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Restriction fragment length polymorphisms of different DNA regions as genetic markers in the hoverfly Episyrphus balteatus (Diptera: Syrphidae)

Published online by Cambridge University Press:  09 March 2007

P. Hondelmann
Affiliation:
Institute of Plant Diseases and Plant Protection, University of Hannover, Herrenhäuser Str. 2, 30419 Hannover, Germany
C. Borgemeister*
Affiliation:
Institute of Plant Diseases and Plant Protection, University of Hannover, Herrenhäuser Str. 2, 30419 Hannover, Germany
H.-M. Poehling
Affiliation:
Institute of Plant Diseases and Plant Protection, University of Hannover, Herrenhäuser Str. 2, 30419 Hannover, Germany
*
*Fax: +49 511 7623015 E-mail: borgemeister@ipp.uni-hannover.de

Abstract

A polymerase chain reaction–restriction fragment length polymorphism (PCR–RFLP) analysis using mitochondrial (A + T-rich region; mtDNA) and genomic (zen-region; nDNA) DNA was performed on 182 female individuals of Episyrphus balteatus (DeGeer), a widespread aphidophagous hoverfly with supposed migratory behaviour. Specimens originated from 13 sampling sites in six European countries. The analyses revealed 12 and 18 haplotypes, respectively, for the two DNA types, several of them with a wide distribution, although seven and eight haplotypes, respectively, occurred only in one location. In contrast to other studies on mobile insects, the genetic diversity was relatively high. However, lack of population subdivision, low genetic distances between populations, the very high gene flow rates, and the complete lack of isolation by distance suggest that E. balteatus populations are largely connected and that there is an absence of large-scale geographic structuring. These results support the hypothesis that E. balteatus is a migratory hoverfly species, capable of moving over large distances. These findings related to the seasonal migrations of this species are discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2005

