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Molecular methods for assessing insect parasitism

Published online by Cambridge University Press:  09 March 2007

M.H. Greenstone
M.H. Greenstone*
Affiliation:
USDA-Agricultural Research Service, Insect Biocontrol Laboratory, Room 214, Building 011A, BARC-West, Beltsville, MD 20705, USA
*
*Fax: 301 504 5104 E-mail: greenstm@ba.ars.usda.gov
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Abstract

Determining insect parasitism rates is problematic due to the small size and lack of useful distinguishing morphological characters of many parasitoid taxa. To solve this problem, entomologists have employed one of four general methods to detect parasitoid protein or nucleic acid markers: serological assay; random amplified polymorphic DNA–polymerase chain reaction “RAPD-PCR” allozyme electrophoresis; or specific PCR. Serological methods, especially with monoclonal antibodies, are unrivalled for specificity, enabling discrimination at the stage as well as species level. However, they have not found favour with many workers, possibly due to complexity and expense. RAPD–PCR has been widely used, but can only be recommended for restricted applications because of its poor reproducibility. Allozyme electrophoresis provides reproducible detection and discrimination of closely related species. Specific-PCR is highly specific and reproducible, and also has the shortest latency for detection, usually 24 h or less after parasitization. The substantial existing literature on allozyme electrophoresis and specific PCR is used to support recommendations on what are apt to be fruitful enzyme systems or genomic regions for detecting and discriminating parasitoids in untried parasitoid–host assemblages.

Keywords

allozyme electrophoresisisozymespecific PCRparasitoidsRAPD–PCR
Type
Review Article
Information
Bulletin of Entomological Research , Volume 96 , Issue 1 , February 2006 , pp. 1 - 13
Copyright
Copyright © Cambridge University Press 2006

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References

Agustí, N., Bourguet, D., Spataro, T., Delos, M., Eychenne, N., Folcher, L. & Arditi, R. (2005) Detection, identification, and geographical distribution of European corn borer larval parasitoids using molecular markers. Molecular Ecology 14, 3267–3274.CrossRefGoogle ScholarPubMed
Allemand, R., Lematre, C., Frey, F., Bouletreau, M., Vavre, F., Nordlander, G., van Alphen, J. & Carton, Y. (2002) Phylogeny of six African Leptopilina species (Hymenoptera: Cynipoidea, Figitidae), parasitoids of Drosophila, with description of three new species. Annales de la Société Entomologique de France 38, 319–332.CrossRefGoogle Scholar
Allen, W.R., Trimble, R.M. & Vickers, P.M. (1992) ELISA used without trituration to detect larvae of Phyllonorycter blancardella (Leidoptera: Gracillariidae) parasitized by Pholetesor ornigis (Hymeoptera: Braconidae). Environmental Entomology 21, 50–56.CrossRefGoogle Scholar
Alvarez, J.M. & Hoy, M.A. (2002) Evaluation of the ribosomal ITS2 DA sequences in separating closely related populations of the parasitoid Ageniaspis (Hymenoptera: Encyrtidae). Annals of the Entomological Society of America 95, 250–256.CrossRefGoogle Scholar
Amornsak, W., Gordh, G. & Graham, G. (1998) Detecting parasitized eggs with polymerase chain reaction and DNA sequence of Trichogramma australicum Girault (Hymenoptera: Trichogrammatidae). Australian Journal of Entomology 37, 174–179.CrossRefGoogle Scholar
Antolin, M.F., Guertin, D.S. & Petersen, J.J. (1996) The origin of gregarious Muscidifurax (Hymenoptera: Pteromalidae) in North America: an analysis using molecular markers. Biological Control 6, 76–82.CrossRefGoogle Scholar
Ashfaq, M., Braun, L., Hegedus, D. & Erlandson, M. (2004) Estimating parasitism levels in Lygus spp. (Hemiptera: Miridae) field populations using standard and molecular techniques. Biocontrol Science and Technology 14, 731–735.CrossRefGoogle Scholar
