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Molecular characterization of Gonatocerus tuberculifemur (Ogloblin) (Hymenoptera: Mymaridae), a prospective Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae) biological control candidate agent from South America: divergent clades

Published online by Cambridge University Press:  13 December 2007

J.H. de León ,
G.A. Logarzo  and
S.V. Triapitsyn
J.H. de León*
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Kika de la Garza Subtropical Agricultural Research Center, Beneficial Insects Research Unit, 2413 E. Highway 83, Weslaco, Texas, 78596, USA
G.A. Logarzo
Affiliation:
United States Department of Agriculture, Agricultural Research Service, South American Biological Control Laboratory, Bolivar 1559 (1686), Buenos Aires, Argentina
S.V. Triapitsyn
Affiliation:
Department of Entomology, University of California, Riverside, California, 92521, USA
*
*Author for correspondence Fax: 001-956-969-4888 E-mail: [email protected]
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Abstract

We genetically characterized the prospective South American egg parasitoid candidate, Gonatocerus tuberculifemur, of the glassy-winged sharpshooter (GWSS), Homalodisca vitripennis, for a neoclassical biological control program in California. Two molecular methods, inter-simple sequence repeat-polymerase chain reaction DNA fingerprinting and a phylogeographic approach inferred from the mitochondrial cytochrome oxidase subunit I gene (COI), were utilized. Five geographic populations from South America were analyzed; in addition, a phylogenetic analysis was performed with several named and one unnamed Gonatocerus species using the COI gene. DNA fingerprinting demonstrated a fixed geographic banding pattern difference in the population from San Rafael, Mendoza Province, Argentina. The COI analysis uncovered haplotype or geographic structure in G. tuberculifemur. A neighbour-joining distance (NJ) and a single most parsimonious tree (MP) clustered the populations into two well-supported distinct clades with strong bootstrap values (97–99% and 92–99%, respectively) with populations from San Rafael clustering into clade 2 and the rest of the populations clustering into clade 1. No haplotype sharing was observed between individuals from the two clades. Phylogenetic analyses performed by NJ and MP methods with 15 Gonatocerus species confirmed species boundaries and again uncovered two distinct clades in G. tuberculifemur with strong bootstrap support (95–100% and 68–100%, respectively). However, the NJ tree supported the morphologically defined relationships better than the MP tree. The molecular evidence in the present study is suggestive of a species level divergence. Because G. tuberculifemur is under consideration as a potential biological control agent for GWSS in California, understanding cryptic variation in this species is critical.

Keywords

Gonatocerus tuberculifemurcytochrome oxidase subunit I gene (COI)ISSR-PCR DNA fingerprintingphylogeneticsbiological control
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 98 , Issue 1 , February 2008 , pp. 97 - 108
Copyright
Copyright © Cambridge University Press 2008

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References

Avise, J.C. (2000) Phylogeography: The History and Formation of Species. 447 pp. Cambridge, MA, USA, Harvard University Press.Google Scholar
Brlansky, R.H., Timmer, L.W., French, W.J. & McCoy, R.E. (1983) Colonization of the sharpshooter vectors, Oncometopia nigricans and Homalodisca coagulata, by xylem-limited bacteria carriers of xylem-limited bacterial disease. Phytopathology 73, 530–535.Google Scholar
