Geographic and temporal variation in moth chemical communication

Evolution

Volumn 63, Issue 8, 2009, Pages 1987-2003

  Groot, Astrid T ^a,e   Inglis, Olive ^a   Bowdridge, Scott ^a,f   Santangelo, Richard G ^a   Blanco, Carlos ^b   López Jr , Juan D ^c   Vargas, Antonio Terán ^d   Gould, Fred ^a   Schal, Coby ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c AGRICULTURAL RESEARCH SERVICE   (United States)

^d Campo Experimental sur de Tamaulipas   (Mexico)

^e MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^f VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Experience; Female sex pheromone; Heliothis subflexa; Heliothis virescens; Male response; Phenotypic plasticity; Selection

Indexed keywords

SEX PHEROMONE;

CHEMICAL ENVIRONMENTAL CONDITIONS; CROP PEST; FEMALE BEHAVIOR; GEOGRAPHICAL REGION; GEOGRAPHICAL VARIATION; INTRASPECIFIC COMPETITION; MALE BEHAVIOR; MOTH; POPULATION GENETICS; SEX PHEROMONE; SEXUAL SELECTION; SPECIES DIVERSITY; TEMPORAL VARIATION;

ANIMAL; ANIMAL COMMUNICATION; ARTICLE; CHEMISTRY; FEMALE; MALE; METABOLISM; MEXICO; MOTH; UNITED STATES;

ANIMAL COMMUNICATION; ANIMALS; FEMALE; MALE; MEXICO; MOTHS; SEX ATTRACTANTS; UNITED STATES;

HELIOTHIS SUBFLEXA; HELIOTHIS VIRESCENS; LEPIDOPTERA; NOCTUIDAE;

EID: 68149115916     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2009.00702.x     Document Type: Article

References (127)