Atanassova, P., Brookes, C.P., Loxdale, H.D. & Powell, L. (1998) Electrophoretic study of five aphid parasitoid species of the genus Aphidius (Hymenoptera: Braconidae), including evidence for reproductively isolated sympatric populations and cryptic species. Bulletin of Entomological Research 88, 3–13.CrossRefGoogle Scholar
Baer, C.F., Tripp, D.W., Bjorksten, A. & Antolin, M.F. (2004) Phylogeography of a parasitoid wasp (Diaretiella rapae): no evidence of host-associated lineages. Molecular Ecology 13, 1859–1869.CrossRefGoogle Scholar
Baker, D.A., Loxdale, H.D. & Edwards, O.R. (2003) Genetic variation and founder effects in the parasitoid wasp, Diaretiella rapae (M'Intosh) (Hymenoptera: Braconidae: Aphidiidae), affecting its potential as a biological control agent. Molecular Ecology 12, 3303–3311.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, 5–14.Google Scholar
Barnay, O., Hommay, G., Gertz, C., Kienlen, J.C., Schubert, G., Marro, J.P., Pizzol, J. & Chavigny, P. (2001) Survey of natural populations of Trichogramma (Hym., Trichogrammatidae) in the vineyards of Alsace (France). Journal of Applied Entomology 125, 469–477.CrossRefGoogle Scholar
Benasson, D., Zhang, D.X., Hartl, D.L. & Hewitt, G.M. (2001) Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends in Ecology and Evolution 16, 314–321.CrossRefGoogle Scholar
Biever, K.D. & Boldt, P.E. (1970) Utilization of soft X-rays for determining pupal parasitism of Pieris rapae. Annals of the Entomological Society of America 63, 1482–1483.CrossRefGoogle Scholar
Black, W.C. (1993) PCR with arbitrary primers: approach with care. Insect Molecular Biology 2, 1–6.CrossRefGoogle ScholarPubMed
BlackW.C., IV, W.C., IV,, DuTeau, N.M., Puterka, G.J., Nechols, J.R. & Pettorini, J.M. (1992) Use of the random amplified polymorphic DNA polymerase chain reaction (RAPD–PCR) to detect DNA polymorphisms in aphids. Bulletin of Entomological Research 82, 151–159.CrossRefGoogle Scholar
Borghuis, A., Pinto, J.D., Platner, G.R. & Stouthamer, R. (2004) Partial cytochrome oxidase II sequences distinguish the sibling species Trichogramma minutum Riley and Trichogramma platneri Nagarkatti. Biological Control 30, 90–94.CrossRefGoogle Scholar
Burks, R.A. & Pinto, J.D. (2002) Reproductive and electrophoretic comparisons of Trichogramma californicum Nagaraja and Nagarkatti with the T. minutum complex. Proceedings of the Entomological Society of Washington 104, 33–40.Google Scholar
Cameron, P.J., Powell, W. & Loxdale, H.D. (1984) Reservoirs for Aphidius ervi (Hymenoptera: Aphidiidae), a polyphagous parasitoid of cereal aphids (Hemiptera: Aphididae). Bulletin of Entomological Research 74, 647–656.CrossRefGoogle Scholar
Campbell, B.C., Stefen-Campbell, J.D. & Werren, J.H. (1993) Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae) inferred from an internal transcribed space (ITS2) and 28s rDNA sequences. Insect Molecular Biology 2, 225–237.CrossRefGoogle Scholar
Castañera, P., Loxdale, H.D. & Nowak, K. (1983) Electrophoretic study of enzymes from cereal aphid populations. II. Use of electrophoresis for identifying aphid parasitoids (Hymenoptera) of Sitobion avenae (F.) (Hemiptera: Aphididae). Bulletin of Entomological Research 73, 659–665.CrossRefGoogle Scholar
Castrovillo, P.J. & Stock, M.W. (1981) Electrophoretic techniques for detection of Glypta fumiferanae, an endoparasitoid of Western spruce budworm. Entomologia Experimentalis et Applicata 30, 176–180.CrossRefGoogle Scholar
Chang, S.-C., Hu, N.-T., Hsin, C.-Y. & Sun, C.-N. (2001) Characterization of differences between two Trichogramma wasps by molecular markers. Biological Control 21, 75–78.CrossRefGoogle Scholar
Chatterjee, S.N., Mohandas, T.P. & Taraphdar, T. (2003) Molecular characterization of the gene pool of Exorista sorbillans (Diptera: Tachinidae), a parasitoid of silkworm, Bombyx mori, in India. European Journal of Entomology 100, 195–200.CrossRefGoogle Scholar