Brower, A.V.Z. (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proceedings of the National Academy of Science USA 91, 6491–6495.CrossRefGoogle ScholarPubMed
Brown, J.K. (2004) Tracing the origin of cryptic insect pests and vectors, and their natural enemies. pp. 113–132in Ehler, L.E., Sforza, R. & Mateille, T. (Eds) Genetics, Evolution, and Biological Control. Wallingford, UK, CABA International.CrossRefGoogle Scholar
Caterino, M.S., Cho, C. & Sperling, F.A.H. (2000) The current state of insect molecular systematics: a thriving tower of Babel. Annual Review of Entomology 45, 1–54.CrossRefGoogle ScholarPubMed
CDFA (2003) Pierce's Disease Program Report to the Legislature. California Department of Food and Agriculture.Google Scholar
CDFA (2005) GWSS Biological Control, Spring Report. California Department of Food and Agriculture.Google Scholar
de León, J.H. & Jones, W.A. (2004) Detection of DNA polymorphisms in Homalodisca coagulata (Homoptera: Cicadellidae) by Polymerase Chain Reaction-based DNA fingerprinting methods. Annals of the Entomological Society of America 97, 574–585.CrossRefGoogle Scholar
de León, J.H. & Jones, W.A. (2005) Genetic differentiation among geographic populations of Gonatocerus ashmeadi (Hymenoptera: Mymaridae), the predominant egg parasitoid of Homalodisca coagulata (Homoptera: Cicadellidae). Journal of Insect Science 5(2), 9. Available online at insectscience.org/5.2.CrossRefGoogle ScholarPubMed
de León, J.H., Jones, W.A. & Morgan, D.J.W. (2004a) Population genetic structure of Homalodisca coagulata (Homoptera: Cicadellidae), the vector of the bacterium Xylella fastidiosa causing Pierce's disease in grapevines. Annals of the Entomological Society of America 97, 809–818.CrossRefGoogle Scholar
de León, J.H., Jones, W.A. & Morgan, D.J.W. (2004b) Molecular distinction between populations of Gonatocerus morrilli, egg parasitoids of the glassy-winged sharpshooter Homalodisca coagulata, from Texas and California: Do cryptic species exist? Journal of Insect Science 4(39), 7. Available online at insectscience.org/4.39.CrossRefGoogle Scholar
de León, J.H., Hagler, J.R., Logarzo, G.A. & Morgan, D.J.W. (2005) The utility of inter-simple sequence repeat-polymerase chain reaction (ISSR-PCR) to distinguish geographic populations of the smoke-tree sharpshooter Homalodisca liturata and egg parasitoids of the genus Gonatocerus. pp. 298–301in Tariq, M.A., Blincoe, P., Mochel, M., Oswalt, S. & Esser, T. (Eds) Proceedings of the Pierce's Disease Research Symposium. California Department of Food and Agriculture, 5–7 December 2005, San Diego, CA.Google Scholar
de León, J.H., Jones, W.A., Sétamou, M. & Morgan, D.J.W. (2006) Genetic and hybridization evidence confirms that a geographic population of Gonatocerus morrilli (Hymenoptera: Mymaridae) from California is a new species: Egg parasitoids of the glassy-winged sharpshooter Homalodisca coagulata (Homoptera: Cicadellidae). Biological Control 38, 282–293.CrossRefGoogle Scholar
Döbel, H. & Denno, R. (1993) Predator-planthopper interactions. pp. 325–399in Denno, R. & Perfect, T. (Eds) Planthoppers, their Ecology and Management. New York, NY, Chapman & Hall.Google Scholar
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.CrossRefGoogle ScholarPubMed
Gordh, G. & Beardsley, J.W. (1999) Taxonomy and biological control. pp. 45–56in Bellows, T.S. & Fisher, T.W. Jr. (Eds) Handbook of Biological Control. San Diego, CA, Academic Press.CrossRefGoogle Scholar
Higgins, D., Thompson, J., Gibson, T., Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.Google Scholar
