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Identification of Host Fruit Volatiles from Domestic Apple (Malus domestica), Native Black Hawthorn (Crataegus douglasii) and Introduced Ornamental Hawthorn (C. monogyna) Attractive to Rhagoletis pomonella Flies from the Western United States

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Abstract

The apple maggot fly, Rhagoletis pomonella, infests apple (Malus domestica) and hawthorn species (most notably the downy hawthorn, Crataegus mollis) in the eastern USA. Evidence suggests that the fly was introduced into the western USA sometime in the last 60 years. In addition to apple, R. pomonella also infests two species of hawthorns in the western USA as major hosts: the native black hawthorn (C. douglasii) and the introduced ornamental English hawthorn, C. monogyna. Apple and downy hawthorn-origin flies in the eastern USA use volatile blends emitted from the surface of their respective ripening fruit to find and discriminate among host trees. To test whether the same is true for western flies, we used coupled gas chromatography and electroantennographic detection (GC-EAD) and developed a 7-component apple fruit blend for western apple-origin flies, an 8-component black hawthorn fruit blend for flies infesting C. douglasii, and a 9-component ornamental hawthorn blend for flies from C. monogyna. Crataegus douglasii and C. monogyna-origin flies showed similar levels of upwind directed flight to their respective natal synthetic fruit blends in flight tunnel assays compared to whole fruit adsorbent extracts, indicating that the blends contain all the behaviorally relevant fruit volatiles to induce maximal response levels. The black and ornamental hawthorn blends shared four compounds in common including 3-methylbutan-1-ol, which appears to be a key volatile for R. pomonella populations in the eastern, southern, and western USA that show a preference for fruit from different Crataegus species. However, the blends also differed from one another and from domesticated apple in several respects that make it possible that western R. pomonella flies behaviorally discriminate among fruit volatiles and form ecologically differentiated host races, as is the case for eastern apple and hawthorn flies.

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References

  • AliNiazee, M. T. and Penrose, R. L. 1981. Apple maggot in Oregon: possible new threat to the Northwest apple industry. Bull. Entomol. Soc. Amer. 27:245–246.

    Google Scholar 

  • AliNiazee, M. T. and Westcott, R. L. 1987. Flight period and seasonal development of the apple maggot, Rhagoletis pomonella (Walsh) (Diptera, Tephritidae) in Oregon. Ann. Entomol. Soc. Amer. 80:823–828.

    Google Scholar 

  • Berlocher, S. H. and Feder, J. L. 2002. Sympatric speciation in phytophagous insects: Moving beyond controversy? Annu. Rev. Entomol. 47:773–815.

    Article  PubMed  CAS  Google Scholar 

  • Berlocher, S. H., McPheron, B. A., Feder, J. L., and Bush, G. L. 1993. A revised phylogeny of the Rhagoletis pomonella (Diptera: Tephritidae) sibling species group. Ann. Entomol. Soc. Amer. 86:716–727.

    Google Scholar 

  • Brunner, J. F. 1987. Apple maggot in Washington state: A review with special reference to its status in other Western States. Meladeria 45:33.

    Google Scholar 

  • Bush, G. L. 1966. The Taxonomy, Cytology, and Evolution of the genus Rhagoletis in North America (Diptera: Tephritidae). Museum of Comparative Zoology, Cambridge, MA.

    Google Scholar 

  • Bush, G. L. 1969. Sympatric host race formation and speciation in frugivorous flies of genus Rhagoletis (Diptera: Tephritidae). Evolution 23:237.

    Article  Google Scholar 

  • Cha, D. H., Powell, T. H. Q., Feder, J. L., and Linn, C. E. Jr. 2011a. Identification of host fruit volatiles from mayhaw species (Crataegus SERIES aestivales) host plants attractive to mayhaw-origin Rhagoletis pomonella flies in the southern United States. J. Chem. Ecol. 37:961–973.

    Article  PubMed  CAS  Google Scholar 

  • Cha, D. H., Powell, T. H. Q., Feder, J. L., and Linn, C. E. Jr. 2011b. Identification of host fruit volatiles from green hawthorn (Crataegus viridis) and blueberry hawthorn (C. brachyacantha) host plants attractive to different phenotypes of Rhagoletis pomonella flies in the southern United States. J. Chem. Ecol. 37:974–983.

    Article  PubMed  CAS  Google Scholar 

  • Coyne, J. A. and Orr, H. A. 2004. Speciation. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Dambroski, H. R. and Feder, J. L. 2007. Host plant and latitude-related diapause variation in Rhagoletis pomonella: A test for multifaceted life history adaptation on different stages of diapause development. J. Evol. Biol. 20:2101–2112.