Chen, Y., Giles, K.L. & Greenstone, M.H. (2002) Molecular evidence for a species complex in the genus Aphelinus (Hymenoptera: Aphenlinidae), with additional data on aphidiine phylogeny. Annals of the Entomological Society of America 95, 29–34.CrossRefGoogle Scholar
Chen, Y., Pike, K.S., Greenstone, M.H. & Shufran, K.A. Molecular markers for, identification of, the hyperparasitoids, Dendrocerus carpenteri, and Alloxysta, xanthopsis in, Lysiphlebus testaceipes, parasitizing cereal, aphids. BioControl in press.Google Scholar
Cole, T.J., Ram, M.S., Dowell, F.E., Omwega, C.O., Overholt, W.A. & Ramaswamy, S.B. (2003) Near-infrared spectroscopic method to identify Cotesia flavipes and Cotesia sesamiae (Hymenoptera: Braconidae). Annals of the Entomological Society of America 96, 865–869.CrossRefGoogle Scholar
Daza-Bustamante, P., Fuentes-Contreras, E., Rodriguez, L.C., Figueroa, C.C. & Niemeyer, H.M. (2002) Behavioural differences between Aphidius ervi populations from two tritrophic systems are due to phenotypic plasticity. Entomologia Experimentalis et Applicata 104, 321–328.CrossRefGoogle Scholar
Dawah, H.A. (1989) Separation of Chlorocytus species (Hymenoptera: Pteromalidae), parasitoids of stem-boring Hymenoptera (Eurytomidae and Cephidae) using enzyme electrophoresis. Entomologist 108, 216–222.Google Scholar
Dawah, H.A., Al-Haddad, F.H. & Jervis, A. (2002) Morphological and biological characterization of three closely related species of Pediobius Walker (Hymenoptera: Eulophidae). Journal of Natural History 36, 423–433.CrossRefGoogle Scholar
Demichelis, S. & Manino, A. (1998) Electrophoretic detection of parasitism by Dryindae in Typhlobcybinae leafhoppers (Homoptera: Auchenorrhyncha). Canadian Entomologist 130, 407–414.CrossRefGoogle Scholar
Edwards, O.R. & Hopper, K.R. (1999) Using superparasitism by a stem borer parasitoid to infer a host refuge. Ecological Entomology 24, 7–12.CrossRefGoogle Scholar
Edwards, O.R. & Hoy, M.A. (1993) Polymorphism in two parasitoids detected using random amplified polymorphic DNA polymerase chain reaction. Biological Control 3, 243–257.CrossRefGoogle Scholar
Edwards, O.R. & Hoy, M.A. (1995) Random amplified polymorphic DNA markers to monitor laboratory-selected, pesticide-resistant Trioxys pallidus (Hymenoptera: Aphidiidae) after release into three California walnut orchards. Environmental Entomology 24, 487–496.CrossRefGoogle Scholar
Elder, J.F. & Turner, B.J. (1995) Concerted evolution of repetitive DNA sequences in eukaryotes. Quarterly Review of Biology 70, 297–320.CrossRefGoogle ScholarPubMed
Ehrlich, H.A. (1989) PCR technology: principles and applications for DNA amplification. New YorkStockton Press.CrossRefGoogle Scholar
Elder, J.F. Jr. & Turner, B.J. (1995) Concerted evolution of repetitive DNA sequences in eukaryotes. Quarterly Review of Biology 70, 297–320.CrossRefGoogle ScholarPubMed
Erlandson, M., Braun, L., Baldwin, D., Soroka, J., Ashfaq, M. & Hegedus, D. (2003) Molecular markers for Peristenus spp. (Hymenoptera: Braconidae), parasitoids associated with Lygus spp. (Hemiptera: Miridae). Canadian Entomologist 135, 71–83.CrossRefGoogle Scholar
Escribano, A., Williams, T., Goulson, D., Cave, R.D., Chapman, J.W. & Caballero, P. (2000) Effect of parasitism on a nucleopolyhedrovirus amplified in Spodopera frugiperda larvae parasitized by Campoletis sonorensis. Entomologia Experimentalis et Applicata 97, 257–264.CrossRefGoogle Scholar
Gariepy, T., Kuhlmann, U., Haye, T., Gillott, C. & Erlandson, M. (2005) A single-step multiplex PCR assay for the detection of European Peristenus spp., parasitoids of Lygus spp. Biocontrol Science and Technology 15, 481–495.CrossRefGoogle Scholar
Geogehegan, J.E., Chudek, J.A., MacKay, R.L., Lowe, C., Moritz, S., McNicol, R.J., Birch, A.N.E., Hunter, G. & Majerus, M.E.N. (2000) Study of the anatomical changes in Coccinella septempunctata (Coleoptera: Coccinellidae) induced by diet and by infection with the larvae of Dinocampus coccinellae (Hymenoptera: Braconidae) using magnetic resonance imaging. European Journal of Entomology 97, 457–461.CrossRefGoogle Scholar