1. Anderson, P., M. M. Sadek, and B. S. Hansson. 2003. Pre-exposure modulates attraction to sex pheromone in a moth. Chem. Senses 28 : 285 291.
2. Andersson, P., B. S. Hansson, U. Nilsson, Q. Han, M. Sjöholm, N. Skals, and S. Anton. 2007. Increased behavioral and neuronal sensitivity to sex pheromone after brief odor experience in a moth. Chem. Senses 32 : 483 491.
3. Barron, A.B. 2001. The life and death of Hopkins' host-selection principle. J. Insect Behav. 14 : 725 737.
4. Bateman, M. 2006. Impact of plant suitability, biogeography, and ecological factors on associations between the specialist Herbivore Heliothis subflexa G. (Lepidoptera: Noctuidae) and the species in its host genus, Physalis L. (Solanaceae), in West-Central Mexico. Ph.D. diss. N.C. State Univ., Raleigh, NC.
5. Bautista, M. N. 2006. Insectos plaga, una guía ilustrada para su identificación. Colegio de postgraduados, Texcoco, Estado de México, Mexico.
6. Blackiston, D. J., E. S. Casey, and M. R. Weiss. 2008. Retention of memory through metamorphosis: can a moth remember what it learned as a caterpillar? PLoS ONE 3 : 1 7.
7. Blanco, C. A., A. P. Teran-Vargas, J. D. Lopez, J. V. Kauffman, and X. K. Wei. 2007. Densities of Heliothis virescens and Helicoverpa zea (Lepidoptera: Noctuidae) in three plant hosts. Fl. Entomol. 90 : 742 750.
8. Brodin, A., and F. Haas. 2006. Speciation by perception. Anim. Behav. 72 : 139 146.
9. Bürger, R., K. A. Schneider, and M. Willensdorfer. 2006. The conditions for speciation through intraspecific competition. Evolution 60 : 2185 2206.
10. Butlin, R. 1995. Genetic variation in mating signals and responses. Pp. 327 366 in D. M. Lambert and H. G. Spencer, eds. Speciation and the recognition concept: theory and application. Johns Hopkins Univ. Press, Baltimore, MD.
11. Butlin, R., and A. J. Trickett. 1997. Can population genetic simulations help to interpret pheromone evolution? Pp. 548 562 in R. T. Cardé and A. K. Minks, eds. Insect pheromone research: new directions. Chapman and Hall, New York.
12. Cardé, R. T. and T. C. Baker. 1984. Sexual communication with pheromones. Pp. 355 383 in W. J. Bell and R. T. Cardé, eds. Chemical ecology of insects. Chapman and Hall, London, U.K.
13. Cardé, R. T., A. Comeau, T. C. Baker, and W. L. Roelofs. 1975. Moth mating periodicity: temperature regulates the circadian gate. Experientia 31 : 46 48.
14. Cardé, R. T., A. M. Cardé, A. S. Hill, and W. L. Roelofs. 1977. Sex pheromone specificity as a reproductive isolating mechanism among the sibling species Archips argyrospilus and A. mortuanus and other sympatric torticine moths (Lepidoptera: Tortricidae). J. Chem. Ecol. 3 : 71 84.
15. Chapin, J. B., D. R. Ganaway, B. R. Leonard, S. Micinsky, E. Burrise, and J. B. Graves. 1997. Species composition of Heliothinae captured in cone traps baited with synthetic bollworm or tobacco budworm pheromones. Southwestern Entomol. 22 : 223 231.
16. Clayton, N.S. 1990. Assortative mating in zebra finch subspecies, Taeniopygia guttata guttata and T. g. castanotis. Phil. Trans R. Soc. Lond. B. 330 : 351 370.
17. Conner, W. E., T. Eisner, R. K. Van Der Meer, A. Guerrero, D. Ghiringelli, and J. Meinwald. 1980. Sex attractant of an arctiid moth (Utetheisa ornatrix): a pulsed chemical signal. Behav. Ecol. Sociobiol. 7 : 55 63.
18. Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer, Sunderland, MA.
19. Dieckmann, U., and M. Doebeli. 1999. On the origin of species by sympatric speciation. Nature 400 : 354 357.
20. Dumont, S. and J. N. McNeil. 1992. Responsiveness of Pseudaletia unipuncta (Lepidoptera: Noctuidae) males, maintained as adults under different temperature and photoperiodic conditions, to female sex pheromone. J. Chem. Ecol. 18 : 1797 1807.
21. Eizaguirra, M., A. Sans, C. López, and R. Albajes. 2002. Effects of mating disruption against the Mediterranean corn borer, Sesamia nonagrioides, on the European corn borer, Ostrinia nubilalis. IOBC/WPRS Bull. 25 : 59 68.
