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Species-specific aggregation pheromones contribute to coexistence in two closely related thrips species

Published online by Cambridge University Press:  21 May 2018

X. Li ,
S. Geng ,
Z. Zhang ,
J. Zhang ,
W. Li ,
J. Huang ,
W. Lin ,
Y. Bei  and
Y. Lu
X. Li
Affiliation:
State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China
S. Geng
Affiliation:
State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China College of Chemistry and Life Science, Zhejiang Normal University, Jinhua, Zhejiang 321004, China
Z. Zhang
Affiliation:
State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China
J. Zhang
Affiliation:
State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China
W. Li
Affiliation:
State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China
J. Huang
Affiliation:
State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China
W. Lin
Affiliation:
State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China
Y. Bei
Affiliation:
State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China
Y. Lu*
Affiliation:
State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control, Institute of Plant Protection and Microbiology, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, China College of Chemistry and Life Science, Zhejiang Normal University, Jinhua, Zhejiang 321004, China
*
*Author for correspondence Phone: +86 571 86400445 Fax: +86 571 86400445 E-mail: luybcn@163.com
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Abstract

Pheromones play an important role in mediating interspecific interactions in insects. In an insect community, pheromones can reveal information about the senders, which could be used by other members of the food web (competitor, natural enemies, etc.) to their own advantage. The aggregation pheromones of two closely related thrips species, Frankliniella occidentalis and Frankliniella intonsa, have been identified with the same major compounds, (R)-lavandulyl acetate and neryl (S)-2-methylbutanoate, but in different ratios. However, the roles of the aggregation pheromones in the interspecific interactions between these two closely related species are unknown. Here, we investigated the roles of major aggregation pheromone compounds in interspecific interactions between F. occidentalis and F. intonsa for both long and short ranges. The results showed that, at tested doses, neither aggregation pheromone-induced long range cross-attraction nor short range cross-mating was detected between F. occidentalis and F. intonsa. Field-trapping trials showed that the species-specificity in aggregation pheromones was regulated by the ratio of two major compounds. However, species-specific blends of the two major compounds had no effect on short-range interactions between these two species. Our data from the thrips species provide support for the ‘aggregation model of coexistence’, explaining the species-specific pheromone-mediated coexistence of closely related species. Thus, species-specific pheromones could be one of the factors affecting population dynamics and community structure in closely related insects with similar niches.

Keywords

Aggregation pheromone(R)-lavandulyl acetateneryl (S)-2-methylbutanoateFrankliniella occidentalisFrankliniella intonsainterspecific interactionscoexistence
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 1 , February 2019 , pp. 119 - 126
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Copyright
Copyright © Cambridge University Press 2018 