Greenstone, M.H. (1996) Serological analysis of arthropod predation: past, present and future, pp. 265–300 in Symondson, W.O.C. & Liddell, J.E. (Eds) The ecology of agricultural pests – biochemical approaches. London, Chapman and Hall.Google Scholar
Greenstone, M.H. & Edwards, M.J. (1998) DNA hybridization probe for endoparasitism by Microplitis croceipes (Hymenoptera: Braconidae). Annals of the Entomological Society of America 91, 415–421.CrossRefGoogle Scholar
Hagler, J.R. & Jackson, C.G. (1998) An immunomarking technique for labeling minute parasitoids. Environmental Entomology 27, 1010–1016.CrossRefGoogle Scholar
Harper, G.L., King, R.A., Dodd, C.S., Harwood, J.D., Glen, D.M., Bruford, M.W. & Symondson, W.O.C. (2005) Rapid screening of invertebrate predators for multiple prey DNA targets. Molecular Ecology 14, 819–827.CrossRefGoogle ScholarPubMed
Hart, A.G., Bowtell, R.W., Köckenberger, W., Wenseleers, T. & Ratneks, F.L.W. (2003) Magnetic resonance imaging in entomology: a critical review. Journal of Insect Science 3, 1–9.CrossRefGoogle ScholarPubMed
Hillis, D.M. & Dixon, M.T. (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Quarterly Review of Biology 66, 411–453.CrossRefGoogle ScholarPubMed
Hochuli, A. & Lanzrein, B. (2001) Characterization of a 212 kD protein, released into the host by the larva of the endoparasitoid Chelonus inanitus (Hymenoptera: Braconidae). Journal of Insect Physiology 47, 1313–1319.CrossRefGoogle Scholar
Hoy, M.A. (2003) Insect molecular genetics. 2nd San Diego, California, Academic Press.CrossRefGoogle Scholar
Hoy, M.A, Jeyaprakash, A., Morakote, R., Lo, P.K. & Nguyen, R. (2000) Genomic analyses of two populations of Ageniaspis citricola (Hymenoptera: Encyrtidae) suggest that a cryptic species may exist. Biological Control 17, 1–10.CrossRefGoogle Scholar
Hufbauer, R., Bogdanowicz, S.M. & Perez, L. (2001) Isolation and characterization of microsatellites in Aphidius ervi (Hymenoptera: Braconidae) and their applicability to related species. Molecular Ecology Notes 1, 197–199.CrossRefGoogle Scholar
Hufbauer, R.A., Bogdanowicz, S.M. & Harrison, R.G. (2004) The population genetics of a biological introduction: mitochondrial DNA and microsatellite variation in native and introduced populations of Aphidius ervi, a parasitoid wasp. Molecular Ecology 13, 337–348.CrossRefGoogle Scholar
Hung, A.C. & Huo, S. (1985) Malic enzyme, phosphoglucomutase and phosphoglucose isomerase enzymes in Trichogramma [Hym: Trichogrammatidae]. Entomophaga 30, 143–149.Google Scholar
Iline, I.I. & Phillips, C.B. (2004) Allozyme markers to help define the South American origins of Microctonus hyperodae (Hymenoptera: Braconidae) established in New Zealand for biological control of Argentine stem weevil. Bulletin of Entomological Research 94, 229–234.CrossRefGoogle ScholarPubMed
Jeffries, M.J. & Lawton, J.H. (1984) Enemy free space and the structure of ecological communities. Biological Journal of the Linnean Society 23, 269–286.CrossRefGoogle Scholar
Jensen, M.K., Kester, M.K., Kankare, M. & Brown, B.L. (2002) Characterization of microsatellite loci in the parasitoid, Cotesia congregate (Say) (Hymenoptera: Braconidae). Molecular Ecology Notes 2, 346–348.CrossRefGoogle Scholar
Jones, D.B., Giles, K.L., Chen, Y. & Shufran, K.A. (2005) Estimation of hymenopteran parasitism in cereal aphids by using molecular markers. Journal of Economic Entomology 98, 217–221.CrossRefGoogle ScholarPubMed
Kazmer, D.J., Hopper, K.R., Coutinot, D.M. & Heckel, D.G. (1995) Suitability of random amplified polymorphic DNA for genetic markers in the aphid parasitoid, Aphelinus asychis Walker. Biological Control 5, 503–512.CrossRefGoogle Scholar
