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Genetic variability within and between English populations of the damson–hop aphid, Phorodon humuli (Hemiptera: Aphididae), with special reference to esterases associated with insecticide resistance

Published online by Cambridge University Press:  10 July 2009

H.D. Loxdale ,
C.P. Brookes ,
I.R. Wynne  and
S.J. Clark
H.D. Loxdale*
Affiliation:
Entomology and Nematology Department
C.P. Brookes
Affiliation:
Entomology and Nematology Department
I.R. Wynne
Affiliation:
Entomology and Nematology Department
S.J. Clark
Affiliation:
Statistics Department IACR-Rothamsted, Harpenden, Hertfordshire, AL5 2JQ, UK
*
*01582 760981[email protected]
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Abstract

The damson–hop aphid, Phorodon humuli (Schrank), is a serious pest of hops in England. It is holocyclic (with obligatory sexual phase) and host alternating. From suction trap data, P. humuli aerial densities are known to be greatest in the main hop growing regions of Herefordshire and Kent (mid-west and south-east England, respectively), some 260 km apart. The aphid is now resistant to several insecticides. This is in part conferred by elevated carboxylesterase activity, ranging from low in susceptible to high in very resistant strains. Enzyme markers, including carboxylesterases (EST-4 to -7), separated electrophoretically from individual insects, have been used to examine the degree of genetic heterogeneity among P. humuli sub-populations on both its hosts – Prunus spp. (primary overwintering host) and hops, Humulus lupulus (secondary summer host). The esterase data revealed heterogeneity among subpopulations collected from wild, unsprayed hosts in regions less than 30 km in area, with a higher mean frequency of elevated esterase variants in the commercial hop growing regions of Herefordshire and Kent, compared with samples from a non-commercial region around Rothamsted. Esterase distributions remained similar over consecutive years. Similarly, allele and genotype frequencies for another enzyme (6-phosphogluconate dehydrogenase, 6-PGD) were also heterogeneous among subpopulations sampled at less than 30 km apart (especially from Prunus) in each of the three regions surveyed, whilst allele and genotype frequencies sometimes remained stable over a number of summers. In addition, 6-PGD genotype frequencies were mostly congruent with Hardy-Weinberg expectations, even for parthenogenetically-reproducing aphids colonizing hops. These data suggest that the 6-PGD alleles tested are selectively neutral; that gene flow (=migration) is restricted between aphid populations, even within a single region (≤ 30 km) and, that the autumn migration from hops to Prunus is probably of shorter range (perhaps less than 20 km) compared with the spring migration from Prunus to hops.

Type
Review Article
Information
Bulletin of Entomological Research , Volume 88 , Issue 5 , October 1998 , pp. 513 - 526
Copyright
Copyright © Cambridge University Press 1998

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References

Beck, A.K. & Büchi, R. (1980) Esterasetest zum Nachweis der Insektizidresistenz bei der Hopfenblattlaus, Phorodon humuli Schrk. Zeitschrift für Angewandte Entomologie 89, 113–121.CrossRefGoogle Scholar
Birch, A.N.E., Fenton, B., Malloch, G., Jones, A.T., Phillips, M.S., Harrower, B.E., Woodford, J.A.T. & Catley, M.A. (1994) Ribosomal spacer length variability in the large raspberry aphid, Amphorophora idaei (Aphidinae: Macrosiphini). Insect Molecular Biology 3, 239–245.Google Scholar
Blackman, R.L. (1981) Species, sex and parthenogenesis. pp. 75–85 in Forey, P.L. (Ed.) The evolving biosphere. British Museum (Natural History), Cambridge University Press.Google Scholar
Blackman, R.L. & Eastop, V.F. (1984) Aphids on the world's crops: an identification and information guide. Chichester, John Wiley & Sons.Google Scholar
Blackman, R.L. & Eastop, V.F. (1994) Aphids on the world's trees: an identification and information guide. Wallingford, CAB International.Google Scholar
Blackman, R.L. & Spence, J.M. (1992) Electrophoretic distinction between the peach–potato aphid, Myzus persicae, and the tobacco aphid, M. nicotianae (Homoptera: Aphididae). Bulletin of Entomological Research 82, 161–165.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