22. Eizaguirra, M., R. Albajes, C. López, A. Sans, and C. Gemeno. 2007. Inhibition of pheromone response in Sesamia nonagrioides by the pheromone of the sympatric corn borer, Ostrinia nubilalis. Pest Manag. Sci. 63 : 608 614.
23. Endler, J. A. 1995. Multiple-trait coevolution and environmental gradients in guppies. Trends Ecol. Evol. 10 : 22 29.
24. Fadamiro, H. Y., and T. C. Baker. 1997. Helicoverpa zea males (Lepidoptera: Noctuidae) respond to the intermittent fine structure of their sex pheromone plume and an antagonist in a flight tunnel. Physiol. Entomol. 22 : 316 324.
25. Gemeno, C., A. Sans, C. López, R. Albajes, and M. Eizaguirre. 2006. Pheromone antagonism in the European corn borer moth Ostrinia nubilalis. J. Chem. Ecol. 32 : 1071 1084.
26. Gerhard, H. C. 1991. Female mate choice in treefrogs: static and dynamic acoustic criteria. Anim. Behav. 42 : 615 635.
27. Glover, T. J., J. J. Knodel, P. S. Robbins, C. J. Eckenrode, and W. L. Roelofs. 1991. Gene flow among three races of European corn borers (Lepidoptera, Pyralidae) in New York State. Environ. Entomol. 20 : 1356 1362.
28. Grant, P. R., and B. R. Grant. 2002. Unpredictable evolution in a 30-year study of Darwin's finches. Science 296 : 707 711.
29. Gray, D. A., and W. H. Cade. 1999. Quantitative genetics of sexual selection in the field cricket, Gryllus integer. Evolution 53 : 848 854.
30. Gries, G., P. W. Schaefer, R. Gries, J. Liska, and T. Gotoh. 2001. Reproductive character displacement in Lymantria monacha from Northern Japan? J. Chem. Ecol. 27 : 1163 1176.
31. Groot, A. T., Y. Fan, C. Brownie, R. A. Jurenka, F. Gould, and C. Schal. 2005a. Effect of PBAN on pheromone production in mated Heliothis virescens and Heliothis subflexa females. J. Chem. Ecol. 31 : 15 28.
32. Groot, A., C. Gemeno, C. Brownie, F. Gould, and C. Schal. 2005b. Male and female antennal responses in Heliothis virescens and H. subflexa to conspecific and heterospecific sex pheromone compounds. Environ. Entomol. 34 : 256 263.
33. Groot, A. T., J. L. Horovitz, J. Hamilton, R. G. Santangelo, C. Schal, and F. Gould. 2006. Experimental evidence for interspecific directional selection on moth pheromone communication. Proc. Natl. Acad. Sci. USA 103 : 5858 5863.
34. Groot, A. T., R. G. Santangelo, E. Ricci, C. Brownie, F. Gould, and C. Schal. 2007. Differential attraction of Heliothis subflexa males to synthetic pheromone lures in Eastern US and Western Mexico. J. Chem. Ecol. 33 : 353 368.
35. Han, Q., and M. A. Caprio 2004. Evidence from genetic markers suggests seasonal variation in dispersal in Heliothis virescens (Lepidoptera: Noctuidae). Environ. Entomol. 33 : 1223 1231.
36. Hartstack, A. W., and J. A. Witz. 1981. Estimating field populations of tobacco budworms from pheromone trap catches. Environ. Entomol. 10 : 908 914.
37. Hartstack, A. W., J. A. Witz, and D. R. Buck. 1979. Moth traps for the tobacco budworm. J. Econ. Entomol. 72 : 519 522.
38. Haynes, K., and M. Birch. 1984. The periodicity of pheromone release and male responsiveness in the artichoke plume moth. Physiol. Entomol. 9 : 287 295.
39. Haynes, K. F., C. Gemeno, K. V. Yeargan, J. G. Millar, and K. M. Johnson. 2002. Aggressive chemical mimicry of moth pheromones by a bolas spider: how does this specialist predator attract more than one species of prey? Chemoecol. 12 : 99 105.
40. Heath, R. R., E. R. Mitchell, and J. Cibrian-Tovar. 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.
41. Heath, R. R., J. R. McLaughlin, F. Prosholt, and P. E. A. Teal. 1991. Periodicity of female sex pheromone titer and release in Heliothis subflexa and H. virescens (Lepidoptera: Noctuidae). Ann. Entomol. Soc. Am. 84 : 182 189.
42. Hillier, N. K., A. C. Kleineidam, and N. J. Vickers. 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 192 : 199 219.
