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Molecular characterization of closely related species in the parasitic genus Encarsia (Hymenoptera: Aphelinidae) based on the mitochondrial cytochrome oxidase subunit I gene

Published online by Cambridge University Press:  09 March 2007

M.M. Monti
Affiliation:
Istituto per la Protezione delle Piante – Sezione di Portici, Consiglio Nazionale delle Ricerche, via Università 133, 80055 Portici (NA), Italy
A.G. Nappo
Affiliation:
Istituto per la Protezione delle Piante – Sezione di Portici, Consiglio Nazionale delle Ricerche, via Università 133, 80055 Portici (NA), Italy
M. Giorgini*
Affiliation:
Istituto per la Protezione delle Piante – Sezione di Portici, Consiglio Nazionale delle Ricerche, via Università 133, 80055 Portici (NA), Italy
*
*Fax: +39 081 7758122 E-mail: [email protected]

Abstract

The genus Encarsia Förster includes parasitoid species that are effective natural enemies of whitefly and armoured scale insect agricultural pests. Within this genus, several species groups have been recognized on the basis of morphological similarity, although their monophyly appears uncertain. It is often difficult to separate morphologically similar species, and there is evidence that some species could in fact be complexes of cryptic species. Their correct identification is fundamental for biological control purposes. Recently, due to unreliability of morphological characters, molecular techniques have been investigated to identify markers that differentiate closely related species. In this study, DNA variation in an ~900 bp segment of the mitochondrial cytochrome oxidase subunit I (COI) gene was examined by both sequencing and PCR–RFLP. Two pairs of species that are difficult to distinguish morphologically were analysed: Encarsia formosa Gahan and Encarsia luteola Howard, belonging to the luteola group, and two populations of Encarsia sophia (Girault & Dodd) from Pakistan and Spain, belonging to the strenua group, recently characterized as cryptic species. High sequence divergence and species-specific restriction patterns clearly differentiate both species pairs. Parsimony analysis of the nucleotide sequences was also performed, including Encarsia hispida De Santis (luteola group) and Encarsia protransvena Viggiani (strenua group). Two monophyletic clades supporting the two groups of species considered were resolved. The results of this study support the use of the COI gene as a useful marker in separating species of Encarsia, for which morphological differences are subtle. Moreover, the COI gene appears potentially useful for understanding phylogenetic relationships in this genus.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2005

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References

Babcock, C.S., Heraty, J.M. (2000) Molecular markers distinguishing Encarsia formosa and Encarsia luteola (Hymenoptera: Aphelinidae). Annals of the Entomological Society of America 93, 738744.CrossRefGoogle Scholar
Babcock, C.S., Heraty, J.M., De Barro, P.J., Driver, F., Schmidt, S. (2001) Preliminary phylogeny of Encarsia Förster (Hymenoptera: Aphelinidae) based on morphology and 28S rDNA. Molecular Phylogenetics and Evolution 18, 306323.CrossRefGoogle Scholar
Baldanza, F. & Giorgini, M. (2001) Karyotype and NOR localization differences between Encarsia formosa Gahan and Encarsia luteola Howard (Hymenoptera: Aphelinidae). Bollettino del Laboratorio di Entomologia agraria ‘Filippo Silvestri’ 56, 3341.Google Scholar
Baldanza, F., Gaudio, L. & Viggiani, G. (1999) Cytotaxonomic studies of Encarsia Förster (Hymenoptera: Aphelinidae). Bulletin of Entomological Research 89, 209215.CrossRefGoogle Scholar
Baldanza, F., Aceto, S., Gaudio, L. & Viggiani, G. (2001) Soluble protein profile variability in four populations of Encarsia citrina (Craw) (Hymenoptera: Aphelinidae) obtained by SDS–PAGE technique. Bollettino del Laboratorio di Entomologia agraria ‘Filippo Silvestri’ 56, 514.Google Scholar
