C. & Gould, F. 2007. Differential attraction of Heliothis subflexa males to synthetic pheromone lures in eastern US and western Mexico. J. Chem. Ecol. 33: 353-368.
21. Groot, A.T., Inglis, O., Bowdrigde, S., Santangelo, R.G., Blanco, C., Lopez, J.D., Teran Vargas, A., Gould, F. & Schal, C. 2009. Geographic and temporal variation in moth chemical communication. Evolution 63: 1987-2003.
22. Haynes, K.F., Gemeno, C., Yeargan, K.V., Millar, J.G. & Johnson, K.M. 2002. Aggressive chemical mimicry of moth pheromones by a bolas spider: how does this specialist predator attract more than one species of pray? Chemoecology 12: 99-105.
23. Heath, R.R., Mitchell, E.R. & Tovar, J.C. 1990. Effect of release rate and ratio of (Z)-11-Hexadecen-1-ol from synthetic pheromone blends on trap capture of Heliothis subflexa (Lepidoptera, Noctuidae). J. Chem. Ecol. 16: 1259-1268.
24. Heath, R.R., McLaughlin, J.R., Proshold, F. & Teal, P.E.A. 1991. Periodicity of female sex pheromone titer and release in Heliothis subflexa and H. virescens (Lepidoptera, Noctuidae). Ann. Entomol. Soc. Am. 84: 182-189.
25. Higgie, M., Chenoweth, S. & Blows, M.W. 2000. Natural selection and the reinforcement of mate recognition. Science 290: 519-521.
26. Hillier, N.K., Kleineidam, C. & Vickers, N.J. 2006. Physiology and glomerular projections of olfactory receptor neurons on the antenna of female Heliothis virescens (Lepidoptera Noctuidae) responsive to behaviorally relevant odors. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 192: 199-219.
27. Hobel, G. & Gerhardt, H.C. 2003. Reproductive character displacement in the acoustic communication system of green tree frogs (Hyla cinerea). Evolution 57: 894-904.
28. Howard, D.J. & Gregory, P.G. 1993. Post-Insemination Signaling Systems and Reinforcement. Philos. Trans. R. Soc. Lond. B Biol. Sci. 340: 231-236.
29. Jurenka, R. 2004. Insect pheromone biosynthesis. In: Chemistry of Pheromones and Other Semiochemicals I, Vol. 239 (S. Schulz, T. Ando & S. Inomata, eds), pp. 97-131. Springer, Berlin.
30. Kent, C., Azanchi, R., Smith, B., Formosa, A. & Levine, J.D. 2008. Social context influences chemical communication in D. melanogaster males. Curr. Biol. 18: 1384-1389.
31. Klun, J.A., Plimmer, J.R. & Bierlleonhardt, B.A. 1979. Trace Chemicals - Essence of sexual communication systems in Heliothis species. Science 204: 1328-1330.
32. Klun, J.A., Leonhardt, B.A., Lopez, J.D. & Lachance, L.E. 1982. Female Heliothis subflexa (Lepidoptera, Noctuidae) sex pheromone - chemistry and congeneric comparisons. Environ. Entomol. 11: 1084-1090.
33. Krupp, J.J., Kent, C., Billeter, J.C., Azanchi, R., So, A.K.C., Schonfeld, J.A., Smith, B.P., Lucas, C. & Levine, J.D. 2008. Social experience modifies pheromone expression and mating behavior in male Drosophila melanogaster. Curr. Biol. 18: 1373-1383.
34. Laster, M.L. 1972. Interspecific hybridization of Heliothis virescens and Heliothis subflexa. Environ. Entomol. 1: 682-687.
35. Linn, C.E., Young, M.S., Gendle, M., Glover, T.J. & Roelofs, W.L. 1997. Sex pheromone blend discrimination in two races and hybrids of the European corn borer moth, Ostrinia nubilalis. Physiol. Entomol. 22: 212-223.
36. Löfstedt, C. 1993. Moth pheromone genetics and evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 340: 167-177.
37. Löfstedt, C., Lofqvist, J., Lanne, B.S., Vanderpers, J.N.C. & Hansson, B.S. 1986. Pheromone dialects in European turnip moths Agrotis segetum. Oikos 46: 250-257.
38. McElfresh, J.S. & Millar, J.G. 1999. Geographic variation in sex pheromone blend of Hemileuca electra from Southern California. J. Chem. Ecol. 25: 2505-2525.
39. McElfresh, J.S. & Millar, J.G. 2001. Geographic variation in the pheromone system of the saturniid moth Hemileuca eglanterina. Ecology 82: 3505-3518.
40. Noor, M.A. 1995. Speciation driven by natural selection in Drosophila. Nature 375: 674-675.
41. Petfield, D., Chenoweth, S.F., Rundle, H.D. & Blows, M.W. 2005. Genetic variance in female condition predicts indirect genetic variance in male sexual display traits. Proc. Natl. Acad. Sci. USA 102: 6045-6050.
42. Pfennig, K.S. & Pfennig, D.W. 2009. Character displacement: ecological and reproductive responses to a common evolutionary problem. Q. Rev. Biol. 84: 253-276.
43. Pigliucci, M. 2001. Syntheses in ecology and evolution. In: Phenotypic plasticity: Beyond nature and nuture, pp. i-328. Johns Hopkins University Press, Baltimore.