43. Houde, A. E., and J. A. Endler. 1990. Correlated evolution of female mating preferences and male color patterns in the guppy Poecilia reticulata. Science 248 : 1405 1408.
44. Jaenicke, J. 1983. Induction of host preference in Drosophila melanogaster. Oecologia 58 : 320 325.
45. Jaenicke, J. 1988. Effects of early adult experience on host selection on insects: some experimental and theoretical results. J. Insect Behav. 1 : 3 15.
46. Jenkins, J. A. 1948. The origin of the cultivated tomato. Econ. Bot. 2 : 379 392.
47. Jiggins, C. D., R. E. Naisbit, R. L. Coe, and J. Mallet. 2001. Reproductive isolation caused by colour pattern mimicry. Nature 411 : 302 305.
48. Johansson, B. G., and T. M. Jones. 2007. The role of chemical communication in mate choice. Biol. Rev. 82 : 265 289.
49. Jurenka, R. 2003. Biochemistry of female moth sex pheromones. Pp. 54 80 in G. J. Blomquist and R.C. Vogt, eds. Insect pheromone biochemistry and molecular biology. Elsevier, Amsterdam.
50. Jurenka, R. A. 2004. Insect pheromone biosynthesis. Topics Curr. Chem. 239 : 97 132.
51. Kirkpatrick, M., and V. Ravigné. 2002. Speciation by natural and sexual selection: models and experiments. Am. Nat. 159 (Suppl 22 35.
52. Klun, J. A., J. R. Plimmer, and B. A. Bierl-Leonhardt. 1979. Trace chemicals: essence of sexual communication systems in Heliothis species. Science 204 : 1328 1330.
53. Klun, J. A., B. A. Bierl-Leonhardt, J. R. Plimmer, A. N. Sparks, M. Primiani, O. L. Chapman, G. Lepone, and G. H. Lee. 1980a. Sex pheromone chemistry of the female tobacco budworm moth Heliothis virescens. J. Chem. Ecol. 6 : 177 183.
54. Klun, J. A., J. R. Plimmer, B. A. Bierl-Leonhardt, A. N. Sparks, M. Primiani, O. L. Chapman, G. H. Lee, and G. Lepone. 1980b. Sex pheromone chemistry of female corn earworm moth, Heliothis zea. J. Chem. Ecol. 6 : 165 175.
55. Klun, J. A., B. A. Leonardt, J. D. Lopez, and L. E. LaChance. 1982. Female Heliothis subflexa (Lepidoptera: Noctuidae) sex pheromone - chemistry and congeneric comparisons. Environ. Entomol. 11 : 1084 1090.
56. Kondrashov, A. S., and F. A. Kondrashov. 1999. Interactions among quantitative traits in the course of sympatric speciation. Nature 400 : 351 354.
57. Laster, M. L. 1972. Interspecific hybridization of Heliothis virescens and H. subflexa. Environ. Entomol. 1 : 682 687.
58. Lim, H., and M. D. Greenfield. 2007. Female pheromonal chorusing in an arctiid moth, Utetheisa ornatrix. Behav. Ecol. 18 : 165 173.
59. Lim, H., and M. D. Greenfield. 2008. Female arctiid moths, Utetheisa ornatrix, orient towards and join pheromonal choruses. Anim. Behav. 75 : 673 680.
60. Lim, H., K. C. Park, T. C. Baker, and M. D. Greenfield. 2007. Perception of conspecific female pheromone stimulates female calling in an arctiid moth, Utetheisa ornatrix. J. Chem. Ecol. 33 : 1257 1271.
61. Linn, C. E., Jr., and W. L. Roelofs. 1995. Pheromone communication in moths and its role in the speciation process. Pp. 263 300 in D. M. Lambert and H. G. Spencer, eds. Speciation and the recognition concept: theory and application. Johns Hopkins Univ. Press, Baltimore, MD.
62. Linn, C. E., Jr., M. G. Campbell, and W. L. Roelofs. 1988. Temperature modulation of behavioral thresholds controlling male moth sex pheromone response specificity. Physiol. Entomol. 13 : 59 67.
63. Linn, C., M. Campbell, and W. Roelofs. 1991. The effects of different blend ratios and temperature on the active space of the Oriental fruit moth sex pheromone. Physiol. Entomol. 16 : 211 222.
64. Linn, C. E., Jr., M. S. Young, M. Gendle, T. J. Glover, and W. L. Roelofs. 1997. Sex pheromone blend discrimination in two races and hybrids of the European corn borer moth, Ostrinia nubilalis. Physiol. Entomol. 22 : 212 223.
65. Linn, C. E., Jr., M. O'Connor, and W. L. Roelofs. 2003. Silent genes and rare males: a fresh look at pheromone blend response specificity in the European corn borer moth, Ostrinia nubilalis. J. Insect Sci. 3 : 15.