Holt, R.D., Keitt, T.H., Lewis, M.A., Maurer, B.A. & Taper, M.L. (2005) Theoretical models of species' borders: single species approaches. OIKOS 108, 18–27.Google Scholar
Hopkins, D.L. (1989) Xylella fastidiosa: xylem-limited bacterial pathogen of plants. Annual Review of Phytopathology 27, 271–290.Google Scholar
Hopkins, D.L. & Mollenhauer, H.H. (1973) Rickettsia-like bacterium associated with Pierce's disease of grapes. Science 179, 298–300.Google Scholar
Hoy, M.A., Ayyamperumal, J., Morakete, R., Lo, M.K.C. & 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
Huber, J.T. (1986) Systematics, biology and hosts of the Mymaridae and Mymarommatidae (Insecta-Hymenoptera): 1758–1984. Entomography 4, 185–243.Google Scholar
Jones, W.A. (2001) Classical biological control of the glassy-winged sharpshooter. pp. 50–51in Tariq, M.A., Oswalt, S. & Esser, T. (Eds) Proceedings of the Pierce's Disease Research Symposium. California Department of Food and Agriculture, 5–7 December 2001, San Diego, CA.Google Scholar
Jones, W.A. (2003) Use of climate matching in an insect biological program. pp. 206in Parra, J.R.P., Zucchi, R.A., Vendramim, J.D., Moraes, R.C.B., Bogorni, P.C., Silveira Neto, S. & Bento, J.M.S. (Eds) Simposito de Controle Biologico. Sao Pedro, SP, Livro de resumos e programa official, Piracicaba, Sociedade Entomologica do Brasil, 2003.Google Scholar
Jones, W.A., Logarzo, G.A., Triapitsyn, S.V., Casas, M., Virla, E.G. & Purcell, A.H. (2005a) Biology and host range of two South American egg parasitoids (Hymenoptera: Mymaridae), possible biocontrol agents for glassy-winged sharpshooter (Say) (Hemiptera: Cicadellidae: Proconiini). Proceedings, 12th International Auchenorrhyncha Congress and 6th International Workshop on Leafhoppers and Planthoppers of Economic Significance, University of California, Berkeley, 7–12 August 2005, Berkeley, CA. Available online at http://nature.berkeley.edu/hoppercongress/.Google Scholar
Jones, W.A., Logarzo, G.A., Virla, E.G. & Luft, E. (2005b) Environmental risk assessment of egg parasitoids from South America: nontarget field and laboratory host range in Argentina and the U.S. pp. 343–344in Tariq, M.A., Blincoe, P., Mochel, M., Oswalt, S. & Esser, T. (Eds) Proceedings of the Pierce's Disease Research Symposium. California Department of Food and Agriculture, 5–7 December 2005, San Diego, CA.Google Scholar
Karp, A. & Edwards, J. (1997) DNA markers: a global overview. pp. 1–13in Caetano-Anolles, G. & Gresshoff, P.M. (Eds) DNA Markers-Protocols, Applications, and Overviews. New York, NY, Wiley-Liss, Inc.Google Scholar
Logarzo, G., Triapitsyn, S.V. & Jones, W.A. (2003) New host records for two species of Gonatocerus (Hymenoptera: Mymaridae), egg parsitoids of proconiine sharpshooters (Hemiptera: Clypeorrhyncha: Cicadellidae), in Peru. Florida Entomologist 86, 486–487.CrossRefGoogle Scholar
Logarzo, G.A., Virla, E.G., Triapitsyn, S.V. & Jones, W.A. (2004) Biology of Zagella delicata (Hymenoptera: Trichogrammatidae), an egg parasitoid of the sharpshooter Tapajosa rubromarginata (Hemiptera: Clypeorrhyncha: Cicadellidae) in Argentina. Florida Entomologist 87, 511–516.CrossRefGoogle Scholar
Logarzo, G.A., Virla, E.G. & Jones, W.A. (2005) Egg parasitoids from Argentina, potential candidates for the biological control of glassy-winged sharpshooter Homalodisca coagulata (Cicadellidae) in the United States. pp. 115–116in Hoddle, M.S. (Ed.) Second International Symposium on Biological Control of Arthropods volume III. USDA Forest Service Publication FHTET-2005-08.Google Scholar