Caprio, E. & Viggiani, G. (2001) Profilo proteico di quattro specie di Encarsia (Hymenoptera: Aphelinidae). Bollettino del Laboratorio di Entomologia agraria ‘Filippo Silvestri’ 56, 1523.Google Scholar
Castineiras, A. (1995) Natural enemies of Bemisia tabaci (Homoptera: Aleyrodidae) in Cuba. Florida Entomologist 78, 538540.CrossRefGoogle Scholar
Castle, S.J., Toscano, N.C., Prabhaker, N., Henneberry, T.J., Palumbo, J.C. (2002) Field evaluation of different insecticide use strategies as resistance management and control tactics for Bemisia tabaci (Hemiptera: Aleyrodidae). Bulletin of Entomological Research 92, 449460.CrossRefGoogle ScholarPubMed
Caterino, M.S., Cho, S. & Sperling, F.A.H. (2000) The current state of insect molecular systematics: a thriving tower of Babel. Annual Review of Entomology 45, 154.CrossRefGoogle ScholarPubMed
Chermiti, B., Braham, M., Cenis, J.L., Alonso, C. & Beitia, F. (1997) Sur la presence en Tunisie des biotypes ‘B‘ et ’non B’ de Bemisia tabaci (Homoptera: Aleyrodidae) et de leurs parasitoides associes. IOBC wprs Bulletin 20 4 108113.Google Scholar
Clark, T.L., Meinke, L.J., Foster, J.E. (2001) PCR–RFLP of the mitochondrial cytochrome oxidase (subunit I) gene provides diagnostic markers for selected Diabrotica species (Coleoptera: Chrysomelidae). Bulletin of Entomological Research 91, 419427.CrossRefGoogle ScholarPubMed
Crozier, R.H., Crozier, Y.C. (1993) The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics 133, 97117.CrossRefGoogle ScholarPubMed
Danforth, B.N., Levin, P. & Packer, L. (1998) Mitochondrial DNA differentiation between two cryptic Halictus (Hymenoptera: Halictidae) species. Annals of the Entomological Society of America 91, 387391.CrossRefGoogle Scholar
De Bach, P. & Rosen, D. (1991) Biological control by natural enemies.2nd edn. Cambridge University Press Cambridge.Google Scholar
Dittrich, V., Uk, S., Ernst, G.H. (1990) Chemical control and insecticide resistance of whiteflies Whiteflies: their bionomics, pest status and management 263286 in Gerling, D. (Ed.) Intercept Ltd, Andover.Google Scholar
Evans, G.A., Polaszek, A., Bennet, F.D. (1995) The taxonomy of the Encarsia flavoscutellum species-group (Hymenoptera: Aphelinidae) parasitoids of Hormaphididae (Homoptera: Aphidoidea). Oriental Insects 29, 3345.CrossRefGoogle Scholar
Gerling, D. (1967) Bionomics of the whitefly–parasite complex associated with cotton in southern California (Homoptera: Aleyrodidae; Hymenoptera: Aphelinidae). Annals of the Entomological Society of America 60, 13061321.CrossRefGoogle Scholar
Gerling, D. (1983) Observations of the biology and interrelationships of parasites attacking the greenhouse whitefly, Trialeurodes vaporariorum (West.) in Hawaii. Proceedings of the Hawaiian Entomological Society 24, 217225.Google Scholar
Gerling, D. (1990) Whiteflies: their bionomics, pest status and management, Intercept Ltd, Andover.Google Scholar
Gerling, D. & Rivnay, T. (1984) A new species of Encarsia (Hym.: Aphelinidae) parasitizing Bemisia tabaci (Hom.: Aleyrodidae). Entomophaga 24, 439444.CrossRefGoogle Scholar
Giorgini, M. (2001) Induction of males in thelytokous populations of Encarsia meritoria Gahan and Encarsia protransvena Viggiani (Hymenoptera: Aphelinidae): a systematic tool. BioControl 46, 427438.CrossRefGoogle Scholar
Giorgini, M. & Baldanza, F. (2004) Species status of two populations of Encarsia sophia (Girault and Dodd) (Hymenoptera: Aphelinidae) native to different geographic areas. Biological Control 30, 2535.CrossRefGoogle Scholar
Goolsby, J.A., Legaspi, J.C., Legaspi, B.C. (1996) Quarantine evaluation of exotic parasitoids of the sweetpotato whitefly, Bemisia tabaci (Gennadius). Southwestern Entomologist 21, 1320.Google Scholar