Brookes, C.P. & Loxdale, H.D. (1987) Survey of enzyme variation in British populations of Myzus persicae (Sulzer) (Hemiptera: Aphididae) on crops and weed hosts. Bulletin of Entomological Research 77, 83–89.Google Scholar
Büchi, R. (1981) Evidence that resistance against pyrethroids in aphids Myzus persicae and Phorodon humuli is not correlated with high carboxylesterase activity. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz 88, 631–634.Google Scholar
Campbell, C.A.M. (1985) Hops (Humulus lupulus L.) pp. 192–194in Hussey, N.W. & Scopes, N. (Eds) Biological pest control: the glasshouse experience. Poole, Blandford Press.Google 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
Daly, J.C. (1989) The use of electrophoretic data in a study of gene flow in the pest species Heliothis armigera (Hübner) and H. punctigera Wallengren (Lepidoptera: Noctuidae). pp. 115–141in Loxdale, H.D. & den Hollander, J. (Eds) Electrophoretic studies on agricultural pests. Oxford, Clarendon Press.Google Scholar
De Barro, P.J., Sherratt, T.N., Carvalho, G.R., Maclean, N., Nicol, D. & Iyengar, A. (1994) An analysis of secondary spread by putative clones of Sitobion avenae within a Hampshire wheat field using the multilocus (GATA)4 probe. Insect Molecular Biology 3, 253–260.CrossRefGoogle Scholar
De Barro, P.J., Sherratt, T.N., Carvalho, G.R., Maclean, N., Nicol, D. & Iyengar, A. (1995a) The use of the multilocus (GATA)4 probe to investigate geographic and micro-geographic genetic differentiation in two aphid species over southern England. Molecular Ecology 4, 375–382.CrossRefGoogle Scholar
De Barro, P.J., Sherratt, T.N., Brookes, C.P., David, O. & Maclean, N. (1995b) Spatial and temporal genetic variation in British field populations of the grain aphid, Sitobion avenae (F.) (Hemiptera: Aphididae) studied using RAPD-PCR. Proceedings of the Royal Society,London, Series B 262, 321–327.CrossRefGoogle Scholar
Devonshire, A.L., Moores, G.D. & ffrench-Constant, R.H. (1986) Detection of insecticide resistance by immunological estimation of carboxylesterase activity in Myzus persicae (Sulzer) and cross reaction of the anitiserum with Phorodon humuli (Schrank) (Hemiptera: Aphididae). Bulletin of Entomological Research 76, 97–107.Google Scholar
Eggers-Schumacher, H.A. & Sander, E. (1988) Spatial and seasonal genetic (allozyme) variation within field populations of Phorodon humuli Schrank (Homoptera: Aphididae) on winter and summer hosts in southern Germany (FGR). The Entomologist 107, 110–121.Google Scholar
Eppler, A. (1988) Untersuchungen zur Wirtswahl von Phorodon humuli Schrk. II. Besiedlung der Winterwirte. Anzeiger für Schädlingskunde, Pflanzenschutz, Umweltschutz 61, 44–48.Google Scholar
Eppler, A. (1995) Ecology of aphids on hops and its significance on spread of hop viruses. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz 102, 2–15.Google Scholar
ffrench-Constant, R.H., Devonshire, A.L. & White, R.P. (1988) Spontaneous loss and reselection of resistance in extremely resistant Myzus persicae (Sulzer). Pesticide Biochemistry and Physiology 30, 1–10.CrossRefGoogle Scholar
Foster, S.P., Harrington, R., Devonshire, A.L., Denholm, I., Devine, G.L. & Kenward, M.G. (1996) Comparative survival of insecticide-susceptible and resistant peach–potato aphids, Myzus persicae (Sulzer) (Hemiptera: Aphididae), in low temperature field trials. Bulletin of Entomological Research 86, 17–27.CrossRefGoogle Scholar
Foster, S.P., Harrington, R., Devonshire, A.L., Denholm, I., Clark, S.J. & Mugglestone, M.A. (1997) Evidence for a possible fitness trade-off between insecticide resistance and the low temperature movement that is essential for survival of UK populations of Myzus persicae (Hemiptera: Aphididae). Bulletin of Entomological Research 87, 573–579.CrossRefGoogle Scholar
Foster, S.P., Denholm, I., Harling, Z.K., Moores, G.D. & Devonshire, A.L. (1998) Intensification of insecticide resistance in UK field populations of the peach–potato aphid, Myzus persicae (Hemiptera: Aphididae) in 1996. Bulletin of Entomological Research 88, 127–130.Google Scholar
Genstat 5 Committee (1993) Genstat 5 Release 3 reference manual. Oxford, Clarendon Press.Google Scholar
