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Resolution of three cryptic agricultural pests (Ceratitis fasciventris, C. anonae, C. rosa, Diptera: Tephritidae) using cuticular hydrocarbon profiling

Published online by Cambridge University Press:  04 June 2014

L. Vaníčková ,
M. Virgilio ,
A. Tomčala ,
R. Břízová ,
S. Ekesi ,
M. Hoskovec ,
B. Kalinová ,
R. R. Do Nascimento  and
M. De Meyer
L. Vaníčková*
Affiliation:
Institute of Chemistry and Biotechnology, Federal University of Alagoas, BR 104 Norte Km 14, 57072-970 Maceió, Alagoas, Brazil Institute of Organic Chemistry and Biochemistry of the ASCR, Flemingovo nám. 2, CZ-166 10 Prague 6, Czech Republic
M. Virgilio
Affiliation:
Royal Museum for Central Africa, Leuvensesteenweg 13, B-3080 Tervuren, Belgium
A. Tomčala
Affiliation:
Institute of Organic Chemistry and Biochemistry of the ASCR, Flemingovo nám. 2, CZ-166 10 Prague 6, Czech Republic
R. Břízová
Affiliation:
Institute of Organic Chemistry and Biochemistry of the ASCR, Flemingovo nám. 2, CZ-166 10 Prague 6, Czech Republic Institute of Chemical Technology in Prague, Technická 5, CZ-166 28 Prague 6, Czech Republic
S. Ekesi
Affiliation:
International Centre of Insect Physiology and Ecology, PO Box 30772-00100 GPO, Nairobi, Kenya
M. Hoskovec
Affiliation:
Institute of Organic Chemistry and Biochemistry of the ASCR, Flemingovo nám. 2, CZ-166 10 Prague 6, Czech Republic
B. Kalinová
Affiliation:
Institute of Organic Chemistry and Biochemistry of the ASCR, Flemingovo nám. 2, CZ-166 10 Prague 6, Czech Republic
R. R. Do Nascimento
Affiliation:
Institute of Chemistry and Biotechnology, Federal University of Alagoas, BR 104 Norte Km 14, 57072-970 Maceió, Alagoas, Brazil
M. De Meyer
Affiliation:
Royal Museum for Central Africa, Leuvensesteenweg 13, B-3080 Tervuren, Belgium
*
*Author for correspondence E-mail: luci.vanickova@gmail.com
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Abstract

Discrimination of particular species within the species complexes of tephritid fruit flies is a very challenging task. In this fruit-fly family, several complexes of cryptic species have been reported, including the African cryptic species complex (FAR complex). Cuticular hydrocarbons (CHCs) appear to be an excellent tool for chemotaxonomical discrimination of these cryptic species. In the present study, CHC profiles have been used to discriminate among three important agricultural pests from the FAR complex, Ceratitis fasciventris, Ceratitis anonae and Ceratitis rosa. Hexane body surface extracts of mature males and females were analyzed by two-dimensional gas chromatography with mass spectrometric detection and differences in CHC profiles between species and sexes tested through multivariate statistics and compared with species identification by means of microsatellite markers. Quantitative as well as qualitative CHC profile differences between sexes and species are reported. The CHC profiles consisted of a mixture of linear, internally methyl-branched and mono-, di- and tri-unsaturated alkanes. Twelve compounds were pinpointed as potential chemotaxonomical markers. The present study shows that presence or absence of particular CHCs might be used in the chemical diagnosis of the FAR complex. Moreover, our results represent an important first step in the development of a useful chemotaxonomic tool for cryptic species identification of these important agricultural pests.