Logarzo, G.A., de León, J.H., Triapitsyn, S.V., González, R.H. & Virla, E.G. (2006) First Report of a Proconiini sharpshooter, Anacuerna centrolinea (Hemiptera: Cicadellidae), in Chile with notes on its biology, host plants, and egg parasitoids. Annals of the Entomological Society of America 99, 879–883.CrossRefGoogle Scholar
Löhr, B.A., Varela, M. & Santos, B. (1990) Exploration for natural enemies of the cassava mealybug, Phenococcus manihoti (Homoptera: Pseudococcidae), in South America for the biological control of this introduced pest in Africa. Bulletin of Entomological Research 80, 417–425.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.Google Scholar
Messing, R.H. & Aliniazee, M.T. (1988) Hybridization and host suitability of two biotypes of Trioxys pallidus (Hymenoptera: Aphidiidae). Annals of the Entomological Society of America 81, 6–9.CrossRefGoogle Scholar
Miller, D.R. & Rossman, A.Y. (1995) Systematics, biodiversity, and agriculture. BioScience 45, 680–686.CrossRefGoogle Scholar
Morgan, D.J.W., Triapitsyn, S.V., Redak, R.A., Bezark, L.G. & Hoddle, M.S. (2000) Biological control of the glassy-winged sharpshooter: current status and future potential. pp. 167–171in Hoddle, M.S. (Ed.) California Conference on Biological Control. 11–12 July 2000, Riverside, CA.Google Scholar
Narang, S.K., Tabachnick, W.J. & Faust, R.M. (1993) Complexities of population genetic structure and implications for biological control programs. pp. 19–52in Narang, S.K., Barlett, A.C. & Faust, R.M. (Eds) Applications of Genetics to Arthropods of Biological Control Significance. Boca Raton, FL, USA, CRC Press Inc.Google Scholar
Nielson, M.W. (1968) The leafhopper vectors of phytopathogenic viruses (Homoptera, Cicadellidae) taxonomy, biology, and virus transmission. USDA Technical Bulletin 1382, 81–84.Google Scholar
Parmesan, C., Gaines, S., Gonzalez, L., Kaufman, D.M., Kingsolver, J., Peterson, T. & Sagarin, R. (2005) Empirical perspectives on species borders: from traditional biogeography to global change. OIKOS 108, 58–75.Google Scholar
Redak, R.A., Purcell, A.H., Lopes, J.R.S., Blua, M.J., Mizell, R.F. & Andersen, P.C. (2004) The biology of xylem fluid-feeding insect vectors of Xylella fastidiosa and their relationship to disease epidemiology. Annual Review of Entomology 49, 243–270.Google Scholar
Roderick, G.K. (2004) Tracing the origins of pests and natural enemies: Genetic and statistical approaches. pp. 97–112in Ehler, L.E., Sforza, R. & Mateille, T. (Eds) Genetics, Evolution, and Biological Control. Wallingford, UK, CABA International.Google Scholar
Roderick, G.K. & Navajas, M. (2003) Genes in new environments: Genetics and evolution in biological control. Nature Reviews Genetics 4, 889–899.Google Scholar
Rosen, D. (1977) The importance of cryptic species and specific identifications as related to biological control. pp. 23–35in Romberger, J.A. (Ed.) Biosystemtics in agriculture. Beltsville Symposium of Agricultural Research, Monteclair, NJ, USA, Allanheld, Osmun and Co.Google Scholar
Saitou, N. & Nei, M. (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.Google Scholar
Sambrook, J. & Russell, D.W. (2001) Molecular cloning: A Laboratory Manual. 3rd edn. Cold Spring Harbor, NY, USA. Cold Spring Harbor Laboratory Press.Google Scholar
Schauff, M.E. & LaSalle, J. (1998) The relevance of systematics to biological control: protecting the investment in research. pp. 425–436in Pest Management-Future Challenges, vol. 1, Proceedings of the 6th Australian Applied Entomological Conference, 29 September–2 October 1998, Brisbane, Australia.Google Scholar