Keen, D.P., Keen, J.E., He, Y. & Jones, C.J. (2001) Development of an enzyme-linked immunosorbent assay for detection of the gregarious hymenopteran parasitoid Muscidifurax raptorellus in house fly pupae. Biological Control 21, 140–151.CrossRefGoogle Scholar
Kimani-Njogu, S.K., Overholt, W.A., Woolley, J.B. & Omwega, C.O. (1998) Electrophoretic and phylogenetic analyses of selected allopatric populations of the Cotesia flavipes complex (Hymenoptera: Braconidae), parasitoids of cereal stem borers. Biochemical Systematics and Ecology 26, 285–296.CrossRefGoogle 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 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, 317–327.CrossRefGoogle ScholarPubMed
Kitthawee, S., Julsilikul, D., Sharpe, R.G. & Baimai, V. (1999) Protein polymorphism in natural populations of Diachasmimorpha longicaudata (Hymenoptera: Braconidae) in Thailand. Genetica 105, 125–131.CrossRefGoogle ScholarPubMed
Kühn, S. & Hoffmann, M. (1999) Infection of Coscinodiscus spp. by the parasitoid nanoflagellate Pirsonia diadema: II. Selective infection behaviour for host species and individual host cells. Journal of Plankton Research 21, 443–454.CrossRefGoogle Scholar
Kuris, A.M., Torchin, M.E. & Lafferty, K.D. (2002) Fecampia erythrocephala rediscovered: prevalence and distribution of a parasitoid of the European shore crab, Carcinus maenas. Journal of the Marine Biological Association of the United Kingdom 82, 955–960.CrossRefGoogle Scholar
Lafferty, K.D. & Kuris, A.M. (2002) Trophic strategies, animal diversity and body size. Trends in Ecology and Evolution 17, 507–513.CrossRefGoogle Scholar
Landais, I., Chavigny, P., Castagnone, C., Pizzol, J., Abad, P. & Vanlerberghe-Masutti, F. (2000) Characterization of a highly conserved satellite DNA from the parasitoid wasp. Trichogramma brassicae 255, 65–73.Google ScholarPubMed
Landry, B.S., Dextraze, L. & Boivin, G. (1993) Random amplified polymorphic DNA markers for DNA fingerprinting and genetic variability of minute parasitic wasp species (Hymenoptera: Mymaridae and Trichogrammatidae) used in biological control programs of phytophagous insects. Genome 36, 580–587.CrossRefGoogle ScholarPubMed
Li, Y.-F., Korol, A.B., Fahima, T., Beiles, A. & Nevo, E. (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Molecular Ecology 11, 2453–2465.CrossRefGoogle ScholarPubMed
Li, Z.-X. & Shen, Z.-R. (2002) PCR-based technique for identification and detection of Trichogramma spp. (Hymenoptera: Trichogrammatidae) with specific primers. Entomologia Sinica 9, 9–16.Google Scholar
Liu, C.-L., You, L.-S., Luo, Q.-H., Ruan, Y., Huang, A.-P. & Guo, C. (2003) Random amplified polymorphic DNA of the similar braconid wasps in cotton field and paddy field from China (Hymenoptera, Braconidae). Acta Zootaxonomica Sinica 28, 568–572.Google Scholar
Loxdale, H.D. & Lushai, G. (1999) Slaves of the environment: The movement of herbivorous insects in relation to their ecology and genotype. Philosophical Transactions of the Royal Society of London B 354, 1479–1495.CrossRefGoogle Scholar
Loxdale, H.D. & MacDonald, C. (2004) Tracking parasitoids at the farmland field scale using microsatellite markers, pp. 107–126 in Werner, D. (Ed.) Biological resources and migration. Proceedings of the international conference and OECD workshop, Phillips University, Marburg, Germany. Berlin Springer-Verlag.CrossRefGoogle Scholar
MacDonald, C. & Loxdale, H.D. (2004) Molecular markers to study population structure and dynamics in beneficial insects (predators and parasitoids). International Journal of Pest Management 50, 215–224.CrossRefGoogle Scholar
MacDonald, C., Brookes, C.P., Edwards, K.J., Baker, D.A., Lockton, S. & Loxdale, H.D. (2003) Microsatellite isolation and characterization in the beneficial parasitoid wasp Diaretiella rapae (M'Intosh) (Hymenoptera: Braconidae: Aphidiinae). Molecular Ecology Notes 3, 601–603.CrossRefGoogle Scholar
May, B., Leonard, D.E. & Vadas, R.L. (1977) Electrophoretic variation and sex linkage in spruce budworm. Journal of Heredity 68, 355–359.CrossRefGoogle Scholar
