Journal of Chemical Ecology

, Volume 39, Issue 3, pp 364–376 | Cite as

Pheromonal Divergence Between Two Strains of Spodoptera frugiperda

  • Melanie Unbehend
  • Sabine Hänniger
  • Robert L. Meagher
  • David G. Heckel
  • Astrid T. Groot


Spodoptera frugiperda consists of two genetically and behaviorally different strains, the corn- and the rice-strain, which seem to be in the process of sympatric speciation. We investigated the role of strain-specific sexual communication as a prezygotic mating barrier between both strains by analyzing strain-specific variation in female pheromone composition of laboratory and field strains, and also male attraction in wind tunnel and field experiments. Laboratory-reared and field-collected females from Florida exhibited strain-specific differences in their relative amount of (Z)-7-dodecenyl acetate (Z7-12:OAc) and (Z)-9-dodecenyl acetate (Z9-12:OAc). In wind tunnel assays, we did not find strain-specific attraction of males to females. However, in field experiments in Florida, we observed some differential attraction to synthetic pheromone blends. In a corn field, the corn-strain blend attracted more males of both strains than the rice-strain blend, but both blends were equally attractive in a grass field. Thus, habitat-specific volatiles seemed to influence male attraction to pheromones. In dose–response experiments, corn-strain males were more attracted to 2 % Z7-12:OAc than other doses tested, while rice-strain males were attracted to a broader range of Z7-12:OAc (2–10 %). The attraction of corn-strain males to the lowest dose of Z7-12:OAc corresponds to the production of this compound by females; corn-strain females produced significantly smaller amounts of Z7-12:OAc than rice-strain females. Although corn-strain individuals are more restricted in their production of and response to pheromones than rice-strain individuals, it seems that differences in sexual communication between corn- and rice-strain individuals are not strong enough to cause assortative mating.


Sexual communication Male attraction Fall armyworm Corn- and rice-strain Synthetic pheromone lures Dose–response experiments Lepidoptera Noctuidae Sympatric speciation 



This research was funded by the Deutsche Forschungsgemeinschaft (P.S.GR362721) and the Max Planck Gesellschaft. We thank Prof. Manfred Ayasse from the Institute of Experimental Ecology at the University of Ulm in Germany for his help with the wind tunnel experiments. Special thanks to Gregg Nuessly from the Everglades Research and Education Center in Belle Glade and to Tommy Toms, Manager of the Graham Farms in Moore Haven, which supported the male trapping experiments in Florida. We thank Antje Schmaltz and Katja Müller (MPICE, Jena, GER) for their assistance in strain-typing trapped males, and Amy Rowley (USDA, Gainesville, FL) for assistance in the field experiments.


  1. Andrade, R., Rodriguez, C., and Oehlschlager, A. C. 2000. Optimization of a pheromone lure for Spodoptera frugiperda (Smith) in Central America. J. Braz. Chem. Soc. 11:609–613.CrossRefGoogle Scholar
  2. Baker, T. C. 2002. Mechanism for saltational shifts in pheromone communication systems. Proc. Natl. Acad. Sci. U. S. A. 99:13368–13370.PubMedCrossRefGoogle Scholar
  3. Batista-Pereira, L. G., Stein, K., de Paula, A. F., Moreira, J. A., Cruz, I., Figueiredo, M. D., Perri, J., and Correa, A. G. 2006. Isolation, identification, synthesis, and field evaluation of the sex pheromone of the Brazilian population of Spodoptera frugiperda. J. Chem. Ecol. 32:1085–1099.PubMedCrossRefGoogle Scholar
