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Electrophoretic study of five aphid parasitoid species of the genus Aphidius (Hymenoptera: Braconidae), including evidence for reproductively isolated sympatric populations and a cryptic species

Published online by Cambridge University Press:  10 July 2009

P. Atanassova ,
C.P. Brookes ,
H.D. Loxdale  and
W. Powell
P. Atanassova
Affiliation:
Entomology and Nematology Department, IACR—Rothamsted, Harpenden, Herts, AL5 2JQ, UK
C.P. Brookes
Affiliation:
Entomology and Nematology Department, IACR—Rothamsted, Harpenden, Herts, AL5 2JQ, UK
H.D. Loxdale*
Affiliation:
Entomology and Nematology Department, IACR—Rothamsted, Harpenden, Herts, AL5 2JQ, UK
W. Powell
Affiliation:
Entomology and Nematology Department, IACR—Rothamsted, Harpenden, Herts, AL5 2JQ, UK
*
* Author for correspondence.
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Abstract

Four polymorphic enzymes (PEP, PGI, PGM and IDH) were separated from adult individuals of five aphid parasitoid species of the genus Aphidius Nees (A. ervi Haliday, A. microlophii Pennacchio & Tremblay, A. eadyi Starý, Gonzalez & Hall, A. picipes Nees and A. urticae Haliday) using horizontal cellulose acetate plate electrophoresis. These markers were used to investigate the genetic relationships, including reproductive isolation and host adaptation/specificity, in laboratory and field populations. Samples were collected from the pea aphid, Acyrthosiphon pisum (Harris) and/or the nettle aphid, Microlophium carnosum (Buckton) in the UK and Bulgaria between 1991 and 1994. Whilst all loci discriminated between some species, PGM discriminated all five species, one species (A. eadyi) bearing two unique alleles (PGMa and PGMc). Aphidius microlophii (from nettle aphid) and A. ervi (from pea aphid), which are difficult to separate morphologically, possessed unique PGM alleles – PGMb and PGMe, respectively. Both parasitoids occur sympatrically, and whilst hybrids heterozygous for PGM were produced in the laboratory (PGMb,e), such genotypes were not observed in the field populations sampled. Hence, the species appear to be reproductively isolated. Most parasitoid populations studied showed mean heterozygote deficiencies per locus (homozygote excess) compared with Hardy-Weinberg expectations. In particular, A. eadyi bearing PGMa alleles were always homozygous whilst additionally, many were homozygous for another allele, PGIb. This is evidence for the existence of one or more morphologically-indistinguishable ‘cryptic’ species occurring sympatrically within European field populations. A dendrogram of relatedness was produced following calculation of Nei's genetic identity coefficient, I from the parasitoid population allele frequency data. All species showed very high similarity between populations at the intraspecific level (>0.9), but fewer interspecific similarities (0.23–0.63). These values compare well with previously published values for Aphidius populations and for other insects.