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References

Aljanabi, S.M. & Martinez, I. (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research 25, 46924693.CrossRefGoogle ScholarPubMed
Ankersmit, G.W., Dijman, H., Keuning, N.J., Mertens, H., Sins, A. & Tacoma, H.M. (1986) Episyrphus balteatus as a predator of the aphid Sitobion avenae on winter wheat. Entomologia Experimentalis et Applicata 42, 271277.CrossRefGoogle Scholar
Aubert, J., Aubert, J.-J., Goeldlin, de & Tiefenau, P. (1976) Douze ans de captures systématiques de Syrphides (Diptères) au Col de Bretolet (Alpes valaisannes). Mitteilungen der Schweizer Entomologischen Gesellschaft 49, 115142.Google Scholar
Avise, J.C. (1994) Molecular markers, natural history and evolution 511. New York, Chapman & Hall.CrossRefGoogle Scholar
Bargen, H., Saudhof, K. & Poehling, H.-M. (1998) Prey finding by larvae and adult females of Episyrphus balteatus. Entomologia Experimentalis et Applicata 87, 245254.CrossRefGoogle Scholar
Ballard, J.W.O. & Whitlock, M.C. (2004) The incomplete natural history of mitochondria. Molecular Ecology 13, 729744.CrossRefGoogle ScholarPubMed
Bohonak, A. (1999) Dispersal, gene flow, and population structure. Quarterly Review of Biology 74, 2145.CrossRefGoogle ScholarPubMed
Brehm, A., Harris, D.J., Hernández, M., Cabrera, V.M., Larruga, J.M., Pinto, F.M. & González, A.M. (2001) Structure and evolution of the mitochondrial DNA complete control region in the Drosophila subobscura subgroup. Insect Molecular Biology 10, 573578.CrossRefGoogle ScholarPubMed
Brower, A.V.Z. & Boyce, T.M. (1991) Mitochondrial DNA variation in monarch butterflies. Evolution 45, 12811286.CrossRefGoogle ScholarPubMed
David, P. (1998) Heterozygosity-fitness correlations: new perspective on old problems. Heredity 80, 531537.CrossRefGoogle ScholarPubMed
Dueñas, J.C.R., Panzetta-Dutari, G.M., Blanco, A. & Gardenal, C.N. (2002) Restriction fragment-length polymorphism of the mtDNA A+T-rich region as a genetic marker in Aedes aegypti (Diptera: Culicidae). Annals of the Entomological Society of America 95, 352358.CrossRefGoogle Scholar
Excoffier, L., Smouse, P.E. & Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479491.CrossRefGoogle ScholarPubMed
Felsenstein, J. (1993) PHYLIP (Phylogeny Inference Package) version 3.5c Seattle Department of Genetics, University of WashingtonGoogle Scholar
Freeland, J.R., May, M., Lodge, R. & Conrad, K.F. (2003) Genetic diversity and widespread haplotypes in a migratory dragonfly, the common green darner Anax junius. Ecological Entomology 28, 413421.CrossRefGoogle Scholar
Gatter, W. & Schmid, U. (1990) Die Wanderungen der Schwebfliegen (Diptera, Syrphidae) am Randecker Maar. Spixiana Supplement 15, 1100.Google Scholar
Gimnig, J.E., Reisen, W.K., Eldridge, B.F., Nixon, K.C. & Schutz, S.J. (1999) Temporal and spatial genetic variation within and among populations of the mosquito Culex tarsalis from California. Journal of Medical Entomology 36, 2329.CrossRefGoogle ScholarPubMed
Gower, J.C. (1966) Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53, 325338.CrossRefGoogle Scholar
Hansson, B. & Westerberg, L. (2002) On the correlation between heterozygosity and fitness in natural populations. Molecular Ecology 11, 24672474.CrossRefGoogle ScholarPubMed
Hart, A.J. & Bale, J.S. (1997) Cold tolerance of the aphid predator Episyrphus balteatus (Diptera, Syrphidae). Physiological Entomology 22, 332338.CrossRefGoogle Scholar
Hedrick, P.W. (2000) Genetics of populations. 553 pp. Sudbury, Suffolk, Jones and Bartlett Publishers.Google Scholar
Hughes, C.L. & Kaufman, T.C. (2002) Hox genes and the evolution of the arthropod body plan. Evolution and Development 4, 459499.CrossRefGoogle ScholarPubMed
Krause, U. & Poehling, H.-M. (1996) Overwintering, oviposition and population dynamics of hoverflies (Diptera: Syrphidae) in northern Germany in relation to small and large-scale landscape structure. Acta Jutlandica 71, 157169.Google Scholar
Legendre, P. & Anderson, M.J. (1998) Program DistPCoA Département de sciences biologiques, Université de MontréalGoogle Scholar
Lessinger, A.C. & Azeredo-Espin, A.M. (2000) Evolution and structural organisation of mitochondrial DNA control region of myiasis-causing flies. Medical and Veterinary Entomology 14, 7180.CrossRefGoogle ScholarPubMed
Lingoes, J.C. (1971) Some boundary conditions for a monotone analysis of symmetric matrices. Psychometrika 36, 195203.CrossRefGoogle Scholar
Llewellyn, K.S., Loxdale, H.D., Harrington, R., Brookes, C.P., Clark, S.J. & Sunnucks, P. (2003) Migration and genetic structure of the grain aphid (Sitobion avenae) in Britain related to climate and clonal fluctuation as revealed using microsatellites. Molecular Ecology 12, 2134.CrossRefGoogle ScholarPubMed
Loxdale, H.D. & Lushai, G. (1998) Molecular markers in entomology. Bulletin of Entomological Research 88, 577600.CrossRefGoogle Scholar
Loxdale, H.D. & Lushai, G. (2001) Use of genetic diversity in movement studies of flying insects. pp. 361386in Woiwod, I.P, Reynolds, D.R, & Thomas, C.D. (Eds) Insect movement: mechanisms and consequences. Royal Entomological Society 20th International SymposiumImperial College, London13–14 September 1999. Wallingford, Oxon CAB International.CrossRefGoogle Scholar
Ludoski, J., Milankov, V. & Vujic, A. (2003) Geographic differentiation between conspecific populations of Cheilosia cumanica, Ch. hypena and Ch. urbana (Diptera: Syrphidae). p. 123 in Second International Symposium on the Syrphidae. Biodiversity and Conservation, 2003Alicante, Spain.Google Scholar
McElroy, D., Moran, P., Bermingham, E. & Kornfield, I. (1992) REAP: an integrated environment for the manipulation and phylogenetic analysis of restriction data. Journal of Heredity 83, 157158.CrossRefGoogle ScholarPubMed