Keywords

cryptic species complexgenus Ceratitiscuticular hydrocarbonspolymorphic microsatellite locichemotaxonomy
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 5 , October 2014 , pp. 631 - 638
Copyright
Copyright © Cambridge University Press 2014 

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References

Anderson, M.J. (2001) A new method for non-parametric multivariate analysis of variance. Australian Journal of Ecology 26, 32–46.Google Scholar
Anderson, M.J. (2003) PCO: a FORTRAN Computer Program for Principal Coordinate Analysis. New Zealand, Department of Statistics, University of Auckland.Google Scholar
Anderson, C.M., Aparicio, G.J., Atangana, A.R., Beaulieu, J., Bruford, M.W., Cain, F., Campos, T., Cariani, A., Carvalho, M.A., Chen, N., Chen, P.P., Clamens, A.L., Clark, A.M., Coeur D'Acier, A., Connolly, P., Cordero-Rivera, A., Coughlan, J.P., Cross, T.S. et al. (2010) Permanent genetic resources added to molecular ecology resources database 1 December 2009–31 January 2010. Molecular Ecology Resources 10, 576–579.Google ScholarPubMed
Baliraine, F.N., Bonizzoni, M., Guglielmino, C.R., Osir, E.O., Lux, S.A., Mulaa, F.J., Gomulski, L.M., Zheng, L., Quilici, S., Gasperi, G. & Malacrida, A.R. (2004) Population genetics of the potentially invasive African fruit fly species, Ceratitis rosa and Ceratitis fasciventris (Diptera: Tephritidae). Molecular Ecology 13, 683–695.CrossRefGoogle Scholar
Barr, N.B. & McPheron, B.A. (2006) Molecular phylogenetics of the genus Ceratitis (Diptera: Tephritidae). Molecular Phylogenetics and Evolution 38, 216–230.CrossRefGoogle Scholar
Besansky, N.J. (1999) Complexities in the analysis of cryptic taxa within the genus Anopheles. Parassitologia 41, 97–100.Google ScholarPubMed
Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winkler, K., Ingram, K.K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22, 148–155.CrossRefGoogle ScholarPubMed
Blomquist, G.J. & Bagnères, A.G. (2010) Insect Hydrocarbons Biology, Biochemistry, and Chemical Ecology. New York, Cambridge University Press.CrossRefGoogle Scholar
Caputo, B., Dani, F.R., Horne, G.L., Petrarca, V., Turillazzi, S., Coluzzi, M., Priestman, A.A. & della Torre, A. (2005) Identification and composition of cuticular hydrocarbons of the major Afrotropical malaria vector Anopheles gambiae s.s. (Diptera: Culicidae): analysis of sexual dimorphism and age-related changes. Journal of Mass Spectrometry 40, 1595–1604.CrossRefGoogle ScholarPubMed
Carlson, D.A. & Yocom, S.R. (1986) Cuticular hydrocarbons from six species of tephritid fruit flies. Archives of Insect Biochemistry and Physiology 3, 397–412.CrossRefGoogle Scholar
Carlson, D.A., Roan, C.S., Yost, R.A. & Hector, J. (1989) Dimethyl disulfide derivatives of long chain alkenes, alkadienes, and alkatrienes for gas chromatography/mass spectrometry. Analytical Chemistry 61, 1564–1571.CrossRefGoogle Scholar
Carlson, D.A., Bernier, U.R. & Sutton, B.D. (1998) Elution patterns from capillary GC for methyl-branched alkanes. Journal of Chemical Ecology 11, 1845–1865.CrossRefGoogle Scholar
Chapman, R.F., Espelie, K.E. & Sword, G.A. (1995) Use of cuticular lipids in grasshopper taxonomy: a study of variation in Schistocerca shoshone (Thomas). Biochemical Systematics and Ecology 23, 383–398.CrossRefGoogle Scholar