Type
Research Article
Information
Bulletin of Entomological Research , Volume 88 , Issue 1 , February 1998 , pp. 3 - 13
Copyright
Copyright © Cambridge University Press 1998

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References

Adamson, R.E., Ward, R.D., Feliciangeli, M.D. & Maingon, R. (1993) The application of random amplified polymorphic DNA for sandfly species identification. Medical and Veterinary Entomology 7, 203–207.CrossRefGoogle ScholarPubMed
Avise, J.C. (1975) Systematic value of electrophoretic data. Systematic Zoology 23, 465–481.CrossRefGoogle Scholar
Avise, J.C. (1977) Genetic differentiation during speciation. pp. 106–122in Ayala, F.J. (Ed.) Molecular evolution. Sunderland, Massachusetts, USA, Sinauer Associates, Inc.Google Scholar
Avise, J.C. (1994) Molecular markers, natural history and evolution. New York, Chapman and Hall.CrossRefGoogle Scholar
Blanchetot, A. & Packer, L. (1992) Genetic variability in the social bee Lasioglossum marginatum and a cryptic undescribed sibling species, as detected by DNA fingerprinting and allozyme electrophoresis. Insect Molecular Biology 1, 89–97.CrossRefGoogle Scholar
Brookes, C.P. & Loxdale, H.D. (1985) A device for simultaneously homogenizing numbers of individual small insects for electrophoresis. Bulletin of Entomological Research 75, 377–378.CrossRefGoogle Scholar
Castañera, P., Loxdale, H.D. & Nowak, K. (1983) Electrophoretic study of enzymes from cereal aphid populations. II. Use of electrophoresis for identifying aphidiid parasitoids (Hymenoptera) of Sitobion avenae (F.) (Hemiptera: Aphididae). Bulletin of Entomological Research 73, 659–665.CrossRefGoogle Scholar
Chen, J-H., Gonzalez, D. & Luhman, J. (1990) A new species of Aphidius (Hymenoptera) attacking the pea aphid, Acyrthosiphon pisum. Entomophaga 35, 509–514.CrossRefGoogle Scholar
Claridge, M.F. (1991) Genetic and biological diversity of insect pests and their natural enemies. pp. 183–194in Hawksworth, D.L. (Ed.) Biodiversity of microorganisms and invertebrates; its role in sustainable agriculture. Wallingford, CAB International.Google Scholar
Clausen, C.P. (1977) Introduced parasites and predators of arthropod pests and weeds: a world review. United States Department of Agriculture; Agriculture Handbook No. 480.Google Scholar
Digilio, M.C. & Pennacchio, F. (1992) A quantitative analysis of pre-mating and post-mating isolation mechanisms between Aphidius ervi Haliday and Aphidius microlophii Pennacchio & Tremblay (Hymenoptera, Braconidae). Bollettino del Laboratorio di Entomologia Agraria ‘Filippo Silvestri’ 49, 117–125.Google Scholar
Eady, R.D. (1969) A new diagnostic character in Aphidius (Hymenoptera: Braconidae) of special significance in species of pea aphid. Proceedings of the Royal Entomological Society of London, Series B 38, 165–173.Google Scholar
Ferguson, A. (1980) Biochemical systematics and evolution. Glasgow and London, Blackie.Google Scholar
Gargiulo, G., Malva, C., Pennacchio, F. & Tremblay, E. (1988) Structure of Aphidius Nees (Hymenoptera, Braconidae) rDNA: a molecular tool in biosystematic research. Bollettino de Laboratorio di Entomologia Agraria ‘Filippo Silvestri’ 45, 203–219.Google Scholar
Gawel, N.J. & Bartlett, A.C. (1993) Characterization of differences between whiteflies using RAPD—PCR. Insect Molecular Biology 2, 33–38.CrossRefGoogle ScholarPubMed
Henry, C.S. (1994) Singing and cryptic speciation in insects. Trends in Ecology and Evolution 9, 388–392.CrossRefGoogle ScholarPubMed
Hopper, K.R., Roush, R.T. & Powell, W. (1993) Management of genetics of biological-control introductions. Annual Review of Entomology 38, 27–51.CrossRefGoogle Scholar
Hudson, A. & Lefkovitch, L.P. (1982) Allozyme variation in four Ontario populations of Xestia adela and X. dolosa and in British population of Xestia c-nigrum (Lepidoptera: Noctuidae). Annals of the Entomological Society of America 75, 250–256.CrossRefGoogle Scholar