66. Linn, C. E., Jr., C. J. Musto, and W. L. Roelofs. 2007. More rare males in Ostrinia: response of asian corn borer moths to the sex pheromone of the European corn borer. J. Chem. Ecol. 33 : 199 212.
67. Liu, Y.-B., and K. F. Haynes. 1994. Evolution of behavioral responses to sex pheromone in mutant laboratory colonies of Trichoplusia ni. J. Chem. Ecol. 20 : 231 238.
68. Ljungberg, H., P. Anderson, and B. H. Hansson. 1993. Physiology and morphology of pheromone-specific sensilla on the antennae of male and female Spodoptera littoralis (Lepidoptera: Noctuidae). J. Insect Physiol. 39 : 253 260.
69. Löfstedt, C. 1990. Population variation and genetic control of pheromone communication systems in moths. Entomol. Exp. Appl. 54 : 199 218.
70. Löfstedt, C. 1993. Moth pheromone genetics and evolution. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 340 : 167 177.
71. Löfstedt, C., W. M. Herrebout, and S. B. J. Menken. 1991. Sex pheromones and their potential role in the evolution of reproductive isolation in small ermine moths (Yponomeutidae). Chemoecol. 2 : 20 28.
72. Lopez, J. D., J. L. Goodenough, and K. R. Beerwinkel. 1994. Comparison of two sex pheromone trap designs for monitoring corn earworm and tobacco budworm (Lepidoptera: Noctuidae). J. Econ. Entomol. 87 : 793 801.
73. Magalhaes, I. S., S. Mwaiko, M. V. Schneider, and O. Seehausen. 2008. Divergent selection and phenotypic plasticity during incipient speciation in Lake Victoria cichlid fish. J. Evol. Biol. 22 : 260 274.
74. Marchetti, K. 1993. Dark habitats and bright birds illustrate the role of the environment in species divergence. Nature 362 : 149 152.
75. Mayr, E. 1963. Animal species and evolution. Harvard Univ. Press, Cambridge, MA.
76. McElfresh, J. S., and J. C. Millar. 1999. Geographic variation in sex pheromone blend of Hemileuca electra from Southern California. J. Chem. Ecol. 25 : 2505 2525.
77. McElfresh, J. S., and J. C. Millar. 2001. Geographic variation in the pheromone system of the saturniid moth Hemileuca eglanterina. Ecology 82 : 3505 3518.
78. McElvare, R. R. 1941. Validity of the species Heliothis subflexa (Gn.) (Lepidoptera). Bull. Brooklyn Entomol. Soc. 36 : 29 30.
79. McNeil, J. N., and J. Deslile. 1989. Host plant pollen influences calling behavior and ovarian development of the sunflower moth, Homoeosoma electellum. Oecologia 80 : 201 205.
80. Murlis, J., M. A. Willis, and R. T. Cardé. 2000. Spatial and temporal structures of pheromone plumes in fields and forests. Physiol. Entomol. 25 : 211 222.
81. Parajulee, M. N., D. R. Rummel, M. D. Arnold, and S. C. Carrol. 2004. Long term seasonal abundance patterns of Helicoverpa zea and Heliothis virescens (Lepidoptera: Noctuidae) in the Texas high plains. J. Econ. Entomol. 97 : 668 677.
82. Pashley, D. P., A. M. Hammond, and T. N. Hardy. 1992. Reproductive isolating mechanisms in fall armyworm host strains (Lepidoptera: Noctuidae). Ann. Entomol. Soc. Am. 85 : 400 405.
83. Phelan, P. L. 1997. Genetic and phylogenetics in the evolution of sex pheromones. Pp. 563 579 in R. T. Cardé and A. K. Minks, eds. Insect pheromone research: new directions. Chapman & Hall, New York.
84. Pope M. M., L. K. Gaston, and T. C. Baker. 1982. Composition, quantification, and periodicity of sex pheromone gland volatiles from individual Heliothis virescens females. J. Chem. Ecol. 8 : 1043 1055.
85. Pope M. M., L. K. Gaston, and T. C. Baker. 1984. Composition, quantification, and periodicity of sex pheromone volatiles from individual Heliothis zea females. J. Insect Physiol. 30 : 943 945.
86. Quero, C., and T. C. Baker. 1999. Antagonistic effect of (Z)-11-hexadecen-1-ol on the pheromone-mediated flight of Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae). J. Insect Behav. 12 : 701 710.
87. Rafaeli, A. 2002. Neuroendocrine control of pheromone biosynthesis in moths. Int. Rev. Cytol. 213 : 49 92.