Morgan, P.B., Jones, C.J., Patterson, R.S. & Milne, D. (1988) Use of electrophoresis for monitoring purity of laboratory colonies of exotic parasitoids (Hymenoptera: Pteromalidae). Advances in Parasitic Hymenoptera Research 1988, 525–531.Google Scholar
Orrego, C. & Agudelo-Silva, F. (1993) Genetic variation in the parasitoid wasp Trichogramma (Hymenoptera: Trichogrammatidae) revealed by DNA amplification of a section of the nuclear ribosomal repeat. Florida Entomologist 76, 519–524.CrossRefGoogle Scholar
Paran, I. & Michelmore, R.W. (1993) Development of reliable PCR-based markers linked to downy mildew resistance genes in lettuce. Theoretical and Applied Genetics 85, 985–993.CrossRefGoogle ScholarPubMed
Parks, S.-J., Taton, T.A. & Mirkin, C.A. (2002) Array-based electrical detection of DNA with nanonparticle probes. Science 295, 1503–1506.CrossRefGoogle Scholar
Persad, A.B., Jeyaprakash, A. & Hoy, M.A. (2004) High-fidelity PCR assay discriminates between immature Lipolexis oregmae and Lysiphlebus testaceipes (Hymenoptera: Aphidiidae) within their aphid hosts. Florida Entomologist 87, 18–24.CrossRefGoogle Scholar
Pinto, J.D., Kazmer, D.J., Planter, G.R. & Sassaman, C.A. (1992) Taxonomy of the Trichogramma minutum complex (Hymenoptera: Trichogrammatidae): allozyme variation and its relationship to reproductive and geographic data. Annals of the Entomological Society of America 85, 413–422.CrossRefGoogle Scholar
Pinto, J.D., Platner, G.R. & Sassaman, C.A. (1993) Electrophoretic study of two closely related species of North American Trichogramma: T. pretiosum and T. deion (Hymenoptera: Trichogrammatidae). Annals of the Entomological Society of America 86, 702–709.CrossRefGoogle Scholar
Pinto, J.D., Platner, G.R. & Stouthamer, R. (2003) The systematics of the Trichogramma minutum species complex (Hymenoptera: Trichogrammatidae), a group of important North American biological control agents: the evidence from reproductive compatibility and allozymes. Biological Control 27, 167–180.CrossRefGoogle Scholar
Pintureau, B. (1993) Enzyme polymorphism in some African, American, and Asiatic Trichogramma and Trichogrammatoidea species (Hymenoptera: Trichogrammatidae). Biochemical Systematics and Ecology 21, 557–573.CrossRefGoogle Scholar
Prinsloo, G., Chen, Y., Giles, L. & Greenstone, M.H. (2002) Release and recovery in South Africa of the exotic aphid parasitoid Aphelinus hordei verified by the polymerase chain reaction. BioControl 47, 127–136.CrossRefGoogle Scholar
Pungerl, N.B. (1986) Morphometric and electrophoretic study of Aphidius species (Hymenoptera: Aphidiidae) reared from a variety of aphid hosts. Systematic Entomology 11, 327–354.CrossRefGoogle Scholar
Ram, P., Tshernyshev, W.B., Afonina, V.M., Greenberg, S.M. & Ageeva, L.I. (1995) Studies on strains of Trichogramma evanescens Westwood from different regions of Eurasia. Biocontrol Science and Technology 5, 329–338.CrossRefGoogle Scholar
Ratcliffe, S.T., Robertson, H.M., Jones, C.J., Bollero, G.A. & Weinzerl, R.A. (2002) Assessment of parasitism of house fly and stable fly (Diptera: Muscidae) pupae by pteromalid (Hymenoptera: Pteromalidae) parasitoids using a polymerase chain reaction. Journal of Medical Entomology 39, 52–60.CrossRefGoogle ScholarPubMed
Richardson, B.J., Baverstock, P.R. & Adams, M. (1986) Allozyme electrophoresis. A handbook for animal systematics and population studies. New York, Academic Press.Google 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, 199–206.CrossRefGoogle Scholar
Sappal, N.P., Jeng, R.S., Hubbes, M. & Liu, F. (1995) Restriction fragment length polymorphisms in polymerase chain reaction amplified ribosomal DNAs of three Trichogramma species (Hymenoptera: Trichogrammatidae). Genome 38, 419–425.CrossRefGoogle Scholar
Schneider, M.V., Driessen, G., Beukeboom, L.W., Boll, R., van Eunen, K., Selzner, A., Talsma, J. & Lapchin, L. (2003) Gene flow between arrhenotokous and thelytokous populations of Venturia canescens (Hymenoptera). Heredity 90, 260–267.CrossRefGoogle ScholarPubMed