Levene, H. (1949) On a matching problem arising in genetics. Annals of Mathematical Statistics 20, 91–94.CrossRefGoogle Scholar
Loxdale, H.D. (1994) Isozyme and protein profiles of insects of agricultural and horticultural importance. pp. 337–375in Hawksworth, D.L. (Ed.) Identification and characterization of pest organisms. Wallingford, CAB International.Google Scholar
Loxdale, H.D., Castañera, P. & Brookes, C.P. (1983) Electrophoretic study of enzymes from cereal aphid populations. I. Electrophoretic techniques and staining systems for characterising isoenzymes from six species of cereal aphids (Hemiptera; Aphididae). Bulletin of Entomological Research 73, 645–657.CrossRefGoogle Scholar
Mackauer, M. (1969) Sexual behaviour and hybridization between three species of Aphidius Nees, parasitic on the pea aphid. Proceedings of the Entomological Society of Washington 71, 339–351.Google Scholar
Mackauer, M. & Starý, P. (1967) Hymenoptera, Ichnumonoidea, World Aphidiidae. Index of Entomophagous Insects. Paris: Le Francois.Google Scholar
Mayr, E. (1963) Animal species and evolution. Cambridge, Massachusetts, Harvard University Press.CrossRefGoogle Scholar
Mescheloff, E. & Rosen, D. (1990) Biosystematic studies on the Aphidiidae of Israel (Hymenoptera: Ichneumonidae). 4. The Genera Pauesia, Diaeretus, Aphidius and Diaeretiella. Israel Journal of Entomology 24, 51–91.Google Scholar
Munstermann, L.E. (1988) Biochemical systematics of nine Nearctic Aedes mosquitoes (subgenus Ochlerotatus, annulipes group B). pp. 133–147in Service, M.W. (Ed.) Biosystematics of haematophagous insects. Oxford, Clarendon Press.Google Scholar
Nei, M. (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 23, 341–369.Google Scholar
Němec, V. & Starý, P. (1984) Utilisation of isozyme analysis in the research on population diversity of aphid parasitoids (Hym., Aphidiidae). Zeitschrift für Angewandte Entomologie 98, 150–159.CrossRefGoogle Scholar
Němec, V. & Starý, P. (1985) Genetic diversity of the parasitoid Aphidius ervi on the pea aphid, Acyrthosiphon pisum in Czechoslovakia (Hymenoptera, Aphidiidae; Homoptera, Aphididae). Acta Entomologica Bohemoslovaca 82, 88–94.Google Scholar
Pennacchio, F. (1989) The Italian species of the genus Aphidius Nees (Hymenoptera, Braconidae, Aphidiinae). Bollettino del Laboratorio di Entomologia Agraria ‘Filippo Silvestri’ 46, 75–106.Google Scholar
Pennacchio, F. & Tremblay, E. (1987) Biosystematic and morphological study of two Aphidius ervi Haliday ‘biotypes’ with the description of a new species. Bollettino del Laboratorio di Entomologia Agraria ‘Filippo Silvestri’ 43, 105–117.Google Scholar
Pennacchio, F., Digilio, M.C., Tremblay, E. & Tranfaglia, A. (1994) Host recognition and acceptance behaviour in two aphid parasitoid species: Aphidius ervi and Aphidius microlophii (Hymenoptera: Braconidae). Bulletin of Entomological Research 84, 57–64.CrossRefGoogle Scholar
Pinto, J.D., Kazmer, D.J., Platner, G.R. & Sassaman, C.A. (1992) Taxonomy of the Trichogramma minutum complex (Hymenoptera: Trichogrammatidae): Allozymic variation and its relationship to reproductive and geographic data. Annals of the Entomological Society of America 85, 413–422.Google Scholar
Powell, W. (1982) The identification of hymenopterous parasitoids attacking cereal aphids in Britain. Systematic Entomology 7, 465–473.CrossRefGoogle Scholar
Powell, W. (1994) Němec and Starý's ‘Population Diversity Centre’ hypothesis for aphid parasitoids re-visited. Norwegian Journal of Agricultural Sciences Supplement 16, 163–169.Google Scholar
Powell, W. & Wright, A.F. (1988) The abilities of the aphid parasitoids Aphidius ervi Haliday and A. rhopalosiphi De Stefani Perez (Hymenoptera: Braconidae) to transfer between different host species and the implications for the use of alternative hosts in pest control strategies. Bulletin of Entomological Research 78, 683–693.CrossRefGoogle Scholar