Hardie, J. (1993) Flight behaviour in migrating insects. Journal of Agricultural Entomology 10, 239–245.Google Scholar
Hebert, P.D.N., Finston, T.L. & Foottit, R. (1991) Patterns of genetic diversity in the sumac gall aphid, Melaphis rhois. Genome 34, 757–762.Google Scholar
Helden, A.J. (1993) Overwintering, migration and migratory morphs of Sitobion avenae (F.). 211 pp. PhD thesis, University of East Anglia, UK.Google Scholar
Herdeg, G. (1982) Investigations on the insecticide resistance of the damson–hop aphid (Phorodon humuli Schrank) in the hop growing region of Tettnang. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz 89, 468–474.Google Scholar
Hrdý, I. (1984) Stability of resistance to insecticides and the spreading of hop aphid R-biotypes in Czechoslovakia. IOBC/WPRS Bulletin 7, 2–9.Google Scholar
Irwin, M.E. & Thresh, J.M. (1988) Long-range aerial dispersal of cereal aphids as virus vectors in North America. Philosophical Transactions of the Royal Society, London. Series B 321, 421–446.Google Scholar
Lewis, G.A. & Madge, D.S. (1984) Esterase activity and associated insecticide resistance in the damson–hop aphid, Phorodon humuli (Schrank) (Hemiptera: Aphididae). Bulletin of Entomological Research 74, 227–238.Google Scholar
Lorriman, F. & Llewellyn, M. (1983) The growth and reproduction of hop aphid (Phorodon humuli) biotypes resistant and susceptible to insecticides. Acta Entomologica Bohemoslovaca 80, 87–95.Google Scholar
Loxdale, H.D. (1990) Estimating levels of gene flow between natural populations of cereal aphids (Homoptera: Aphididae). Bulletin of Entomological Research 80, 331–338.Google Scholar
Loxdale, H.D. (1994) Isozyme and protein profiles of insects of agricultural and horticultural importance. pp. 337–375in Hawksworth, D.L. (Ed.) The identification and characterization of pest organisms. Wallingford, CAB International.Google Scholar
Loxdale, H.D. & Brookes, C.P. (1988) Electrophoretic study of enzymes from cereal aphid populations. V. Spatial and temporal genetic similarity between holocyclic populations of the bird-cherry oat aphid Rhopalosiphum padi (L.) (Hemiptera: Aphididae) in Britain. Bulletin of Entomological Research 78, 241–249.Google Scholar
Loxdale, H.D. & Brookes, C.P. (1989) Use of genetic markers (allozymes) to study the structure, overwintering and dynamics of pest aphid populations. pp. 231–270in Loxdale, H.D. & den Hollander, J. (Eds) Electrophoretic studies on agricultural pests. Systematics Association Special Volume No. 39, Oxford, Clarendon Press.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.Google Scholar
Loxdale, H.D. & Brookes, C.P. (1990) Genetic stability within and restricted migration (gene flow) between local populations of the blackberry–grain aphid Sitobion fragariae in south-east England. Journal of Animal Ecology 59, 495–512.CrossRefGoogle Scholar
Loxdale, H.D., Tarr, I.J., Weber, C.P., Brookes, C.P., Digby, P.G.N. & Castañera, P. (1985) Electrophoretic study of enzymes from cereal aphid populations. III. Spatial and temporal genetic variation of populations of Sitobion avenae (F.) (Hemiptera: Aphididae). Bulletin of Entomological Research 75, 121–141.Google Scholar
Loxdale, H.D., Hardie, J., Halbert, S., Foottit, R., Kidd, N.A.C. & Carter, C.I. (1993) The relative importance of short- and long-range movement of flying aphids. Biological Reviews 68, 291–311.Google Scholar
Loxdale, H.D., Brookes, C.P. & De Barro, P.J. (1996) Application of novel molecular markers (DNA) in agricultural entomology. pp. 149–198in Symondson, W.O.C. & Liddell, J.E. (Eds) The ecology of agricultural pests: biochemical approaches. Systematics Association Special Volume No. 53, Chapman & Hall.Google Scholar
Majerus, M., Amos, W. & Hurst, G. (1996) Evolution: The four billion year war. Harlow, Essex, Longmans.Google Scholar
McCauley, D.E. & Goff, P.W. (1998) Intrademic genetic structure and natural selection in insects. pp. 181–204in Mopper, S. & Strauss, S.Y. (Eds) Genetic structure and local adaptation in natural insect populations. New York, Chapman & Hall.Google Scholar
Muir, R.C. (1979) Insecticide resistance in damson–hop aphid, Phorodon humuli in commercial hop gardens in Kent. Annals of Applied Biology 92, 1–9.CrossRefGoogle Scholar