88. Raffa, K. F., and D. L. Dahlsten. 1995. Differential responses among natural enemies and prey to bark beetle pheromones. Oecologia 102 : 17 23.
89. Raina, A. K. 1988. Selected factors influencing neurohormonal regulation of sex pheromone production in Heliothis species. J. Chem. Ecol. 14 : 2063 2069.
90. Raina, A. K. 1989. Male-induced termination of sex pheromone production and receptivity in mated females of Heliothis zea. J. Insect Physiol. 35 : 821 826.
91. Raina, A. K. 2003. Pheromone production in corn earworm: effect of temperature and humidity. Southw. Entomol. 28 : 115 120.
92. Ramaswamy, S. B., S. A. Randle, and W. K. Ma. 1985. Field evaluation of the sex pheromone components of Heliothis virescens (Lepidoptera: Noctuidae) in cone traps. Environ. Entomol. 14 : 293 296.
93. Ray, S. 1999. Survival of olfactory memory through metamorphosis in the fly Musca domestica. Neurosc. Lett. 259 : 37 40.
94. Ritchie, M. G., E. J. Halsey, and J. M. Gleason. 1999. Drosophila song as a species-specific mating signal and the behavioural importance of Kyriacou and Hall cycles in D. melanogaster song. Anim. Behav. 58 : 649 657.
95. Ritchie, M. G., M. Saarikettu, S. Livingstone, and A. Hoikkala. 2001. Characterization of female preference functions for Drosophila montana courtship song and a test of the temperature coupling hypothesis. Evolution 55 : 721 727.
96. Roelofs, W. L., A. S. Hill, R. T. Cardé, and T. C. Baker. 1974. Two sex pheromone components of the tobacco budworm moth, Heliothis virescens. Life Sci. 14 : 1555 1562.
97. Roelofs, W. L., W. Liu, G. Hao, H. Jiao, A. P. Rooney, and C. E. Linn, Jr. 2002. Evolution of moth sex pheromones via ancestral genes. Proc. Natl. Acad. Sci. U.S.A. 99 : 13621 13626.
98. Saetre, G.-P., T. Moum, S. Burei, M. Krai, M. Adamjan, and J. Moreno. 1997. A sexually selected character displacement in flycatchers reinforces premating isolation. Nature 387 : 589 592.
99. Schal, C. and R. T. Cardé. 1985. Rhythmic extrusion of pheromone gland elevates pheromone release rate. Experientia 41 : 617 619.
100. Schneider, J. C., R. T. Roush, W. F. Kitten, and M. L. Laster. 1989. Movement of Heliothis virescens (Lepidoptera: Noctuidae) in Mississippi in the Spring - implications for area-wide management. Env. Entomol. 18 : 438 446.
101. Schneider, D., S. Schulz, E. Priesner, J. Ziesmann, and W. Francke. 1998. Autodetection and chemistry of female and male pheromone in both sexes of the tiger moth Panaxia quadripunctaria. J. Comp. Physiol. A. 182 : 153 161.
102. Shaw, K. L., and Y. M. Parsons. 2002. Divergence of mate recognition behavior and its consequences for genetic architectures of speciation. Am. Nat. 159 : S61 S75.
103. Sheck, A. L., and F. Gould. 1993. The genetic basis of host range in Heliothis virescens: larval survival and growth. Entomol. Exp. Appl. 69 : 157 172.
104. Sheck, A. L, A. T. Groot, C. Ward, C. Gemeno, J. Wang, C. Schal, and F. Gould. 2006. Genetics of pheromone blend differences between Heliothis virescens and Heliothis subflexa: a chromosome mapping approach. J. Evol. Biol. 19 : 600 617.
105. Solé, J., A. Sans, M. Riba, E. Rosa, M. P. Bosch, M. Barrot, J. Palència, J. Castellà, and A. Guerrero. 2008. Reduction of damage by the Mediterranean corn borer, Sesamia nonagrioides, and the European corn borer, Ostrinia nubilalis, in maize fields by a trifluoromethyl ketone pheromone analog. Entomol. Exp. Appl. 126 : 28 39.
106. Slabbekoorn, H., and T. B. Smith. 2002. Habitat-dependent song divergence in the little greenbul: an analysis of environmental selection pressures on acoustic signals. Evolution 56 : 1849 1858.
107. Sparks, A. N., J. R. Raulston, P. D. Lingren, J. E. Carpenter, J. A. Klun, and B. G. Mullinix. 1979. Field response of male Heliothis virescens to pheromonal stimuli and traps. ESA Bull. 25 : 268 274.