Scheffer, S.J. (2000) Molecular Evidence of Cryptic Species within the Liriomyza huidobrensis (Diptera: Agromyzidae). Journal of Economic Entomology 93, 1146–1151.Google Scholar
Scheffer, S.J., Giblin-Davis, R.M., Taylor, G.S., Davies, K.A., Purcell, M., Lewis, L., Goolsby, J. & Center, T.D. (2004) Phylogenetic relationships, species limits, and host specificity of gall-forming Fergonsonina flies (Diptera: Fergusoninidae) feeding on Melaleuca (Myrtaceae). Annals of the Entomological Society of America 97, 1216–1221.CrossRefGoogle Scholar
Simon, C., Frati, F., Bechenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a complilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701.CrossRefGoogle Scholar
Smith, P.T. (2005) Mitochondrial DNA variation among populations of the glassy-winged sharpshooter, Homalodisca coagulata. Journal of Insect Science 5(41) 8 pp. Available online at insectscience.org/5.41.CrossRefGoogle ScholarPubMed
Sorensen, J.T. & Gill, R.J. (1996) A range extension of Homalodisca coagulata (Say) (Hemiptera: Clypeorrhyncha: Cicadellidae) to southern California. Pan-Pacific Entomology 72, 160–161.Google Scholar
Swofford, D.L. (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland, MA, USA, Sinauer Assoc.Google Scholar
Takiya, D.M., McKamey, S.H. & Cavichioli, R.R. (2006) Validity of Homalodisca and of H. vitripennis as the name for Glassy-Winged Sharpshooter (Hemiptera: Cicadellidae: Cicadellinae). Annuals of the Entomological Society of America 99, 648–655.CrossRefGoogle Scholar
Thompson, J.D., Gibson, T.J., Plewniak, F. & Higgins, D.G. (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 4876–4882.Google Scholar
Triapitsyn, S.V. (2006) A key to the Mymaridae (Hymenoptera) egg parasitoids of proconiine sharpshooters (Hemiptera: Cicadellidae) in the Nearctic region, with description of two new species of Gonatocerus. Zootaxa 1203, 1–38.Google Scholar
Turner, W.F. & Pollard, H.N. (1959) Life histories and behavior of five insect vectors of phony peach disease. USDA Technical Bulletin 1188, 28 pp.Google Scholar
Unruh, T.R. & Woolley, J.B. (1999) Molecular methods in classical biological control. pp. 57–85in Van Driesche, R.G. & Bellows, T.S. Jr. (Eds) Biological Control. New York, NY, Chapman and Hall.Google Scholar
Virla, E.G., Logarzo, G.A., Jones, W.A. & Triapitsyn, S. (2005) Biology of Gonatocerus tuberculifemur (Hymenoptera: Mymaridae), an egg parasitoid of the sharpshooter, Tapajosa rubromarginata (Hemiptera: Cicadellidae). Florida Entomologist 88, 67–71.CrossRefGoogle Scholar
Varela, L.G., Smith, R.J. & Phillips, P.A. (2001) Pierce's Disease. University of California Agricultural Natural Research, Publication 21600.Google Scholar
Werren, J.H., Windsor, D. & Guo, L. (1995) Distribution of Wolbachia among Neotropical arthropods. Proceedings of the Royal Society of London Series B 262, 197–204.Google Scholar
Wolfe, A.D. & Liston, A. (1998) Contributions of PCR-based methods to plant systematic and evolutionary biology. pp. 43–86in Soltis, D.E., Soltis, P.S. & Doyle, J.J. (Eds) Molecular Systematics of Plants II: DNA Sequencing. New York, NY, Kluwer.Google Scholar
Young, D.A. (1958) A synopsis of the species of Homalodisca in the United States (Homoptera: Cicadellidae). Bulletin of the Brooklyn Entomological Society 53, 7–13.Google Scholar
Young, D.A. (1968) Taxonomic study of the Cicadellinae. Part 1. Proconiini. United States National Museum Bulletin 261, 193–204.Google Scholar
Zietkiewicz, E., Rafalski, A. & Labuda, D. (1994) Genomic fingerprinting by simple sequence repeat (SSR)-anchored polymerase chain reaction amplification. Genomics 20, 176–183.Google Scholar