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References

Akella, S.V.S., Kirk, W.D.J., Lu, Y.-b., Murai, T., Walters, K.F.A. & Hamilton, J.G.C. (2014) Identification of the aggregation pheromone of the melon thrips, Thrips palmi. PLoS ONE 9, e103315.Google Scholar
Andersson, M.N., Löfstedt, C. & Newcomb, R.D. (2015) Insect olfaction and the evolution of receptor tuning. Frontiers in Ecology & Evolution 3, 53.Google Scholar
Atkinson, W.D. & Shorrocks, B. (1979) Competition on a divided and ephemeral resource. Journal of Animal Ecology 48, 899–908.Google Scholar
Ayres, B.D., Ayres, M.P., Abrahamson, M.D. & Teale, S.A. (2001) Resource partitioning and overlap in three sympatric species of Ips bark beetles (Coleoptera: Scolytidae). Oecologia 128, 443–453.Google Scholar
Bartelt, R.J., Schaner, A.M. & Jackson, L.L. (1987) Aggregation pheromones in five taxa of the Drosophila virilis species group. Physiological Entomology 11, 367–376.Google Scholar
Bartelt, R.J., Weaver, D.K. & Arbogast, R.T. (1995) Aggregation pheromone of Carpophilus dimidiatus (F.) (Coleoptera: Nitidulidae) and responses to Carpophilus pheromones in South Carolina. Journal of Chemical Ecology 21, 1763–1779.Google Scholar
Broughton, S. & Harrison, J. (2012) Evaluation of monitoring methods for thrips and the effect of trap colour and semiochemicals on sticky trap capture of thrips (Thysanoptera) and beneficial insects (Syrphidae, Hemerobiidae) in deciduous fruit trees in Western Australia. Crop protection (Guildford, Surrey) 42, 156–163.Google Scholar
Byers, J.A., Birgersson, G. & Francke, W. (2013) Aggregation pheromones of bark beetles, Pityogenes quadridens and P. bidentatus, colonizing Scotch pine: olfactory avoidance of interspecific mating and competition. Chemoecology 23, 251–261.Google Scholar
Dobzhansky, T. (1940) Genetics and the Origin of Species. New York, Columbia University Press.Google Scholar
Gai, H.T., Zhi, J.R., Li, Z.X. & Jiang, Y.J. (2010) Survival rates of Frankliniella occidentalis and Frankliniella intonsa after exposure to adverse temperature conditions. Chinese Journal of Ecology 29, 1533–1537.Google Scholar
Gai, H.T., Zhi, J.R. & Yue, Z. (2012) Population dynamics of Frankliniella occidentalis and Frankliniella intonsa on pepper. Southwest China Journal of Agricultural Sciences 25, 337–339.Google Scholar
Geng, S.S., Li, X.W., Zhang, J.M., Zhang, Z.J. & Lu, Y.B. Research on field application of aggregation pheromones of Frankliniella occidentalis and Frankliniella intonsa and their roles in interspecific interaction. Acta Entomologica Sinica 60, 1439–1446.Google Scholar
Greenblatt, R.E., Burkholder, W.E., Cross, J.H., Cassidy, R.F., Silverstein, R.M., Levinson, A.R. & Levinson, H.Z. (1977) Chemical basis for interspecific responses to sex pheromones of Trogoderma species (Coleoptera: Dermestidae). Journal of Chemical Ecology 3, 337–347.Google Scholar
Hamilton, J.G.C., Hall, D.R. & Kirk, W.D.J. (2005) Identification of a male-produced aggregation pheromone in the western flower thrips Frankliniella occidentalis. Journal of Chemical Ecology 31, 1369–1379.Google Scholar
Hansson, B.S. & Stensmyr, M.C. (2011) Evolution of insect olfaction. Neuron 72, 698–711.Google Scholar
Ives, A.R. (1991) Aggregation and coexistence in a carrion fly community. Ecological Monographs 61, 75–94.Google Scholar
Kirk, W.D.J. & Hamilton, J.G.C. (2004) Evidence for a male-produced sex pheromone in the western flower thrips Frankliniella occidentalis. Journal of Chemical Ecology 30, 167–174.Google Scholar
Kogel, W. & Deventer, P. (2003) Intraspecific attraction in the western flower thrips, Frankliniella occidentalis; indication for a male sex pheromone. Entomologia Experimentalis et Applicata 107, 87–89.Google Scholar
Krueger, S., Moritz, G., Lindemann, P., Radisch, D. & Tschuch, G. (2016) Male pheromones influence the mating behavior of Echinothrips americanus. Journal of Chemical Ecology 42, 294–299.Google Scholar
Lewis, T. (1997) Thrips as Crop Pests. New York, CAB International.Google Scholar
Lu, Y.B., Zhang, Z.J., Wu, Q.J., Du, Y.Z., Zhang, H.R., Yu, Y., Wang, E.D., Wang, M.H., Wang, M.Q., Tong, X.L., Lu, L.H., Tan, X.Q. & Fu, W.D. (2011) Research progress of the monitoring, forecast and sustainable management of invasive alien pest Frankliniella occidentalis in China. Chinese Journal of Applied Entomology 48, 488–496.Google Scholar
Lu, Y.B., Zhang, J.M., Li, W.D., Zhang, Z.J., Bei, Y.W., Zhang, P.J., Huang, F. & Lin, W.C. (2015) Attractants of flower thrips. China Patent, CN 104381256 A, Zhejiang Academy of Agricultural Sciences, 2015-03-04.Google Scholar
Ming, Q.-L., Yan, Y.-H. & Wang, C.-Z. (2007) Mechanisms of premating isolation between Helicoverpa armigera (Hubner) and Helicoverpa assulta (Guenee) (Lepidoptera: Noctuidae). Journal of Insect Physiology 53, 170–178.Google Scholar
Monti, L., Lalanne-Cassou, B., Lucas, P., Malosse, C. & Silvain, J.F. (1995) Differences in sex pheromone communication systems of closely related species: Spodoptera latifascia (walker) and S. descoinsi lalannecassou & silvain (Lepidoptera: Noctuidae). Journal of Chemical Ecology 21, 641–660.Google Scholar
Moore, A.J. (2012) The evolution of social signals: morphological, functional, and genetic integration of the sex pheromone in Nauphoeta cinerea. Evolution 51, 1920–1928.Google Scholar
