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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

  • P. Atanassova (a1), C.P. Brookes (a1), H.D. Loxdale (a1) and W. Powell (a1)
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.

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COPYRIGHT: © Cambridge University Press 1998
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* Author for correspondence.
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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.
Avise, J.C. (1975) Systematic value of electrophoretic data. Systematic Zoology 23, 465–481.
Avise, J.C. (1977) Genetic differentiation during speciation. pp. 106–122in Ayala, F.J. (Ed.) Molecular evolution. Sunderland, Massachusetts, USA, Sinauer Associates, Inc.
Avise, J.C. (1994) Molecular markers, natural history and evolution. New York, Chapman and Hall.
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.
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.
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.
Chen, J-H., Gonzalez, D. & Luhman, J. (1990) A new species of Aphidius (Hymenoptera) attacking the pea aphid, Acyrthosiphon pisum. Entomophaga 35, 509–514.
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.
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.
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.
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.
Ferguson, A. (1980) Biochemical systematics and evolution. Glasgow and London, Blackie.
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.
Gawel, N.J. & Bartlett, A.C. (1993) Characterization of differences between whiteflies using RAPD—PCR. Insect Molecular Biology 2, 33–38.
Henry, C.S. (1994) Singing and cryptic speciation in insects. Trends in Ecology and Evolution 9, 388–392.
Hopper, K.R., Roush, R.T. & Powell, W. (1993) Management of genetics of biological-control introductions. Annual Review of Entomology 38, 27–51.
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.
Levene, H. (1949) On a matching problem arising in genetics. Annals of Mathematical Statistics 20, 91–94.
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.
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.
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.
Mackauer, M. & Starý, P. (1967) Hymenoptera, Ichnumonoidea, World Aphidiidae. Index of Entomophagous Insects. Paris: Le Francois.
Mayr, E. (1963) Animal species and evolution. Cambridge, Massachusetts, Harvard University Press.
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.
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.
Nei, M. (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 23, 341–369.
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.
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.
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.
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.
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.
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.
Powell, W. (1982) The identification of hymenopterous parasitoids attacking cereal aphids in Britain. Systematic Entomology 7, 465–473.
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.
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.
Pungerl, N.B. (1983) Variability in characters commonly used to distinguish Aphidius species (Hymenoptera: Aphidiidae) Systematic Entomology 8, 425–430.
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.
Richardson, B.J., Baverstock, P.R. & Adams, M. (1986) Allozyme electrophoresis. A handbook for animal systematics and population studies. London, Academic Press.
Rogers, J.S. (1972) Measures of genetic similarity and genetic distance. University of Texas Publications 7213, 145–153.
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.
Sneath, P.H.A. & Sokal, R.R. (1973) Numerical taxonomy. San Francisco, W.H. Freeman and Co.
Starý, P. (1971) Biology of aphid parasitoids (Hymenoptera: Aphidiidae) with respect to integrated control. The Hague, Dr W. Junk.
Starý, P. (1973) A review of the Aphidius species (Hymenoptera, Aphidiidae) of Europe. Annotationes Zoologicae et Botanicae, Bratislava 84, 1–85.
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.
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.
Swofford, D.L. (1989) BIOSYS-1 user'manual (release 1.7). University of Illinois, Champaign, Illinois, USA pp. 1–43.
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.
Tremblay, E. & Pennacchio, F. (1988) Speciation in aphidiine Hymenoptera. Advances in Parasitic Hymenoptera Research 1988, 139–146.
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.
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.
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.
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.
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.
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.
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.
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