Silva, I.M.M.S., Honda, J., van Kan, F., Hu, J., Neto, L., Pintureau, B. & Stouthamer, R. (1999) Molecular differentiation of five Trichogramma species occurring in Portugal. Biological Control 16, 177–184.CrossRefGoogle Scholar
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weightings, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701.CrossRefGoogle Scholar
Soldevila, A.I. & Jones, D. (1991) Immunoanalysis of unique protein in Trichoplusia ni parasitized by the braconid wasp Chelonus near curvimaculatus. Insect Biochemistry 21, 845–856.CrossRefGoogle Scholar
Stouthamer, R., Hu, J., van Kan, F.J.P.M., Platner, G.R. & Pinto, J.D. (1999) The utility of internally transcribed spacer 2 DNA sequences of the nuclear ribosomal gene for distinguishing sibling species of Trichogramma. BioControl 43, 421–440.CrossRefGoogle Scholar
Stouthamer, R., Gai, Y., Koopmanschap, A.B., Platner, G.R. & Pinto, J.D. (2000) ITS-2 sequences do not differ for the closely related species Trichogramma minutum and T. platneri. Entomologia Experimentalis et Applicata 95, 105–111.CrossRefGoogle Scholar
Stuart, M.K. (1998) An antibody diagnostic for hymenopteran parasitism is specific for a homologue of elongation factor-1α. Archives of Insect Biochemistry and Physiology 39, 1–8.3.0.CO;2-P>CrossRefGoogle Scholar
Stuart, M.K. & Burkholder, W.E. (1991) Monoclonal antibodies specific for Laelius pedatus (Bethylidae) and Bracon hebetor (Braconidae), two hymenopterous parasitoids of stored-product pests. Biological Control 1, 302–308.CrossRefGoogle Scholar
Stuart, M.K. & Greenstone, M.H. (1996) Serological diagnosis of parasitism: a monoclonal antibody-based immunodot assay for Microplitis croceipes (Hymenoptera: Braconidae). pp. 301 –321 in Symondson, W.O.C. & Liddell, J.E. (Eds) The ecology of agricultural pests. London, Chapman & Hall.Google Scholar
Stuart, M.K. & Greenstone, M.H. (1997) Immunological detection of hymenopteran parasitism in Helicoverpa zea and Heliothis virescens. Biological Control 8, 197–202.CrossRefGoogle Scholar
Suckling, D.M., Burnip, G.M., Gibb, A.R., Daly, J.M. & Armstrong, K.F. (2001) Plant and host effects on the leafroller parasitoid Dolichogenidia tasmanica. Entomologia Experimentalis et Applicata 100, 253–260.CrossRefGoogle Scholar
Sunnucks, P. & Hales, D.F. (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphidiae). Molecular Biology and Evolution 13, 510–524.CrossRefGoogle Scholar
Sunnucks, P., Wilson, A.C.C., Beheregaray, L.B., Zenger, K., French, J. & Taylor, A.C. (2000) SSCP is not so difficult: the application and utility of single-stranded conformation polymorphism in evolutionary biology and ecology. Molecular Ecology 9, 1699–1710.CrossRefGoogle ScholarPubMed
Takada, H. (1998) A review of Aphidius colemani (Hymenoptera: Braconidae; Aphidiinae) and closely related species indigenous to Japan. Applied Entomology and Zoology 33, 59–66.CrossRefGoogle Scholar
Taton, T.A., Mirkin, C.A. & Letsinger, R.L. (2000) Scanometric DNA array detection with nanoparticle probes. Science 289, 1757–1760.CrossRefGoogle ScholarPubMed
Taylor, D.B. & Szalanski, A.L. (1999) Identification of Muscidifurax spp. by polymerase chain reaction-restriction fragment length polymorphism. Biological Control 15, 270–273.CrossRefGoogle Scholar
Tilmon, K.J., Danforth, B.N., Day, W.H. & Hoffmann, M.P. (2000) Determining parasitoid species composition in a host population: a molecular approach. Annals of the Entomological Society of America 93, 640–647.CrossRefGoogle Scholar
Tomiuk, J., Wöhrmann, K. & Eggers-Schumacher, H.A. (1979) Enzyme patterns as a characteristic for the identification of aphids. Zeitschrift für Angewandte Entomologie 88, 440–446.CrossRefGoogle Scholar
Unruh, T.R., White, W., Gonzales, D., Gordh, G. & Luck, R.F. (1983) Heterozygosity and effective population size in laboratory populations of Aphidius ervi (Hym.: Aphidiidae). Entomophaga 28, 245–258.CrossRefGoogle Scholar