Clarke, K.R. (1993) Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18, 117–143.CrossRefGoogle Scholar
Copren, K.A., Nelson, L.J., Vargo, E.L. & Haverty, M.I. (2005) Phylogenetic analyses of mtDNA sequences corroborate taxonomic designations based on cuticular hydrocarbons in subterranean termites. Molecular Phylogenetics and Evolution 35, 689–700.CrossRefGoogle ScholarPubMed
Curtis, S., Sztepanacz, J.L., White, B.E., Dyer, K.A., Rundle, H.D., & Mayer, P. (2013) Epicuticular compounds of Drosophila subquinaria and D. recens: identification, quantification, and their role in female mate choice. Journal of Chemical Ecology 39, 579–590.CrossRefGoogle Scholar
Dahbi, A., Hefetz, A. & Lenoir, A. (2008) Chemotaxonomy of some Cataglyphis ants from Morocco and Burkina Faso. Biochemical Systematics and Ecology 36, 564–572.CrossRefGoogle Scholar
De Meyer, M. (2001) On the identity of the Natal fruit fly Ceratitis rosa Karsch (Diptera, Tephritidae). Bulletin de l'Institut Royal des Sciences Naturelles de Belgique Entomologie 71, 55–62.Google Scholar
De Meyer, M. & Freidberg, A. (2006) Revision of the subgenus Ceratitis (Pterandrus) Bezzi (Diptera: Tephritidae). In Freidberg, A. (Ed.) Biotaxonomy of Tephritoidea. Israel Journal of Entomology 35/36, 197–315.Google Scholar
De Meyer, M., Robertson, M., Peterson, T. & Mansell, M. (2008) Climatic modeling for the med fly and Natal fruit fly. Journal of Biogeography 35, 270–281.CrossRefGoogle Scholar
Dyck, V.A., Hendrichs, J. & Robinson, A.S. (2005) Steril Insect Technique Principles and Practice in Area-Wide Integrated Pest Management Dordrecht. Springer.Google Scholar
Everaerts, C., Maekawa, K., Farine, J.P., Shimada, K., Luykx, P., Brossut, R. & Nalepa, C.A. (2008) The Cryptocercus punctulatus species complex (Dictyoptera: Cryptocercidae) in the eastern United States: comparison of cuticular hydrocarbons, chromosome number, and DNA sequences. Molecular Phylogenetics and Evolution 47, 950–959.CrossRefGoogle ScholarPubMed
Everaerts, C., Farine, J.-P., Cobb, M. & Ferveur, J.-F. (2010) Drosophila cuticular hydrocarbons revisited: mating status alters cuticular profiles. PLoS ONE 5, 9607.CrossRefGoogle ScholarPubMed
Fletcher, B.S. (1989) Life history strategies of tephritid fruit flies. pp. 195–208in Robinson, A.S. & Hooper, G.H. (Eds) Fruit Flies: Their Biology, Natural Enemies and Control. Amsterdam, Netherlands, Elsevier.Google Scholar
Garros, C., Van Bortel, W., Trung, H.D., Coosemans, M. & Manguin, S. (2006) Review of the minimus complex of Anopheles, main malaria vector in Southeast Asia: from taxonomic issues to vector control strategies. Tropical Medicine and International Health 11, 102–114.CrossRefGoogle ScholarPubMed
Geiselhardt, S., Otte, T. & Hilker, M. (2009) The role of cuticular hydrocarbons in male mating behavior of the mustard leaf beetle, Phaedon cochleariae (F.). Journal of Chemical Ecology 35, 1162–1171.CrossRefGoogle ScholarPubMed
Gemeno, C., Laserna, N., Riba, M., Valls, J., Castañé, C. & Alomar, O. (2012) Cuticular hydrocarbons discriminate cryptic Macrolophus species (Hemiptera: Miridae). Bulletin of Entomological Research 102, 624–631.CrossRefGoogle ScholarPubMed
Gibbs, A.G. (2011) Thermodynamics of cuticular transpiration. Journal of Insect Physiology 57, 1066–1069.CrossRefGoogle ScholarPubMed