  4. Busato, G. R., Grutzmacher, A. D., de Oliveira, A. C., Vieira, E. A., Zimmer, P. D., Kopp, M. M., Bandeira, J. D., and Magalhaes, T. R. 2004. Analysis of the molecular structure and diversity of Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae) populations associated to the corn and rice crops in Rio Grande do Sul State. Brazil. Neotrop. Entomol. 33:709–716.CrossRefGoogle Scholar
  5. Cardé, R. T. and Baker, T. C. 1984. Sexual communication with pheromones, pp. 355–383, in W. J. Bell and R. T. Cardé (eds.), Chemical Ecology of Insects. Chapman & Hall, London.Google Scholar
  6. Cardé, R. T. and Haynes, K. F. 2004. Structure of the pheromone communication channel in moths, pp. 283–332, in R. T. Cardé and J. G. Millar (eds.), Advances in Insect Chemical Ecology. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  7. Charlton, R. E., Kanno, H., Collins, R. D., and Carde, R. T. 1993. Influence of pheromone concentration and ambient-temperature on flight of the gypsy moth, Lymantria dispar (L.), in a sustained flight wind-tunnel. Physiol. Entomol. 18:349–362.CrossRefGoogle Scholar
  8. Clark, P. L., Molina-Ochoa, J., Martinelli, S., Skoda, S. R., Isenhour, D. J., Lee, D. J., Krumm, J. T., and Foster, J. E. 2007. Population variation of the fall armyworm, Spodoptera frugiperda, in the Western Hemisphere. J. Insect Sci. 7:5.PubMedCrossRefGoogle Scholar
  9. Coyne, J. A. and Orr, H. A. 2004. Speciation. Sinauer Associates, Sunderland.Google Scholar
  10. Deng, J. Y., Wei, H. Y., Huang, Y. P., and Du, J. W. 2004. Enhancement of attraction to sex pheromones of Spodoptera exigua by volatile compounds produced by host plants. J. Chem. Ecol. 30:2037–2045.PubMedCrossRefGoogle Scholar
  11. Descoins, C., Silvain, J. F., Lalannecassou, B., and Cheron, H. 1988. Monitoring of crop pests by sexual trapping of males in the French West-Indies and Guyana. Agric. Ecosyst. Environ. 21:53–65.CrossRefGoogle Scholar
  12. Fleischer, S. J., Harding, C. L., Blom, P. E., White, J., and Grehan, J. 2005. Spodoptera frugiperda pheromone lures to avoid nontarget captures of Leucania phragmatidicola. J. Econ. Entomol. 98:66–71.PubMedCrossRefGoogle Scholar
  13. Foster, S. P. and Howard, A. J. 1999. The effects of source dosage, flight altitude, wind speed, and ground pattern on the sex pheromone-mediated flight manoeuvres of male lightbrown apple moth, Epiphyas postvittana (Walker). N. Z. J. Zool. 26:97–104.CrossRefGoogle Scholar
  14. Groot, A. T., Marr, M., Schoefl, G., Lorenz, S., Svatos, A., and Heckel, D. G. 2008. Host strain specific sex pheromone variation in Spodoptera frugiperda. Front. Zool. 5:20. doi: 10.1186/1742-9994-5-20.PubMedCrossRefGoogle Scholar
  15. Groot, A. T., Marr, M., Heckel, D. G., and Schöfl, G. 2010. The roles and interactions of reproductive isolation mechanisms in fall armyworm (Lepidoptera: Noctuidae) host strains. Ecol. Entomol. 35:105–118.CrossRefGoogle Scholar
  16. Haynes, K. F. and Hunt, R. E. 1990. Interpopulational variation in emitted pheromone blend of cabbage looper moth, Trichoplusia ni. J. Chem. Ecol. 16:509–519.CrossRefGoogle Scholar
  17. Heath, R. R., Teal, P. E. A., Tumlinson, J. H., and Mengelkoch, J. L. 1986. Prediction of release ratios of multicomponent pheromones from rubber septa. J. Chem. Ecol. 12:2133–2143.CrossRefGoogle Scholar
  18. Jones, R. L. and Sparks, A. N. 1979. (Z)-9-tetradecen-1-ol acetate, a secondary sex pheromone of the fall armyworm, Spodoptera frugiperda (J. E. Smith). J. Chem. Ecol. 5:721–725.CrossRefGoogle Scholar
  19. Juárez, M. L., Murua, M. G., Garcia, M. G., Ontivero, M., Vera, M. T., Vilardi, J. C., Groot, A. T., Castagnaro, A. P., Gastaminza, G., and Willink, E. 2012. Host association of Spodoptera frugiperda (Lepidoptera: Noctuidae) corn and rice strains in Argentina, Brazil, and Paraguay. J. Econ. Entomol. 105:573–582.PubMedCrossRefGoogle Scholar