Murai, T. (1988) Studies on the ecology and control of flower thrips, Frankliniella intonsa (Trybom). Bulletin of the Shimane Agricultural Experiment Station 23, 1–73.Google Scholar
Olaniran, O.A. (2013) The roles of pheromones of adult western flower thrips. PHD Thesis, Keele University, UK.Google Scholar
Olaniran, O.A., Sudhakar, A.V.S., Drijfhout, F.P., Dublon, I.A.N., Hall, D.R., Hamilton, J.G.C. & Kirk, W.D.J. (2013) A male-predominant cuticular hydrocarbon, 7-methyltricosane, is used as a contact pheromone in the western flower thrips Frankliniella occidentalis. Journal of Chemical Ecology 39, 559–568.Google Scholar
Paterson, H.E.H. (1985) The recognition concept of species. pp. 21–29 in Vrba, E. S. (Ed.) Species and Speciation. Pretoria, South Africa, Transvaal Museum.Google Scholar
Price, T.L., Sonenshine, D.E., Norval, R.A., Yunker, C.E. & Burridge, M.J. (1994) Pheromonal composition of two species of African Amblyomma ticks: similarities, differences and possible species-specific components. Experimental & Applied Acarology 18, 37–50.Google Scholar
Roelofs, W.L. (1995) The chemistry of sex attraction. pp. 21–29 in Eisner, T. & Meinwald, J. (Eds) Chemical Ecology: The Chemistry of Biotic Interaction. Washington, DC, National Academy Press.Google Scholar
Romani, R., Isidoro, N. & Bin, F. (2010) Antennal structures used in communication by egg parasitoids. pp. 57–96 in Consoli, F. L., Parra, J. R. P. & Zucchi, R. A.. (Eds.) Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma. Dordrecht, Netherlands, Springer.Google Scholar
Sampson, C. (2014) Management of the western flower thrips on strawberry. PHD. Thesis, Keele University, UK.Google Scholar
Sevenster, J.G. & Alphen, J.V. (1996) Aggregation and coexistence. II. A neotropical Drosophila community. Journal of Animal Ecology 65, 308–324.Google Scholar
Swarup, S., Williams, T.I. & Anholt, R.R.H. (2011) Functional dissection of odorant binding protein genes in Drosophila melanogaster. Genes Brain & Behavior 10, 648–657.Google Scholar
Symonds, M.R. & Wertheim, B. (2005) The mode of evolution of aggregation pheromones in Drosophila species. Journal of Evolutionary Biology 18, 1253–1263.Google Scholar
Teulon, D.A.J. & Nielsen, M.C. (2005) Distribution of western (glasshouse strain) and Intonsa flower thrips in New Zealand. New Zealand Plant Protection 58, 208–212.Google Scholar
Tillman, P.G., Aldrich, J.R., Khrimian, A. & Cottrell, T.E. (2010) Pheromone attraction and cross-attraction of Nezara, Acrosternum, and Euschistus spp. stink bugs (Heteroptera: Pentatomidae) in the field. Environmental Entomology 39, 610–617.Google Scholar
Toda, M.J., Kimura, M.T. & Tuno, N. (1999) Coexistence mechanisms of mycophagous drosophilids on multispecies fungal hosts: aggregation and resource partitioning. Journal of Animal Ecology 68, 794–803.Google Scholar
Ullah, M.S. & Lim, U.T. (2015) Life history characteristics of Frankliniella occidentalis and Frankliniella intonsa (Thysanoptera: Thripidae) in constant and fluctuating temperatures. Journal of Economic Entomology 108, 1000–1009.Google Scholar
Vet, L. (1999) From chemical to population ecology: infochemical use in an evolutionary context. Journal of Chemical Ecology 25, 31–49.Google Scholar
Wang, C.L., Lin, F.C., Chiu, Y.C. & Shih, H.T. (2010) Species of Frankliniella Trybom (Thysanoptera: Thripidae) from the Asian-Pacific area. Zoological Studies 49, 824–838.Google Scholar
Wang, H.-L., Zhao, C.-H. & Wang, C.-Z. (2005) Comparative study of sex pheromone composition and biosynthesis in Helicoverpa armigera, H. assulta and their hybrid. Insect Biochemistry and Molecular Biology 35, 575–583.Google Scholar
Wertheim, B., van Baalen, E.-J.A., Dicke, M. & Vet, L.E.M. (2005) Pheromone-mediated aggregation in nonsocial arthropods: an evolutionary ecological perspective. Annual Review of Entomology 50, 321–346.Google Scholar
Wojtasek, H., Hansson, B.S. & Leal, W.S. (1998) Attracted or repelled?–a matter of two neurons, one pheromone binding protein, and a chiral center. Biochemical & Biophysical Research Communications 250, 217–222.Google Scholar
Zhang, P.J., Zhu, X.Y. & Lu, Y.B. (2011) Behavioural and chemical evidence of a male-produced aggregation pheromone in the flower thrips Frankliniella intonsa. Physiological Entomology 36, 317–320.Google Scholar
Zhang, Z.K. & Lei, Z.R. (2015) Identification, expression profiling and fluorescence-based binding assays of a chemosensory protein gene from the Western flower thrips, Frankliniella occidentalis. PLoS ONE 10, 128–145.Google Scholar
Zhang, Z.K., Sheng-Yong, W.U. & Lei, Z.R. (2015) cDNA cloning, expression profiling and immunolocalization of a chemosensory protein in the western flower thrips, Frankliniella occidentalis(Thysanoptera: Thtipidae). Acta Entomologica Sinica 58, 1–14.Google Scholar
Zhang, Z.K., Wu, S.Y. & Lei, Z.R. (2016) Cloning, sequence analysis and expression profile of an odorant binding protein gene in western flower thrips (Frankliniella occidentalis). Scientia Agricultura Sinica 49, 1106–1116.Google Scholar
Zhu, X.Y., Zhang, P.J. & Lu, Y.B. (2012) Isolation and identification of the aggregation pheromone released by male adults of Frankliniella intonsa (Thysanoptera: Thripidae). Acta Entomologica Sinica 55, 376–385.Google Scholar