Goolsby, J.A., Ciomperlik, M.A., Legaspi, B.C. Jr, Legaspi, J.C., Wendel, L.E. (1998) Laboratory and field evaluation of exotic parasitoids of Bemisia tabaci (Gennadius) (biotype ‘B’) (Homoptera: Aleyrodidae) in the Lower Rio Grande Valley of Texas. Biological Control 12, 127135.CrossRefGoogle Scholar
Hayat, M. (1998) Aphelinidae of India (Hymenoptera: Chalcidoidea): a taxonomic revision. Memoirs on Entomology International 13, 1416.Google Scholar
Hebert, P.D.N., Ratnasingam, S., deWaard, J.R. (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London Series B 270, Supplement 1, 9699CrossRefGoogle ScholarPubMed
Heinz, K.M., Parrella, M.P. (1994) Biological control of Bemisia argentifolii (Homoptera: Aleyrodidae) infesting Euphorbia pulcherrima: evaluations of releases of Encarsia luteola (Hymenoptera: Aphelinidae) and Delphastus pusillus (Coleoptera: Coccinellidae). Environmental Entomology 23, 13461353.CrossRefGoogle Scholar
Heraty, J.M. & Polaszek, A. (2000) Morphometric analysis and descriptions of selected species in the Encarsia strenua group (Hymenoptera: Aphelinidae). Journal of Hymenoptera Research 1, 142169.Google Scholar
Heraty, J.M. & Wolley, J.B. (2002) Encarsia species of the world, a searchable database. http://chalcidoids.tamu.edu/ENCARSIA/Encarsia.htmGoogle Scholar
Hoddle, M.S., Van, R.G., Sanderson, J.P. (1998) Biology and use of the whitefly parasitoid Encarsia formosa. Annual Review of Entomology 43, 645669.CrossRefGoogle ScholarPubMed
Hoelmer, K.A., Osborne, L.S., Bennett, F.D., Yokomi, R.K. (1994) Biological control of sweetpotato whitefly in Florida 101113 in Rosen, D., Bennett, F.D., Capinera, J.L. (Eds) Pest management in the subtropics. Biological control – a Florida perspective, Intercept Limited, Andover.Google Scholar
Hoy, M.A. (1994) Insect molecular genetics. An introduction to principles and applications San Diego. Academic Press, Inc, California.Google Scholar
Huang, J. & Polaszek, A. (1998) A revision of the Chinese species of Encarsia Förster (Hymenoptera: Aphelinidae): parasitoids of whiteflies, scale insects and aphids (Hemiptera: Aleyrodidae, Diaspididae, Aphidoidea). Journal of Natural History 32, 18251966.CrossRefGoogle Scholar
Kaijta, H., Made, I. & Naito, A. (1992) Parasitism of the tobacco whitefly, Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae), by Encarsia transvena (Timberlake) (Hymenoptera: Aphelinidae) in Indonesia. Applied Entomology and Zoology 27, 468470.CrossRefGoogle Scholar
Kapadia, M.N. & Puri, N. (1990) Development, relative proportions and emergence of Encarsia transvena (Timberlake) and Eretmocerus mundus Mercet, important parasitoids of Bemisia tabaci (Gennadius). Entomon 15, 235239.Google Scholar
Kirk, A.A., Lacey, L.A., Brown, J.K., Ciomperlik, M.A., Goolsby, J.A., Vacek, D.C., Wendel, L.E. & Napompeth, B. (2000) Variation in the Bemisia tabaci s.l. species complex (Hemiptera: Aleyrodidae) and its natural enemies leading to successful biological control of Bemisia biotype B in the USA. Bulletin of Entomological Research 90, 317327.CrossRefGoogle ScholarPubMed
Kruse, J.J. & Sperling, F.A.H. (2001) Molecular phylogeny within and between species of the Archips argyrospila complex (Lepidoptera: Tortricidae). Annals of the Entomological Society of America 94, 166173.CrossRefGoogle Scholar
Kumar, S., Tamura, K., Jacobsen, I.B. & Nei, M. (2001) MEGA 2: molecular evolution genetic analysis software. Bioinformatics 17, 12441245.CrossRefGoogle ScholarPubMed
Legaspi, J.C., Legaspi, B.C. Jr, Carruthers, R.I., Goolsby, J., Jones, W.A., Kirk, A.A., Moomaw, C., Poprawski, T.J., Ruiz, R.A., Talekar, N.S., Vacek, D. (1996) Foreign exploration for natural enemies of Bemisia tabaci from Southeast Asia. Subtropical Plant Science 48, 4348.Google Scholar
Lin, C.P., Wood, T.K. (2002) Molecular phylogeny of the North American Enchenopa binotata (Homoptera: Membracidae) species complex. Annals of the Entomological Society of America 95, 162171.CrossRefGoogle Scholar