108. Stadelbacher, E. A. 1981. Role of early-season wild and naturalized host plants in the buildup of the F1 generation of Heliothis zea (Lepidoptera, Noctuidae) and H. virescens (Lepidoptera: Noctuidae) in the delta of Mississippi. Env. Entomol. 10 : 766 770.
109. Stadelbacher, E. A., M. W. Barry, A. K. Raina, and J. R. Plimmer. 1983. Fatal interspecific mating of two Heliothis species induced by synthetic sex pheromone. Experientia 39 : 1174 1176.
110. Tafoya, F., L. Cruz-López, J. F. Barrera, and R. Magallanes-Cedeño. 2002. Pheromone trap efficiency for Heliothis virescens (F.) (Lepidoptera: Noctuidae) captures in tobacco. Agrociencia 36 : 355 364.
111. Teal, P. E. A., and J. H. Tumlinson. 1997. Effects of interspecific hybridization between Heliothis virescens and Heliothis subflexa on the sex pheromone communication system. Pp. 535 547 in R. T. Cardé and A. K. Minks, eds. Insect pheromone research: new directions. Chapman and Hall, New York.
112. Teal, P. E. A., R. R. Heath, J. H. Tumlinson, and J. R. McLaughlin. 1981. Identification of sex pheromone of Heliothis subflexa (G.) (Lepidoptera: Noctuidae) and field trapping studies using different blends of components. J. Chem. Ecol. 7 : 1011 1022.
113. Teal, P.E.A., J. H. Tumlinson, and R. R. Heath. 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.
114. Tillman, J. A., S. J. Seybold, R. A. Jurenka, and G. J. Blomquist. 1999. Insect pheromones - an overview of biosynthesis and endocrine regulation. Insect Biochem. Mol. Biol. 29 : 481 514.
115. Tully, T., V. Cambiazo, and L. Kruse. 1994. Memory through metamorphosis in normal and mutant Drosophila. J. Neurosci. 14 : 66 74.
116. Tumlinson, J. H., P. E. Hendricks, E. R. Mitchell, R. E. Doolittle, and M. M. Brennan. 1975. Isolation, identification and synthesis of the sex pheromone of the tobacco budworm. J. Chem. Ecol. 1 : 203 214.
117. Tumlinson, J. H., R. R. Heath, and P. E. A. Teal. 1982. Analysis of chemical communication systems of Lepidoptera. Pp. 1 25 in B. A. Leonhardt, and M. Beroza, eds. Insect pheromone technology - chemistry and applications. Am. Chem. Soc., Washington, D.C.
118. Van Emden, H. F., B. Sponagl, E. Wagner, T. Baker, S. Ganguly, and S. Douloumpaka. 1996. Hopkins' 'host selection principle,' another nail in its coffin. Physiol. Entomol. 21 : 325 328.
119. Vetter, R. S., and T. C. Baker. 1983. Behavioral responses of male Heliothis virescens in a sustained flight-tunnel to combinations of seven compounds identified from female glands. J. Chem. Ecol. 9 : 747 759.
120. Vetter, R. S., and T. C. Baker. 1984. Behavioral response of male Heliothis zea moths in sustained flight tunnel to combinations of 4 compounds identified from female sex pheromone gland. J. Chem. Ecol. 10 : 193 202.
121. Vickers, N. J. 2002. Defining a synthetic blend attractive to male Heliothis subflexa under wind tunnel conditions. J. Chem. Ecol. 28 : 1255 1267.
122. Vickers, N. J., and T. C. Baker. 1997. Chemical communication in heliothine moths. VII. Correlation between diminished responses to point-source plumes and single filaments similarly tainted with a behavioral antagonist. J. Comp. Physiol. A 180 : 523 536.
123. Wade, M. J., and C. J. Goodnight. 1998. Perspective: the theories of Fisher and Wright in the context of metapopulations: when nature does many small experiments. Evolution 52 : 1537 1553.
124. Webster, R. P., and R. T. Cardé. 1982. Relationships among pheromone titre, calling and age in the omnivorous leafroller moth (Platynota stultana). J. Insect Physiol. 28 : 925 933.
125. Wright, S. 1931. Evolution in Mendelian populations. Genetics 16 : 97 159.
126. Wright, S. 1932. The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proc. 6th Int. Congr. Genet. 1 : 356 366.
127. Zhu, J., B. B. Chastain, B. G. Spohn, and K. F. Haynes. 1997. Assortative mating in two pheromone strains of the Cabbage looper moth, Trichoplusia ni. J. Insect Behav. 10 : 805 817.