  20. Klun, J. A. and COOPERATORS 1975. Insect sex pheromones: Intraspecific pheromonal variability of Ostrinia nubilalis Lepidoptera, Pyralidae in North America and Europe. Environ. Entomol. 4:891–894.Google Scholar
  21. Klun, J. A., Chapman, O. L., Mattes, K. C., Wojtkowski, P. W., Beroza, M., and Sonnet, P. E. 1973. Insect sex pheromones: Minor amount of opposite geometrical isomer critical to attraction. Science 181:661–663.PubMedCrossRefGoogle Scholar
  22. Kochansky, J., Cardé, R. T., Liebherr, J., and Roelofs, W. L. 1975. Sex pheromone of the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae), in New York. J. Chem. Ecol. 1:225–231.CrossRefGoogle Scholar
  23. Landolt, P. J. and Phillips, T. W. 1997. Host plant influences on sex pheromone behavior of phytophagous insects. Annu. Rev. Entomol. 42:371–391.PubMedCrossRefGoogle Scholar
  24. Landolt, P. J., Heath, R. R., Millar, J. G., Davishernandez, K. M., Dueben, B. D., and Ward, K. E. 1994. Effects of host plant, Gossypium hirsutum L., on sexual attraction of cabbage looper moths, Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae). J. Chem. Ecol. 20:2959–2974.CrossRefGoogle Scholar
  25. Lassance, J. M. 2010. Journey in the Ostrinia world: from pest to model in chemical ecology. J. Chem. Ecol. 36:1155–1169.PubMedCrossRefGoogle Scholar
  26. Lassance, J. M., Groot, A. T., Liénard, M. A., Antony, B., Borgwardt, C., Andersson, F., Hedenström, E., Heckel, D. G., and Löfstedt, C. 2010. Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones. Nature 466:486–489.PubMedCrossRefGoogle Scholar
  27. Levy, H. C., Garcia-Maruniak, A., and Maruniak, J. E. 2002. Strain identification of Spodoptera frugiperda (Lepidoptera: Noctuidae) insects and cell line: PCR-RFLP of cytochrome oxidase C subunit I gene. Fla. Entomol. 85:186–190.CrossRefGoogle Scholar
  28. Lima, E. R. and McNeil, J. N. 2009. Female sex pheromones in the host races and hybrids of the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae). Chemoecology 19:29–36.CrossRefGoogle Scholar
  29. Liu, Y. B. and Haynes, K. F. 1993. Impact of (Z)-7-dodecenol and turbulence on pheromone-mediated flight maneuvers of male Trichoplusia ni. Physiol. Entomol. 18:363–371.CrossRefGoogle Scholar
  30. Löfstedt, C. 1993. Moth pheromone genetics and evolution. Phil. Trans. Royal Soc. Lond. B. 340:167–177.CrossRefGoogle Scholar
  31. Löfstedt, C. and Kozlov, M. 1997. A phylogenetic analysis of pheromone communication in primitive moths, pp. 473–489, in R. T. Cardé and A. K. Minks (eds.), Insect Pheromone Research: New Directions. Chapman & Hall, New York.CrossRefGoogle Scholar
  32. Löfstedt, C., Lanne, B. S., Lofqvist, J., Appelgren, M., and Bergstrom, G. 1985. Individual variation in the pheromone of the turnip moth, Agrotis segetum. J. Chem. Ecol. 11:1181–1196.CrossRefGoogle Scholar
  33. Lu, Y. J. and Adang, M. J. 1996. Distinguishing fall armyworm (Lepidoptera: Noctuidae) strains using a diagnostic mitochondrial DNA marker. Fla. Entomol. 79:48–55.CrossRefGoogle Scholar
  34. Lu, Y. J., Kochert, G. D., Isenhour, D. J., and Adang, M. J. 1994. Molecular characterization of a strain-specific repeated DNA sequence in the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). Insect Mol. Biol. 3:123–130.PubMedCrossRefGoogle Scholar
  35. Luginbill, P. 1928. The fall armyworm. U. S. Dept. Agric. Tech. Bull. 34:1–92.Google Scholar
  36. Machado, V., Wunder, M., Baldissera, V. D., Oliveira, J. V., Fiuza, L. M., and Nagoshi, R. N. 2008. Molecular characterization of host strains of Spodoptera frugiperda (Lepidoptera: Noctuidae) in Southern Brazil. Ann. Entomol. Soc. Am. 101:619–626.CrossRefGoogle Scholar