Milankov, V., Stamenkovic, J., Vujic, A. & Simic, S. (2002) Geographic variation of Cheilosia vernalis (Fallen, 1817) (Diptera: Syrphidae). Acta Zoologica Academiae Scientiarum Hungaricae 48, 255267.Google Scholar
Mun, J.H., Song, Y.H., Heong, K.L. & Roderick, G.K. (1999) Genetic variation among Asian populations of rice planthoppers, Nilaparvata lugens and Sogatella furcifera (Hemiptera: Delphacidae): mitochondrial DNA sequences. Bulletin of Entomological Research 89, 245253.CrossRefGoogle Scholar
Nathan, R., Perry, G., Cronin, J.T., Strand, A.E. & Cain, M.L. (2003) Methods for estimating long-distance dispersal. OIKOS 103, 261273.CrossRefGoogle Scholar
Nei, M. (1987) Molecular evolutionary genetics. pp. 512New York, Columbia University Press.CrossRefGoogle Scholar
Nei, M. & Li, W.H. (1979) Mathematical model for studying genetic variation in terms of restriction endonuclease. Proceedings of the National Academy of Sciences of the USA 76, 52695273.CrossRefGoogle Scholar
Nei, M. & Tajima, F. (1981) DNA polymorphism detectable by restriction endonucleases. Genetics 97, 145163.CrossRefGoogle ScholarPubMed
Nei, M., Maruyama, T. & Chakraborty, R. (1975) The bottleneck effect and genetic variability in populations. Evolution 29, 110.CrossRefGoogle ScholarPubMed
Parker, P.G., Snow, A.A., Schug, M.D., Booton, G.C. & Fuerst, P.A. (1998) What molecules can tell us about populations: choosing and using a molecular marker. Ecology 79, 361382.Google Scholar
Peck, L.V. (1988) Syrphidae. pp. 11230 in Papp, L. (Ed.) Catalogue of Palearctic Diptera. Vol. 8 Soós Á. Amsterdam, Elsevier Syrphidae-Conopidae.Google Scholar
Raymond, M. & Rousset, F. (2003) Genepop 3.4 Institut des Sciences de L'Évolution, Université de Montpellier Laboratoire Génétique et EnvironnementGoogle Scholar
Roderick, G.K. (1996) Geographic structure of insect populations: gene flow, phylogeography, and their uses. Annual Review of Entomology 41, 325352.CrossRefGoogle ScholarPubMed
Salveter, R. (1996) Populationsaufbau aphidophager Schwebfliegen (Diptera: Syrphidae) in der Agrarlandschaft. 116 pp. PhD thesis, University of Berne, Switzerland.Google Scholar
Salveter, R. & Nentwig, W. (1993) Schwebfliegen (Diptera, Syrphidae) in der Agrarlandschaft: Phänologie, Abundanz und Markierungsversuche. Mitteilungen der Naturforschenden Gesellschaft in Bern N.F 50, 147191.Google Scholar
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular cloning. A laboratory manual. 2nd edn. New York, Cold Spring Harbor Laboratory PressGoogle Scholar
Schneider, S., Roessli, D. & Excoffier, L. (2001) Arlequin: a software for population genetics data analysis. Ver 2.001 Genetics and Biometry Laboratory, Department of Anthropology, University of GenevaGoogle Scholar
Schultheis, A.S., Weigt, L.A. & Hendricks, A.C. (2002) Gene flow, dispersal, and nested clade analysis among populations of the stonefly Peltoperla tarteri in the southern Appalachians. Molecular Ecology 11, 317327.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
Slatkin, M. (1985) Gene flow in natural populations. Annual Review of Ecology and Systematics 16, 393420.CrossRefGoogle Scholar
Slatkin, M. (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139, 457462.CrossRefGoogle ScholarPubMed
Stauber, M., Prell, A. & Schmidt-Ott, U. (2002) A single Hox3 gene with composite bicoid and zerknüllt expression characteristics in non-cyclorrhaphan flies. Proceedings of the National Academy of Sciences of the USA 99, 274279.CrossRefGoogle ScholarPubMed
Steenis, J., van Steenis van, W. & Wakkie, B. (2001) Hoverflies in southern Skåne, Sweden. Entomologisk Tidskrift 122, 1527.Google Scholar
Sullivan, M.S. & Sutherland, J.P. (2000) Geographical variation in morphology and asymmetry in Episyrphus balteatus DeGeer. Tijdschrift voor Entomologie 142, 327331.CrossRefGoogle Scholar
Svensson, B.G. & Janzon, L.-Å;. (1984) Why does the hoverfly Metasyrphus corollae migrate. Ecological Entomology 9, 329335.CrossRefGoogle Scholar
Szalanski, A.L. (1995) Genetic characterization and population genetics of stable fly (Diptera: Muscidae). 138 pp. PhD thesis, University of Lincoln, Nebraska.Google Scholar
Tauber, M.J., Tauber, C.A. & Masaki, S. (1986) Seasonal adaptions of insects pp. 411Oxford, Oxford University Press.Google Scholar
Taylor, M.F.J., McKechnie, S.W., Pierce, N. & Kreitman, M. (1993) The lepidopteran mitochondrial control region: structure and evolution. Molecular Biology and Evolution 10, 12591272.Google ScholarPubMed
Tenhumberg, B., Poehling, H.-M. (1995) Syrphids as natural enemies of cereal aphids in Germany: aspects of their biology and efficacy in different years and regions. Agriculture, Ecosystems and Environment 52, 3943.CrossRefGoogle Scholar
Tizado-Morales, E.J., Marcos-García, M., Núňez, Pérez E. (1991) Aphidophagous hoverflies recorded in Leon (Spain). pp. 111120 in Polgár, L. Chambers, R.J. Dixon, A.F.G. Hodek, I. (Eds) Behaviour and impact of aphidophaga. Proceedings of the fourth meeting of the IOBC working group Ecology of Aphidophaga. The Hague, SPB Publishing.Google Scholar
Torp, E. (1994) Danmarks svirrefluer. pp. 490Stenstrup, Apollo Books.Google Scholar
Verlinden, L. & DeCleer, K. (1987) The hoverflies of Belgium and their faunistics: frequency, distribution, phenology 170 Bruxelles Institut Royal des Sciences Naturelles de BelgiqueGoogle Scholar
Wright, S. (1951) The genetical structure of populations. Annals of Eugenetics 15, 323354.CrossRefGoogle ScholarPubMed
Wynne, I.R. (2001) Population genetic structure of Portevinia maculata pp. 5051Germany, Stuttgart.Google Scholar
Zhang, D.-X. & Hewitt, G.M. (2003) Nuclear DNA analyses in genetic studies of populations: practice, problems and prospects. Molecular Ecology 12, 563584.CrossRefGoogle Scholar