    Article  PubMed  CAS  Google Scholar 

  • Dambroski, H. R., Linn, C. E. Jr., Feder, J. L., Berlocher, S. H., Nojima, S., and Roelofs, W. L. 2005. The genetics of fruit odor discrimination in Rhagoletis pomonella flies and its implications for sympatric host race formation and speciation. Evolution 59:1953–1964.

    PubMed  CAS  Google Scholar 

  • Feder, J. L. 1998. The apple maggot fly, Rhagoletis pomonella: Flies in the face of conventional wisdom? pp 130–144, in D. J. Howard and S. H. Berlocher (eds.), Endless Forms: Species and Speciation. Oxford University Press, Oxford.

    Google Scholar 

  • Feder, J. L. and Forbes, A.A. 2007. Habitat avoidance and speciation for phytophagous insect specialists. Funct. Ecol. 21:585–597.

    Article  Google Scholar 

  • Feder, J. L. and Forbes, A.A. 2008. Host fruit-odor discrimination and sympatric host-race formation. in K. J. Tilmon (ed.), The Evolutionary Biology of Herbivorous Insects: Specialization, Speciation, and Radiation. University of California Press, Berkley, CA.

    Google Scholar 

  • Feder, J. L., Opp, S. B., Wlazlo, B., Reynolds, K., Go, W., and Spisak, S. 1994. Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly. Proc. Natl. Acad. Sci. USA 91:7990–7994.

    Article  PubMed  CAS  Google Scholar 

  • Fein, B. L., Reissig, W. H., and Roelofs, W. L. 1982. Identification of apple volatiles attractive to the apple maggot. J. Chem. Ecol. 8:1473–1487.

    Article  CAS  Google Scholar 

  • Forbes, A. A., Fisher, J., and Feder, J. L. 2005. Habitat avoidance: Overlooking an important aspect of host-specific mating and sympatric speciation? Evolution 59:1552–1559.

    PubMed  Google Scholar 

  • Forbes, A. A. and Feder, J. L. 2006. Divergent preferences of Rhagoletis pomonella host races for olfactory and visual cues. Entomol. Exp. App. 119:121–127.

    Article  Google Scholar 

  • Funk, D. J., Filchak, K. E., and Feder, J. L. 2002. Herbivorous insects: model systems for the comparative study of speciation ecology. Genetics 116:251–267.

    Google Scholar 

  • Greenwald, R., Chaykovsky, M., and Corey, E. J. 1963. The Wittig reaction using methylsulfinyl carbanion-dimethyl sulfoxide. J. Org. Chem. 28:1128–1129.

    Article  CAS  Google Scholar 

  • Linn, C. E. Jr., Feder, J. L., Nojima, S., Dambroski, H. R., Berlocher, S. H., and Roelofs, W. L. 2003. Fruit odor discrimination and sympatric host race formation in Rhagoletis. Proc. Natl. Acad. Sci. USA 100:11490–11493.

    Article  PubMed  CAS  Google Scholar 

  • Linn, C. E. Jr., Dambroski, H. R., Feder, J. L., Berlocher, S. H., Nojima, S., and Roelofs, W. L. 2004. Postzygotic isolating factor in sympatric speciation in Rhagoletis flies: reduced response of hybrids to parental host-fruit odors. Proc. Natl. Acad. Sci. USA 101:17753–17758.

    Article  PubMed  CAS  Google Scholar 

  • Linn, C. E. Jr., Nojima, S., and Roelofs, W. L. 2005a. Antagonist effects of non-host fruit volatiles on discrimination of host fruit by Rhagoletis flies infesting apple (Malus pumila), hawthorn (Crataegus spp.), and flowering dogwood (Cornus florida). Entomol. Exp. Appl. 114:97–105.

    Article  CAS  Google Scholar 

  • Linn, C. E. Jr., Dambroski, H., Nojima, S., Feder, J. L., Berlocher, S. H., and Roelofs, W. L. 2005b. Variability in response specificity of apple, hawthorn, and flowering dogwood-infesting Rhagoletis flies to host fruit volatile blends: implications for sympatric host shifts. Entomol. Exp. Appl. 116:55–64.

    Article  Google Scholar 

  • Mcpheron, B. A. 1990. Genetic-structure of the apple maggot fly (Diptera: Tephritidae) populations. Ann. Entomol. Soc. Amer. 83:568–577.