  37. Malo, E. A., Castrejon-Gomez, V. R., Cruz-Lopez, L., and Rojas, J. C. 2004. Antennal sensilla and electrophysiological response of male and female Spodoptera frugiperda (Lepidoptera: Noctuidae) to conspecific sex pheromone and plant odors. Ann. Entomol. Soc. Am. 97:1273–1284.CrossRefGoogle Scholar
  38. Martinelli, S., Clark, P. L., Zucchi, M. I., Silva-Filho, M. C., Foster, J. E., and Omoto, C. 2007. Genetic structure and molecular variability of Spodoptera frugiperda (Lepidoptera: Noctuidae) collected in maize and cotton fields in Brazil. Bull. Entomol. Res. 97:225–231.PubMedCrossRefGoogle Scholar
  39. McMichael, M. and Prowell, D. P. 1999. Differences in amplified fragment-length polymorphisms in fall armyworm (Lepidoptera: Noctuidae) host strains. Ann. Entomol. Soc. Am. 92:175–181.Google Scholar
  40. Meagher, R. L. and Gallo-Meagher, M. 2003. Identifying host strains of fall armyworm (Lepidoptera\Noctuidae) in Florida using mitochondrial markers. Fla. Entomol. 86:450–455.CrossRefGoogle Scholar
  41. Miller, J. R. and Roelofs, W. L. 1980. Individual variation in sex pheromone component ratios in two populations of the redbanded leafroller moth, Argyrotaenia velutinana. Environ. Entomol. 9:359–363.Google Scholar
  42. Nagoshi, R. N. 2010. The fall armyworm Triose phosphate isomerase (Tpi) gene as a marker of strain identity and interstrain mating. Ann. Entomol. Soc. Am. 103:283–292.CrossRefGoogle Scholar
  43. Nagoshi, R. N. and Meagher, R. L. 2003. FR tandem-repeat sequence in fall armyworm (Lepidoptera: Noctuidae) host strains. Ann. Entomol. Soc. Am. 96:329–335.CrossRefGoogle Scholar
  44. Nagoshi, R. N. and Meagher, R. L. 2008. Review of fall armyworm (Lepidoptera: Noctuidae) genetic complexity and migration. Fla. Entomol. 91:546–554.Google Scholar
  45. Nagoshi, R. N., Meagher, R. L., Adamczyk, J. J., Braman, S. K., Brandenburg, R. L., and Nuessly, G. 2006. New restriction fragment length polymorphisms in the cytochrome oxidase I gene facilitate host strain identification of fall armyworm (Lepidoptera: Noctuidae) populations in the Southeastern United States. J. Econ. Entomol. 99:671–677.PubMedCrossRefGoogle Scholar
  46. Nagoshi, R. N., Silvie, P., Meagher, R. L., Lopez, J., and Machados, V. 2007. Identification and comparison of fall armyworm (Lepidoptera: Noctuidae) host strains in Brazil, Texas, and Florida. Ann. Entomol. Soc. Am. 100:394–402.CrossRefGoogle Scholar
  47. Nagoshi, R. N., Meagher, R. L., Flanders, K., Gore, J., Jackson, R., Lopez, J., Armstrong, J. S., Buntin, G. D., Sansone, C., and Leonard, B. R. 2008. Using haplotypes to monitor the migration of fall armyworm (Lepidoptera: Noctuidae) corn-strain populations from Texas and Florida. J. Econ. Entomol. 101:742–749.PubMedCrossRefGoogle Scholar
  48. Ochieng, S. A., Park, K. C., and Baker, T. C. 2002. Host plant volatiles synergize responses of sex pheromone-specific olfactory receptor neurons in male Helicoverpa zea. J. Comp. Physiol. A. 188(4):325–333.CrossRefGoogle Scholar
  49. Party, V., Hanot, C., Said, I., Rochat, D., and Renou, M. 2009. Plant terpenes affect intensity and temporal parameters of pheromone detection in a moth. Chem. Senses 34:763–774.PubMedCrossRefGoogle Scholar
  50. Pashley, D. P. 1986. Host-associated genetic differentiation in fall armyworm (Lepidoptera, Noctuidae): a sibling species complex? Ann. Entomol. Soc. Am. 79:898–904.Google Scholar
  51. Pashley, D. P. 1989. Host-associated differentiation in armyworms (Lepidoptera: Noctuidae): an allozymic and mitochondrial DNA perspective, pp. 103–114, in H. D. Loxdale and J. D. Hollander (eds.), Electrophoretic Studies on Agricultural Pests. Oxford University Press, New York.Google Scholar