Linton, J.M., Mordue, A.J., Cruickshank, R.H., Meiswinkel, R., Mellor, P.S., Dallas, J.F. (2002) Phylogenetic analysis of the mitochondrial cytochrome oxidase subunit I gene of five species of the Culicoides imicola species complex. Medical and Veterinary Entomology 16, 139146.CrossRefGoogle Scholar
Loxdale, H.D. & Lushai, G. (1998) Molecular markers in entomology. Bulletin of Entomological Research 88, 577600.CrossRefGoogle Scholar
Manzari, S., Polaszek, A., Belshaw, R. & Quicke, D.L.J. (2002) Morphometric and molecular analysis of the Encarsia inaron species-group (Hymenoptera: Aphelinidae), parasitoids of whiteflies (Hemiptera: Aleyrodidae). Bulletin of Entomological Research 92, 165175.CrossRefGoogle ScholarPubMed
McAuslane, H.J., Johnson, F.A., Knauft, D.A., Colvin, D.L. (1993) Seasonal abundance and within-plant distribution of parasitoids of Bemisia tabaci (Homoptera: Aleyrodidae) in peanuts. Environmental Entomology 22, 10431050.CrossRefGoogle Scholar
Noyes, J.S. (2002) Interactive catalogue of world Chalcidoidea. 2nd edn. Taxapad and The Natural History Museum, London.Google Scholar
Onillon, J.C. & Maignet, P. (2000) Les parasitoides du biotype ‘B’ de Bemisia tabaci Gennadius (Homoptera: Aleyrodidae). Que peut-on en attendre pour la controle biologique de ce ravageur. IOBC wprs Bulletin 23 1 101107.Google Scholar
Osborne, L.S., Hoelmer, K. & Gerling, D. (1990) Prospects for biological control of Bemisia tabaci. IOBC wprs Bulletin 13 5 153160.Google Scholar
Otranto, D., Colwell, D.D., Traversa, D., Stevens, J.R. (2003) Species identification of Hypoderma affecting domestic and wild ruminants by morphological and molecular characterization. Medical and Veterinary Entomology 17, 316325.CrossRefGoogle ScholarPubMed
Ozawa, A., Satou, M. & Masuda, T. (1992) Parasitism of an indigenous parasitoid Encarsia transvena (Timberlake), on the sweetpotato whitefly, Bemisia tabaci Gennadius, in sweetpotato fields. Proceedings of the Kanto-Tosan Plant Protection Society 39, 199200.Google Scholar
Pedata, P.A. & Polaszek, A. (2003) A revision of the Encarsia longifasciata species group (Hymenoptera: Aphelinidae). Systematic Entomology 28, 361374.CrossRefGoogle Scholar
Pedata, P.A., Giorgini, M. & Viggiani, G. (1994) Variazioni morfologiche in Encarsia formosa Gahan (Hymenoptera: Aphelinidae) in relazione agli ospiti. in Atti XVII Congresso Nazionale Italiano di Entomologia, Udine, Italy. 347350Arti Grafiche Friulane, Udine.Google Scholar
Polaszek, A. (1991) Egg parasitism in Aphelinidae (Hymenoptera: Chalcidoidea) with special reference to Centrodora and Encarsia species. Bulletin of Entomological Research 81, 97106.CrossRefGoogle Scholar
Polaszek, A., Evans, G.A., Bennet, F.D. (1992) Encarsia parasitoids of Bemisia tabaci (Hymenoptera: Aphelinidae, Homoptera: Aleyrodidae): a preliminary guide to identification. Bulletin of Entomological Research 82, 375392.CrossRefGoogle Scholar
Polaszek, A., Abd-Rabou, S. & Huang, J. (1999) The Egyptian species of Encarsia (Hymenoptera: Aphelinidae): a preliminary review. Zoologische Mededelingen Leiden 73, 161163.Google Scholar
Polaszek, A., Manzari, S. & Quicke, D.L.J. (2004) Morphological and molecular taxonomic analysis of the Encarsia meritoria species-complex (Hymenoptera, Aphelinidae), parasitoids of whiteflies (Hemiptera, Aleyrodidae) of economic importance. Zoologica Scripta 33, 403421.CrossRefGoogle Scholar
Prabhaker, N., Toscano, N.C., Castle, S.J., Henneberry, T.J. (1997) Selection for imidacloprid resistance in silverleaf whiteflies from the Imperial Valley and development of a hydroponic bioassay for resistance monitoring. Pesticide Science 51, 419428.3.0.CO;2-L>CrossRefGoogle Scholar
Riley, D.G., Ciomperlik, M.A. (1997) Regional population dynamics of whitefly (Homoptera: Aleyrodidae) and associated parasitoids (Hymenoptera: Aphelinidae). Environmental Entomology 26, 10491055.CrossRefGoogle Scholar