Peterson, M.A. & Denno, R.F. (1998) Life-history strategies and the genetic structure of phytophagous insect populations. pp. 263–322in Mopper, S. & Strauss, S.Y. (Eds) Genetic structure and local adaptation in natural insect populations. New York, Chapman & Hall.CrossRefGoogle 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
Simon, J.C. & Hebert, P.D.N. (1995) Patterns of genetic variation among Canadian populations of the bird cherry–oat aphid, Rhopalosiphum padi L. (Homoptera: Aphididae). Heredity 74, 346–353.CrossRefGoogle Scholar
Simon, J.C., Carrel, E., Hebert, P.D.N., Dedryver, C.A., Bonhomme, J. & Le Gallic, J.F. (1996) Genetic diversity and mode of reproduction in French populations of the aphid Rhopalosiphum padi L. Heredity 76, 305–313.Google Scholar
Strauss, S.Y. & Karban, R. (1998) The strength of selection: intraspecific variation in host-plant quality and the fitness of herbivores. pp. 156–177in Mopper, S. & Strauss, S.Y. (Eds) Genetic structure and local adaptation in natural insect populations. New York, Chapman & Hall.Google Scholar
Swofford, D.L. (1989) BIOSYS-1 user's manual (Release 1.7). University of Illinois, Champaign, Illinois.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
Taimr, L. & Kříž, J. (1978) Stratiform drift of the hop aphid (Phorodon humuli Schrank). Zeitschrift für Angewandte Entomologie 86, 71–79.CrossRefGoogle Scholar
Tatchell, G.M., Parker, S.J. & Woiwod, I.P. (1983) Synoptic monitoring of migrant insect pests in Great Britain and western Europe IV. Host plants and their distribution for pest aphids in Great Britain. Rothamsted Experimental Station, Harpenden, Hertfordshire, U.K. Report for 1982. Part 2, pp. 45–159.Google Scholar
Tatchell, G.M., Plumb, R.T. & Carter, N. (1988) Migration of alate morphs of the bird cherry aphid (Rhopalosiphum padi) and implications for the epidemiology of barley yellow dwarf virus. Annals of Applied Biology 112, 1–11.CrossRefGoogle Scholar
Taylor, L.R. (1965) Flight behaviour and aphid migration. Proceedings North Central Branch – Entomological Society of America 20, 9–19.Google Scholar
Taylor, L.R., Woiwod, I.P. & Taylor, R.A.J. (1979) The migratory ambit of the hop aphid and its significance in aphid population dynamics. Journal of Animal Ecology 48, 955–972.Google Scholar
Taylor, L.R., French, R.A., Woiwod, I.P., Dupuch, M.J. & Nicklen, J. (1981) Synoptic monitoring for migrant insect pests in Great Britain and western Europe. I. Establishing expected values for species content, population stability and phenology of aphids and moths. Rothamsted Experimental Station. Report for 1980, Part, 2, pp. 41–104.Google Scholar
Tomiuk, J. & Wöhrmann, K. (1980) Enzyme variability in populations of aphids. Theoretical and Applied Genetics 57, 125–127.CrossRefGoogle ScholarPubMed
Wachendorff, U. & Zoebelein, G. (1988) Diagnosis of insecticide resistance in Phorodon humuli (Homoptera: Aphididae). Entomologia Generalis 13, 145–155.Google Scholar
Walton, M.P., Loxdale, H.D. & Allen-Williams, L. (1990) 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.Google Scholar
Wilding, N., Mardell, S.K., Brookes, C.P. & Loxdale, H.D. (1993) The use of polyacrylamide gel electrophoresis of enzymes to identify entomophthoralean fungi in aphid hosts. Journal of Invertebrate Pathology 62, 268–272.CrossRefGoogle Scholar
Woiwod, I.P. & Harrington, R. (1994) Flying in the face of change; the Rothamsted Insect Survey. pp. 321–342in Leigh, R.A. & Johnston, A.E. (Eds) Long-term experiments in agricultural and ecological sciences. Wallingford, CAB International.Google Scholar
Workman, P.L. & 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
Wright, S. (1978) Evolution and the genetics of populations, Vol. 4. Variability within and among natural populations. University of Chicago, Chicago.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. & Hewitt, G.M. (Eds) Genes in ecology. Oxford, Blackwells Scientific Publications.Google Scholar
Wynne, I.R., Howard, J.J., Loxdale, H.D. & Brookes, C.P. (1994) Population genetic structure during aestivation in the sycamore aphid Drepanosiphum platanoidis (Hemiptera: Drepanosiphidae). European Journal of Entomology 91, 375–383.Google Scholar