44. Price, T.D., Qvarnstrom, A. & Irwin, D.E. 2003. The role of phenotypic plasticity in driving genetic evolution. Proc. R. Soc. Lond. B Biol. Sci. 270: 1433-1440.
45. Rafaeli, A. 2005. Mechanisms involved in the control of pheromone production in female moths: recent developments. Entomol. Exp. Appl. 115: 7-15.
46. Raina, A.K. 1988. Selected factors influencing neuro-hormonal regulation of sex pheromone production in Heliothis species. J. Chem. Ecol. 14: 2063-2069.
47. Raina, A.K. 2003. Pheromone production in corn earworm: effect of temperature and humidity. Southwest. Entomol. 28: 115-120.
48. Ramaswamy, S.B., Randle, S.A. & Ma, W.K. 1985. Field evaluation of the sex pheromone components of Heliothis virescens (Lepidoptera, Noctuidae) in cone traps. Environ. Entomol. 14: 293-296.
49. Ritchie, M.G. 1996. The shape of female mating preferences. Proc. Natl. Acad. Sci. USA 93: 14628-14631.
50. Ritchie, M.G. 2007. Sexual selection and speciation. Annu. Rev. Ecol. Evol. Syst. 38: 79-102.
51. Roelofs, W.L., Hill, A.S., Cardé, R.T. & Baker, T.C. 1974. 2 Sex pheromone components of Tobacco budworm moth, Heliothis virescens. Life Sci. 14: 1555-1562.
52. Schneider, D., Schulz, S., Priesner, E., Ziesmann, J. & Francke, W. 1998. Autodetection and chemistry of female and male pheromone in both sexes of the tiger moth Panaxia quadripunctaria. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 182: 153-161.
53. Teal, P.E.A. & Tumlinson, J.H. 1986. Terminal steps in pheromone biosynthesis by Heliothis virescens and Heliothis zea. J. Chem. Ecol. 12: 353-366.
54. Teal, P.E.A., Heath, R.R., Tumlinson, J.H. & McLaughlin, J.R. 1981. Identification of a sex pheromone of Heliothis subflexa (Gn) (Lepidoptera, Noctuidae) and field trapping studies using different blends of components. J. Chem. Ecol. 7: 1011-1022.
55. Teal, P.E.A., Tumlinson, J.H. & Heath, R.R. 1986. Chemical and behavioral analyses of volatile sex pheromone components released by calling Heliothis virescens (F) females (Lepidoptera, Noctuidae). J. Chem. Ecol. 12: 107-126.
56. Tóth, M., Löfstedt, C., Blair, B.W., Cabello, T., Farag, A., Hansson, B.S., Kovalev, B.G., Maini, S., Nesterov, E.A., Pajor, I., Sazonov, A.P., Shamshev, I.V., Subchev, M. & Szöcs, G. 1992. Attraction of male Turnip moths Agrotis segetum (Lepidoptera: Noctuidae) to sex pheromone components and their mixtures at 11 sites in Europe, Asia, and Africa. J. Chem. Ecol. 18: 1337-1347.
57. Tumlinson, J.H., Hendricks, D.E., Mitchell, E.R., Doolittle, R.E. & Brennan, M.M. 1975. Isolation, identification and synthesis of the sex pheromone of the Tobacco budworm. J. Chem. Ecol. 1: 203-214.
58. Vetter, R.S. & Baker, T.C. 1983. Behavioral responses of male Heliothis virescens in a sustained flight tunnel to combinations of 7 compounds identified from female sex pheromone glands. J. Chem. Ecol. 9: 747-759.
59. Via, S., Gomulkiewicz, R., Dejong, G., Scheiner, S.M., Schlichting, C.D. & Vantienderen, P.H. 1995. Adaptive phenotypic plasticity - Consensus and controversy. Trends Ecol. Evol. 10: 212-217.
60. Vickers, N.J. 2002. Defining a synthetic pheromone blend attractive to male Heliothis subflexa under wind tunnel conditions. J. Chem. Ecol. 28: 1255-1267.
61. Vickers, N.J. & Baker, T.C. 1997a. Chemical communication in heliothine moths .7. Correlation between diminished responses to point source plumes and single filaments similarly tainted with a behavioral antagonist. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 180: 523-536.
62. Vickers, N.J. & Baker, T.C. 1997b. Flight of Heliothis virescens males in the field in response to sex pheromone. Physiol. Entomol. 22: 277-285.
63. Wang, H.L., Ming, Q.L., Zhao, C.H. & Wang, C.Z. 2008. Genetic basis of sex pheromone blend difference between Helicoverpa armigera (Hubner) and Helicoverpa assulta (Guenee) (Lepidoptera Noctuidae). J. Insect Physiol. 54: 813-817.
64. Widmayer, P., Heifetz, Y. & Breer, H. 2009. Expression of a pheromone receptor in ovipositor sensilla of the female moth (Heliothis virescens). Insect Mol. Biol. 18: 541-547.
65. Zhu, J.W., Chastain, B.B., Spohn, B.G. & Haynes, K.F. 1997. Assortative mating in two pheromone strains of the cabbage looper moth, Trichoplusia ni. J. Insect Behav. 10: 805-817.