Rivnay, T. & Gerling, D. (1987) Aphelinidae parasitoids (Hymenoptera: Chalcidoidea) of whiteflies (Hemiptera: Aleyrodidae) in Israel, with description of three new species. Entomophaga 32, 463475.CrossRefGoogle Scholar
Roehrdanz, R.L., Reed, D.K., Burton, R.L. (1993) Use of polymerase chain reaction and arbitrary primers to distinguish laboratory-raised colonies of parasitic Hymenoptera. Biological Control 3, 199206.CrossRefGoogle Scholar
Schauff, M.E., Evans, G.A., Heraty, J.M. (1996) A pictorial guide to the species of Encarsia (Hymenoptera: Aphelinidae) parasitic on whiteflies (Homoptera: Aleyrodidae) in North America. Proceedings of the Entomological Society of Washington 98, 135.Google Scholar
Schmidt, S., Naumann, I.D., De Barro, P.J. (2001) Encarsia species (Hymenoptera: Aphelinidae) of Australia and the Pacific Islands attacking Bemisia tabaci and Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) – a pictorial key and description of four new species. Bulletin of Entomological Research 91, 369387.CrossRefGoogle ScholarPubMed
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651701.CrossRefGoogle Scholar
Sperling, F.A., Hickey, D.A. (1994) Mitochondrial DNA sequence variation in the spruce budworm species complex (Choristoneura: Lepidoptera). Molecular Biology and Evolution 11, 656665.Google ScholarPubMed
Stansly, P.A., Schuster, D.J., Liu, T.X. (1997) Apparent parasitism of Bemisia argentifolii (Homoptera: Aleyrodidae) by Aphelinidae (Hymenoptera) on vegetable crops and associated weeds in South Florida. Biological Control 9, 4957.CrossRefGoogle Scholar
Stauffer, C. (1997) A molecular method for differentiating sibling species within the genus Ips. pp. 8791in Gré goire, A.M., Liebhold, F.M., Stephen, K.R., Day, S.M., Salom, J.C. (Eds) Proceedings: Integrating cultural tactics into the management of bark beetle and reforestation pests. USDA Forest Service General Technical Report NE-236.Google Scholar
Szalanski, A.L., Roeherdanz, R.L., Taylor, D.B. (2000) Genetic relationship among Diabrotica species (Coleoptera: Chrysomelidae) based on rDNA and mtDNA sequences. Florida Entomologist 83, 262267.CrossRefGoogle Scholar
van Lenteren, J.C., Drost, Y.C., van, H.J.W, Posthuma-Doodeman, C.J.A.M. (1997) Aphelinid parasitoids as sustainable biological control agents in greenhouses. Journal of Applied Entomology 121, 473485.CrossRefGoogle Scholar
van Meer, M.M.M., van Kan, F.J.P.M., Breeuwer, J.A.J. & Stouthamer, R. (1995) Identification of symbionts associated with parthenogenesis in Encarsia formosa (Hymenoptera: Aphelinidae) and Diplolepis rosae (Hymenoptera: Cynipidae). pp. 8186 in Proceedings of the Section of Experimental and Applied Entomology NEV Amsterdam 6.Google Scholar
Viggiani, G. & Mazzone, P. (1979) Contributi alla conoscenza morfo-biologica delle specie del complesso Encarsia Foerster- Prospaltella Ashmead (Hym. Aphelinidae). 1. Un commento sull'attuale stato, con proposte sinonimiche e descrizione di Encarsia silvestri n. sp., parassita di Bemisia citricola Gom. Men. (Hom. Aleyrodidae). Bollettino del Laboratorio di Entomologia agraria ‘Filippo Silvestri’ 44, 121179.Google Scholar
Vogler, A.P., DeSalle, R., Assman, T., Knisley, C.B., Shultz, T.D. (1993) Molecular population genetics of the endangered tiger beetle, Cicindela dorsalis (Coleoptera: Cicindellidae). Annals of the Entomological Society of America 86, 142152.CrossRefGoogle Scholar
Zchori-Fein, E., Roush, R.T., Hunter, M.S. (1992) Male production induced by antibiotic treatment in Encarsia formosa (Hymenoptera: Aphelinidae), an asexual species. Experientia 48, 102105.CrossRefGoogle Scholar
Zhang, D.X., Hewitt, G.M. (1996) Assessment on the universality and utility of a set of conserved mitochondrial COI primers in insects. Insect Molecular Biology 6, 143150.CrossRefGoogle Scholar