Goh, S.H., Ooi, K.E., Chuah, C.H., Yong, H.S., Khoo, S.G. & Ong, S.H. (1993) Cuticular hydrocarbons from two species of Malaysian Bactrocera fruit flies. Biochemical Systematics and Ecology 21, 215–226.CrossRefGoogle Scholar
Gozansky, T.K., Soroker, V. & Hefetz, A. (1997) The biosynthesis of Dufour's gland constituents of the honeybee (Apis mellifera). Invertebrate Neuroscience 3, 239–243.CrossRefGoogle Scholar
Guillem, R.M., Drijfhout, F.P. & Martin, S.J. (2012) Using chemo-taxonomy of host ants to help conserve the large blue butterfly. Biological Conservation 148, 39–43.CrossRefGoogle Scholar
Havens, J.A. & Etges, W.J. (2013) Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. IX. Host plant and population specific epicuticular hydrocarbon expression influences mate choice and sexual selection. Journal of Evolutionary Biology 26, 562–576.CrossRefGoogle ScholarPubMed
Haverty, M.I., Nelson, L.J. & Page, M. (1990) Cuticular hydrocarbons of four populations of Coptotermes formosanus Shikari in the United States: similarities and origins of introductions. Journal of Chemical Ecology 16, 1635–1647.CrossRefGoogle Scholar
Haverty, M.I., Woodrow, R.J., Nelson, L.J. & Grace, J.K. (2000) Cuticular hydrocarbons of termites of the Hawaiian Islands. Journal of Chemical Ecology 26, 1167–1191.CrossRefGoogle Scholar
Horne, G.L. & Priestman, A.A. (2002) The chemical characterization of the epicuticular hydrocarbons of Aedes aegypti (Diptera: Culicidae). Bulletin of Entomological Research 92, 287–294.CrossRefGoogle ScholarPubMed
Howard, R.W. & Blomquist, G.J. (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annual Review of Entomology 50, 371–393.CrossRefGoogle ScholarPubMed
Jennings, J.H., Etges, W.J., Schmitt, T. & Hoikkala, A. (2014) Cuticular hydrocarbons of Drosophila montana: geographic variation, sexual dimorphism and potential roles as pheromones. Journal of Insect Physiology 61, 16–24.CrossRefGoogle ScholarPubMed
Jombart, T. (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405.CrossRefGoogle Scholar
Kather, R. & Martin, S.J. (2012) Cuticular hydrocarbon profiles as a taxonomic tool: advantages, limitations and technical aspects. Physiological Entomology 37, 25–32.CrossRefGoogle Scholar
Lahav, S., Soroker, V., Hefetz, A. & Vander Meer, R.K. (1999) Direct behavioral evidence for hydrocarbons as ant recognition discriminators. Naturwissenschaften 86, 246–249.CrossRefGoogle Scholar
Lavine, B.K., Carlson, D.A. & Calkins, C.O. (1992) Classification of tephritid fruit fly larvae by gas chromatography/pattern recognition techniques. Microchemical Journal 45, 50–57.CrossRefGoogle Scholar
Lockey, K.H. (1991) Insect hydrocarbon classes: implications for chemotaxonomy. Insect Biochemistry 21, 91–97.CrossRefGoogle Scholar
Lucas, C., Fresneau, D., Kolmer, K., Heinze, J., Delabie, J.H.C. & Pho, D.B. (2002) A multidisciplinary approach to discriminating different taxa in the species complex Pachycondyla villosa (Formicidae). Biological Journal of the Linnean Society 75, 249–259.CrossRefGoogle Scholar
Martin, S. & Drijfhout, F. (2009) A review of ant cuticular hydrocarbons. Journal of Chemical Ecology 35, 1151–1161.CrossRefGoogle ScholarPubMed