  52. Pashley, D. P. and Ke, L. D. 1992. Sequence evolution in mitochondrial ribosomal and ND-1 genes in Lepidoptera - implications for phylogenetic analysis. Mol. Biol. Evol. 9:1061–1075.PubMedGoogle Scholar
  53. Pashley, D. P., Hammond, A. M., and Hardy, T. N. 1992. Reproductive isolating mechanisms in fall armyworm host strains (Lepidoptera, Noctuidae). Ann. Entomol. Soc. Am. 85:400–405.Google Scholar
  54. Phelan, P. L. 1992. Evolution of sex pheromones and the role of asymmetric tracking, pp. 245–264, in B. T. Roitberg and M. B. Isman (eds.), Insect Chemical Ecology. An Evolutionary Approach. Chapman & Hall, New York.Google Scholar
  55. Prowell, D. P., McMichael, M., and Silvain, J. F. 2004. Multilocus genetic analysis of host use, introgression, and speciation in host strains of fall armyworm (Lepidoptera: Noctuidae). Ann. Entomol. Soc. Am. 97:1034–1044.CrossRefGoogle Scholar
  56. R Development Core Team. 2007. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  57. Reddy, G. V. P. and Guerrero, A. 2004. Interactions of insect pheromones and plant semiochemicals. Trends Plant Sci. 9:253–261.PubMedCrossRefGoogle Scholar
  58. Roelofs, W. L. and Carde, R. T. 1974. Sex pheromones in the reproductive isolation of lepidopterous species, pp. 96–114, in M. C. Birch (ed.), Pheromones. North-Holland, Amsterdam.Google Scholar
  59. Rojas, J. C. 1999. Influence of age, sex and mating status, egg load, prior exposure to mates, and time of day on host-finding behavior of Mamestra brassicae (Lepidoptera: Noctuidae). Environ. Entomol. 28:155–162.Google Scholar
  60. Schöfl, G., Heckel, D. G., and Groot, A. T. 2009. Time-shifted reproductive behaviours among fall armyworm (Noctuidae: Spodoptera frugiperda) host strains: evidence for differing modes of inheritance. J. Evol. Biol. 22:1447–1459.PubMedCrossRefGoogle Scholar
  61. Sekul, A. A. and Sparks, A. N. 1967. Sex pheromone of the fall armyworm moth: isolation, identification and synthesis. J. Econ. Entomol. 60:1270–1272.Google Scholar
  62. Smadja, C. and Butlin, R. K. 2009. On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102:77–97.PubMedCrossRefGoogle Scholar
  63. Sparks, A. N. 1979. A review of the biology of the fall armyworm. Fla. Entomol. 62:82–86.CrossRefGoogle Scholar
  64. Tamaki, Y. 1985. Sex pheromones, pp. 145–191, in G. A. Kerkut and L. I. Gilbert (eds.), Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 9. Pergamon Press, Oxford.Google Scholar
  65. Tumlinson, J. H., Mitchell, E. R., Teal, P. E. A., Heath, R. R., and Mengelkoch, L. J. 1986. Sex pheromone of fall armyworm, Spodoptera frugiperda (J. E. Smith): identification of components critical to attraction in the field. J. Chem. Ecol. 12:1909–1926.CrossRefGoogle Scholar
  66. Tumlinson, J. H., Mitchell, E. R., and Yu, H.-S. 1990. Analysis and field evaluation of volatile blend emitted by calling virgin females of beet armyworm moth, Spodoptera exigua (Hübner). J. Chem. Ecol. 16:3411–3423.CrossRefGoogle Scholar
  67. Wicker-Thomas, C. 2011. Evolution of insect pheromones and their role in reproductive isolation and speciation. Ann. Soc. Entomol. Fr. 47:55–62.Google Scholar
  68. Yang, Z. H., Bengtsson, M., and Witzgall, P. 2004. Host plant volatiles synergize response to sex pheromone in codling moth, Cydia pomonella. J. Chem. Ecol. 30:619–629.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Melanie Unbehend
    • 1
  • Sabine Hänniger
    • 1
  • Robert L. Meagher
    • 2
  • David G. Heckel
    • 1
  • Astrid T. Groot
    • 1
    • 3
  1. 1.Department of EntomologyMPICEJenaGermany
  2. 2.USDA-ARSGainesvilleUSA
  3. 3.Institute for Biodiversity and Ecosystem DynamicsUniversity of AmsterdamAmsterdamthe Netherlands

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