Pungerl, N.B. (1983) Variability in characters commonly used to distinguish Aphidius species (Hymenoptera: Aphidiidae) Systematic Entomology 8, 425–430.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.Google Scholar
Richardson, B.J., Baverstock, P.R. & Adams, M. (1986) Allozyme electrophoresis. A handbook for animal systematics and population studies. London, Academic Press.Google Scholar
Rogers, J.S. (1972) Measures of genetic similarity and genetic distance. University of Texas Publications 7213, 145–153.Google Scholar
Smith, D.C., Lyons, S.A. & Berlocher, S.H. (1993) Production and electrophoretic variation of F1 hybrids between the sibling species Rhagoletis pomonella and R. cornivora. Entomologia Experimentalis et Applicata 69, 209–213.CrossRefGoogle Scholar
Sneath, P.H.A. & Sokal, R.R. (1973) Numerical taxonomy. San Francisco, W.H. Freeman and Co.Google Scholar
Starý, P. (1971) Biology of aphid parasitoids (Hymenoptera: Aphidiidae) with respect to integrated control. The Hague, Dr W. Junk.Google Scholar
Starý, P. (1973) A review of the Aphidius species (Hymenoptera, Aphidiidae) of Europe. Annotationes Zoologicae et Botanicae, Bratislava 84, 1–85.Google Scholar
Starý, P. (1993) The fate of released parasitoids (Hymenoptera, Braconidae, Aphidiinae) for biological control of aphids in Chile. Bulletin of Entomological Research 83, 633–639.CrossRefGoogle Scholar
Starý, P., Gonzalez, D. & Hall, J.C. (1980) Aphidius eadyi n. sp. (Hymenoptera: Aphidiidae), a widely distributed parasitoid of the pea aphid, Acyrthosiphon pisum (Harris) in the Palaearctic. Entomologica Scandinavica 11, 473–480.CrossRefGoogle Scholar
Swofford, D.L. (1989) BIOSYS-1 user'manual (release 1.7). University of Illinois, Champaign, Illinois, USA pp. 1–43.Google Scholar
Swofford, D.L. & Selander, R.K. (1981) BIOSYS-1. A FORTRAN program for the comprehensive analysis of electrophoretic data in population genetics and systematics. Journal of Heredity 72, 281–283.CrossRefGoogle Scholar
Tremblay, E. & Pennacchio, F. (1988) Speciation in aphidiine Hymenoptera. Advances in Parasitic Hymenoptera Research 1988, 139–146.Google Scholar
Unruh, T.R., White, W., Gonzalez, D., Gordh, G. & Luck, R.F. (1983) Heterozygosity and effective size in laboratory populations of Aphidius ervi (Hymenoptera: Aphidiidae). Entomophaga 28, 245–258.CrossRefGoogle Scholar
Unruh, T.R., White, W., Gonzalez, D. & Luck, R.F. (1986) Electrophoretic studies of parasitic Hymenoptera and implications for biological control. pp. 150–163in Patterson, R.S. and Rutz, D.A. (Eds) Biological control of muscoid flies. Miscellaneous Publications of the Entomological Society of America 61.Google Scholar
Unruh, T.R., Gonzalez, D. & Woolley, J.B. (1989) Genetic relationships among seventeen Aphidius (Hymenoptera: Aphidiidae) populations, including six species. Annals of the Entomological Society of America 82, 754–768.CrossRefGoogle Scholar
Walton, M.P., Loxdale, H.D. & Allen-Williams, L. (1990) Electrophoretic ‘keys’ for the identification of aphidiid parasitoids (Hymenoptera: Braconidae: Aphelinidae) of Sitobion avenae (F.) (Hemiptera: Aphididae). Biological Journal of the Linnean Society 40, 333–346.Google Scholar
Wilkerson, R.C., Parsons, T.J., Albright, D.G., Klein, T.A. & Braun, M.J. (1993) Random amplified polymorphic DNA (RAPD) markers readily distinguish cryptic mosquito species (Diptera; Culicidae: Anopheles). Insect Molecular Biology 1, 205–211.CrossRefGoogle ScholarPubMed
Workman, P.L. and Niswander, J.D. (1970) Population studies of south-western Indian tribes. II. Local genetic differentiation in the Papago. American Journal of Human Genetics 22, 24–49.Google Scholar
Wynne, I.R., Loxdale, H.D. & Brookes, C.P. (1992) Use of a cellulose acetate system for allozyme electrophoresis. pp. 494–499in Berry, R.J., Crawford, T.J. and Hewitt, G.M. (Eds) Genes in ecology. Oxford, Blackwells Scientific Publications.Google Scholar