Martin, S.J., Helantera, H. & Drijfhout, F.P. (2008) Evolution of species-specific cuticular hydrocarbon patterns in Formica ants. Biological Journal of the Linnean Society 95, 131–140.CrossRefGoogle Scholar
Oliveira, C., Manfrin, M.H., Sene, F., Jackson, L.L. & Etges, W.J. (2011) Variations on a theme: diversification of cuticular hydrocarbons in a clade of cactophilic Drosophila. BMC Evolutionary Biology 11, 1–19.CrossRefGoogle Scholar
Paterson, H.E.H. (1991) The recognition of cryptic species among economically important insects. pp. 1–10in Zalucki, M.P. (Ed.) Heliothis: Research Methods and Prospects. Springer.Google Scholar
Pokorny, T., Lunau, K., Quezada-Euan, J.J.G. & Eltz, T. (2014) Cuticular hydrocarbons distinguish cryptic sibling species in Euglossa orchid bees. Apidologie 45, 276–283.CrossRefGoogle Scholar
Pomonis, J.G., Fatland, C.F., Nelson, D.R. & Zaylskie, R.G. (1978) Insect hydrocarbons corroboration of structure by synthesis and mass spectrometry of mono- and dimethylalkanes. Journal of Chemical Ecology 4, 27–39.CrossRefGoogle Scholar
Rouault, J.D., Marican, C., Wicker-Thomas, C. & Jallon, J.M. (2004) Relations between cuticular hydrocarbon (HC) polymorphism, resistance against desiccation and breeding temperature; a model for HC evolution in D. melanogaster and D. simulans. Genetica 120, 195–212.CrossRefGoogle Scholar
Schlick-Steiner, B.C., Steiner, F.M., Moder, K., Seifert, B., Sanetra, M., Dyreson, E., Stauffer, C. & Christian, E. (2006) A multidisciplinary approach reveals cryptic diversity in western palearctic tetramorium ants (Hymenoptera: Formicidae). Molecular Phylogenetics and Evolution 40, 259–273.CrossRefGoogle ScholarPubMed
Shirangi, T.R., Dufour, H.D., Williams, T.M. & Carroll, S.B. (2009) Rapid evolution of sex pheromone-producing enzyme expression in Drosophila. PLoS Biology 7, e1000168.CrossRefGoogle ScholarPubMed
Steinke, D., Virgilio, M., Jordaens, K., Breman, F.C., Backeljau, T. & De Meyer, M. (2012) Identifying insects with incomplete DNA barcode libraries, African fruit flies (Diptera: Tephritidae) as a test case. PLoS ONE 7, e31581.Google Scholar
Suarez, E., Nguyen, H.P., Ortiz, I.P., Lee, K.J., Kim, S.B., Krzywinski, J. & Schug, K.A. (2011) Matrix-assisted laser desorption/ionization-mass spectrometry of cuticular lipid profiles can differentiate sex, age, and mating status of Anopheles gambiae mosquitoes. Analytica Chimica Acta 706, 157–163.CrossRefGoogle ScholarPubMed
Sutton, B.D. & Carlson, B.D. (1993) Interspecific variation in tephritid fruit fly larvae surface hydrocarbons. Archives of Insect Biochemistry and Physiology 23, 53–65.CrossRefGoogle Scholar
Sutton, B.D. & Steck, G.J. (1994) Discrimination of Carribean and Mediterranean fruit fly larvae (Diptera:Tephritidae) by cuticular hydrocarbon analysis. Florida Entomologist 77, 231–237.CrossRefGoogle Scholar
Takahashi, A., Fujiwara-Tsujii, N., Yamaoka, R., Itoh, M., Ozaki, M. & Takano-Shimizu, T. (2012) Cuticular hydrocarbon content that affects male mate preference of Drosophila melanogaster from West Africa. International Journal of Evolutionary Biology 2012, 1–10.Google Scholar
Thomas, M.L. & Simmons, L.W. (2008) Sexual dimorphism in cuticular hydrocarbons of the Australian field cricket Teleogryllus oceanicus (Orthoptera: Gryllidae). Journal of Insect Physiology 54, 1081–1089.CrossRefGoogle ScholarPubMed