Vanlerberghe-Masutti, F. & Chavigny, P. (1997) Characterization of a microsatellite locus in the parasitoid wasp Aphelinus abdominalis (Hymenoptera: Aphelinidae). Bulletin of Entomological Research 87, 313–318.CrossRefGoogle Scholar
Vaughn, T.T. & Antolin, M.F. (1998) Population genetics of an opportunistic parasitoid in an agricultural landscape. Heredity 80, 152–162.CrossRefGoogle Scholar
Walton, M.P., Loxdale, H.D. & Allen-Williams, L. (1990a) Electrophoretic “keys” for the identification of parasitoids (Hymenoptera: Braconidae: Aphelinidae) attacking Sitobion avenae (F.) (Hemiptera: Aphididae). Biological Journal of the Linnean Society 40, 333–346.CrossRefGoogle Scholar
Walton, M.P., Powell, W., Loxdale, H.D. & Allen-Williams, L. (1990b) Electrophoresis as a tool for estimating levels of hymenopterous parasitism in field populations of the cereal aphid, Sitobion avenae. Entomologia Experimentalis et Applicata 54, 271–279.CrossRefGoogle Scholar
Weathersbee, A.A. III, Shufran, K.A., Panchal, T.D., Dang, P.M. & Evans, G.A. (2004) Detection and differentiation of parasitoids (Hymenoptera: Aphidiidae and Aphelinidae) of the brown citrus aphid (Homoptera: Aphididae): Species-specific polymerase chain reaction amplification of 18S rDNA. Annals of the Entomological Society of America 97, 286–292.CrossRefGoogle Scholar
Wool, W., van Emden, H.F. & Bunting, S.W. (1978) Electrophoretic detection of the internal parasite, Aphidius matricariae in Myzus persicae. Annals of Applied Biology 90, 21–26.CrossRefGoogle Scholar
Wynne, I.R., Loxdale, H.D. & Brookes, C.P. (1992) Use of a cellulose acetate system for allozyme electrophoresis. pp. 494 – 499 in Berry, R.J., Crawford, T.J. & Hewitt, G.M. (Eds) Genes in ecology. Oxford, Blackwells Scientific Publications.Google Scholar
Yazlovetskii, I.G., Sumenkova, V.V., Ageeva, L.I. & Dyurich, G.F. (1981) Species identification of Trichogramma by electrophoresis in polyacrylamide gel. Soviet Agricultural Science 9, 40–43.Google Scholar
Zhu, Y.-C. & Greenstone, M.H. (1999) Polymerase chain reaction techniques for distinguishing three species and two strains of Aphelinus (Hymenoptera: Aphelinidae) from Diuraphis noxia and Schizaphis graminum (Homoptera: Aphididae). Annals of the Entomological Society of America 92, 71–79.CrossRefGoogle Scholar
Zhu, Y.-C. & Williams, L. III (2002) Detecting the egg parasitoid Anaphes iole (Hymenoptera: Mymaridae) in tarnished plant bug (Heteroptera: Miridae) eggs by using a molecular approach. Annals of the Entomological Society of America 95, 359–365.CrossRefGoogle Scholar
Zhu, Y.-C., Burd, J.D., Elliott, N.C. & Greenstone, M.H. (2000) Specific ribosomal DNA marker for early polymerase chain reaction detection of Aphelinus hordei (Hymenoptera: Aphelinidae) and Aphidius colemani (Hymenoptera: Aphidiidae) from Diuraphis noxia (Homoptera: Aphididae). Annals of the Entomological Society of America 93, 486–491.CrossRefGoogle Scholar
Zhu, Y.-C., Dowdy, A.K. & Baker, J.E. (1999) Detection of single-base substitution in an esterase gene and its linkage to malathion resistance in the parasitoid Anisopteromalus calandrae (Hymenoptera: Pteromalidae). Pesticide Science 55, 398–404.3.0.CO;2-O>CrossRefGoogle Scholar
Zhu, Y.-C., Dowdy, A.K. & Baker, J.E. (2004a) Molecular differentiation of two strains of the parasitoid Anisopteromalus calandrae (Hymenoptera: Pteromalidae) using specific PCR primers. Journal of Entomological Science 39, 1–10.CrossRefGoogle Scholar
Zhu, Y.C., Riddick, E.W., Williams, L., Schotzko, D.J., Logarzo, G.A & Jackson, C.G. (2004b) Potential of detection and identification of nymphal parasitoids (Hymenoptera: Braconidae) of Lygus bugs (Heteroptera: Miridae) by using polymerase chain reaction and ITS2 sequence analysis techniques. Annals of the Entomological Society of America 97, 743–752.CrossRefGoogle Scholar