    Google Scholar 

  • National Agricultural Statistics Service 2009. Apples, Washington. U.S. Department of Agriculture. Washington Field Office. www.nass.usda.gov.

  • Neilson, W. T. A. and Mcallan, J. W. 1965. Artificial diets for apple maggot 3. Improved defined diets. J. Econ. Entomol. 58:542.

    Google Scholar 

  • Nojima, S., Linn, C. E., Jr., Zhang, A., Morris, B., and Roelofs, W. L. 2003a. Identification of host fruit volatiles from hawthorn (Crataegus spp.) attractive to hawthorn-origin Rhagoletis pomonella flies. J. Chem. Ecol. 29:319–334.

    Google Scholar 

  • Nojima, S., Linn, C. E., Jr., Zhang, A., Morris, B., and Roelofs, W. L. 2003b. Identification of host fruit volatiles from flowering dogwood (Cornus florida) attractive to dogwood-origin Rhagoletis pomonella flies. J. Chem. Ecol. 29:2347–2357.

    Article  CAS  Google Scholar 

  • Prokopy, R. J., Bennett, E. W., and Bush, G. L. 1971. Mating behavior in Rhagoletis pomonella (Diptera: Tephritidae). I. Site of assembly. Can. Entomol. 103:1405–1409.

    Article  Google Scholar 

  • Prokopy, R. J., Bennett, E. W., and Bush, G. L. 1972. Mating behavior in Rhagoletis pomonella (Diptera: Tephritidae). II. Temporal organization. Can. Entomol. 104:97–104.

    Article  Google Scholar 

  • Tracewski, K. T., Brunner, J. F., Hoyt, S. C., and Dewey, S. R. 1987. Occurrence of Rhagoletis pomonella (Walsh) in hawthorns, Crataegus, of the Pacific Northwest (USA). Melanderia 45:19–25.

    Google Scholar 

  • Yee, W. L. 2008. Host plant use by apple maggot, western cherry fruit fly, and other Rhagoletis species (Diptera:Tephritidae) in central Washington state. Pan. Pac. Entomol. 84:163–178.

    Article  Google Scholar 

  • Yee, W. L. and Goughnour, R. B. 2008. Host plant use by and new host records of apple maggot, western cherry fruit fly, and other Rhagoletis species (Diptera: Tephritidae) in western Washington state. Pan. Pac. Entomol. 84:179–183.

    Article  Google Scholar 

  • Yee, W. L., Landolt, P. J., and Darnell, T. J. 2005. Attraction of Rhagoletis pomonella (Diptera: Tephritidae) and nontarget flies to traps baited with ammonium carbonate and fruit volatile lures in Washington and Oregon. J. Agr. Urb. Entomol. 22:133–149.

    CAS  Google Scholar 

  • Zhang, A., Linn, C. E. Jr., Wright, S., Prokopy, R., Reissig, W., and Roelofs, W. L. 1999. Identification of a new blend of apple volatiles attractive to the apple maggot, Rhagoletis pomonella. J. Chem. Ecol. 25:1221–1232.

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Mike Chong at the University of Waterloo, Ontario, Canada, for the synthesis of DMNT. We thank Tracy Arcella, Stewart Berlocher, Scott Egan, Andrew Forbes, Glen Hood, Dave Costello, H. W. Jackson, and Jim Stevens for help in collecting fruit and fly samples, thoughtful discussion, and/or assistance in helping us prepare the manuscript for publication. We thank Blair Wolfley, Washington State University, Vancouver, and Clark County, WA General Services, for providing storage and rearing facilities. We acknowledge Meralee Nash for collection of fruit and rearing of larvae from Puyallup. We thank Callie Musto, Kathy Poole, and Paula Fox for maintaining the flies received from Notre Dame and Yakima, and Harvey Reissig, Cynthia Smith, and Dave Combs for use of the Geneva, New York, apple maggot colony. The research was supported by grants to J.L.F. and C.E.L. from the National Science Foundation (#0614378) to J.L.F. from the USDA, and to W.L.Y. from the Washington Tree Fruit Research Commission and Washington State Commission on Pesticide Registration.

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Correspondence to Charles E. Linn Jr.

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Cha, D.H., Yee, W.L., Goughnour, R.B. et al. Identification of Host Fruit Volatiles from Domestic Apple (Malus domestica), Native Black Hawthorn (Crataegus douglasii) and Introduced Ornamental Hawthorn (C. monogyna) Attractive to Rhagoletis pomonella Flies from the Western United States. J Chem Ecol 38, 319–329 (2012). https://doi.org/10.1007/s10886-012-0087-9

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