Van Den Dool, H. & Kratz, P.D. (1963) A generalization of the retention index system including linear temperature programmed gas–liquid partition chromatography. Journal of Chromatograpy A 11, 463–471.CrossRefGoogle Scholar
Vaníčková, L. (2012) Chemical Ecology of Fruit Flies: Genera Ceratitis and Anastrepha. Prague, Department of Chemistry of Natural Compounds, Institute of Chemical Technology.Google Scholar
Vaníčková, L., Svatoš, A., Kroiss, J., Kaltenpoth, M., Nascimento, R.R., Hoskovec, M., Břízová, R. & Kalinová, B. (2012) Cuticular hydrocarbons of the South American fruit fly Anastrepha fraterculus: variability with sex and age. Journal of Chemical Ecology 38, 1133–1142.CrossRefGoogle ScholarPubMed
Virgilio, M., Backeljau, T. & De Meyer, M. (2007 a) FAR complex and barcoding. p. 142 in Proceedings of the Second International Barcode of Life Conference, Taipei, Taiwan.Google Scholar
Virgilio, M., Backeljau, T. & De Meyer, M. (2007 b) Incongruence of phylogenetic signals and shared polymorphisms prevent the molecular characterization of the Ceratitis fasciventris, C. anonae, C. rosa complex (Diptera: Tephritidae). p. 520 in Proceedings of the 11th Congress of the European Society for Evolutionary Biology, Upsalla, Sweden.Google Scholar
Virgilio, M., Backeljau, T., Barr, N. & Meyer, M.D. (2008) Molecular evaluation of nominal species in the Ceratitis fasciventris, C. anonae, C. rosa complex (Diptera: Tephritidae). Molecular Phylogenetics and Evolution 48, 270–280.CrossRefGoogle Scholar
Virgilio, M., Backeljau, T., Nevado, B. & De Meyer, M. (2010) Comparative performances of DNA barcoding across insect orders. BMC Bioinformatics 11, 206–216.CrossRefGoogle ScholarPubMed
Virgilio, M., Jordaens, K., Breman, F.C., Backeljau, T. & De Meyer, M. (2012) Identifying insects with incomplete DNA barcode libraries, African fruit flies (Diptera: Tephritidae) as a test case. PLoS ONE 7, e31581.CrossRefGoogle ScholarPubMed
Virgilio, M., Delatte, H., Quilici, S., Backeljau, T. & De Meyer, M. (2013) Cryptic diversity and gene flow among three African agricultural pests: Ceratitis rosa, Ceratitis fasciventris and Ceratitis anonae (Diptera, Tephritidae). Molecular Ecology 22, 2526–2539.CrossRefGoogle Scholar
Wakayama, E.J., Dillwith, J.W. & Blomquist, G.J. (1985) Occurrence and metabolism of arachidonic acid in the housefly, Musca domestica (L.). Insect Biochemistry 15, 367–374.CrossRefGoogle Scholar
White, I.M. & Elson-Harris, M. (1992) Fruit Flies of Economic Significance: Their Identification and Bionomics. Oxon, UK, CAB International and The Australian Center for Agricultural Research Canberra, Australia, p. 601.CrossRefGoogle Scholar
Wicker-Thomas, C. (2007) Pheromonal communication involved in courtship behavior in Diptera. Journal of Insect Physiology 53, 1089–1100.CrossRefGoogle ScholarPubMed
Ye, G., Li, K., Zhu, J., Zhu, G. & Hu, C. (2007) Cuticular hydrocarbon composition in pupal exuviae for taxonomic differentiation of six necrophagous flies. Journal of Medical Entomology 44, 450–456.CrossRefGoogle ScholarPubMed
Yuval, B. & Hendrichs, J. (2001) Behavioral of flies in the genus Ceratitis (Dacinae: Ceratitidini). in Aluja, M. & Norrbom, A.L. (Eds) Fruit Flies (Tephritidae) Phylogeny and Evolution of Behavior. Boca Raton, FL, CRC Press.Google Scholar