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Biological and genetic characterization of morphologically similar Therioaphis trifolii (Hemiptera: Aphididae) with different host utilization

Published online by Cambridge University Press:  10 July 2009

P. Sunnucks ,
F. Driver ,
W. V. Brown ,
M. Carver ,
D. F. Hales  and
W. M. Milne
P. Sunnucks
Affiliation:
School of Biological Sciences, Macquarie University, NSW 2109, Australia
F. Driver
Affiliation:
CSIRO Division of Entomology, GPO Box 1700, Canberra, ACT 2601, Australia
W. V. Brown
Affiliation:
CSIRO Division of Entomology, GPO Box 1700, Canberra, ACT 2601, Australia
M. Carver
Affiliation:
CSIRO Division of Entomology, GPO Box 1700, Canberra, ACT 2601, Australia
D. F. Hales
Affiliation:
School of Biological Sciences, Macquarie University, NSW 2109, Australia
W. M. Milne*
Affiliation:
CSIRO Division of Entomology, GPO Box 1700, Canberra, ACT 2601, Australia
*
*Author for correspondence.
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Abstract

The aphid Therioaphis trifolii (Monell) is indigenous to the western Palaearctic region, where it colonizes lucerne (alfalfa), clovers and related legumes. A form of the species, T. trifolii f. maculata (the spotted alfalfa aphid, SAA), has been known in Australia since 1977, feeding almost exclusively on Medicago sativa (lucerne). Since 1989, T. trifolii has been found in Australia colonizing Trifolium subterraneum (subclover). We have compared samples of T. trifolii in Australia collected on lucerne and subclover using several techniques: survival and reproduction on different hosts, morphology, cuticular hydrocarbon profile, karyology, and a combination of RAPD-PCR and mitochondrial DNA (cytochrome oxidase) genetic markers. Whereas there were no distinct differences in cuticular hydrocarbons and karyology, we found significant correlated differences between the host on which aphids were collected, some morphological characters, and the genotypes of the aphids. Aphids collected from lucerne were always of one genetic type, and nearly all those from subclover were of another. Both groups of aphids are morphologically distinguishable from the yellow clover aphid (YCA), the other form of the species recognized so far. We conclude that the clover-colonizers (spotted clover aphid, SCA) and the lucerne-colonizers (SAA) are each host-restricted forms (biotypes) of T. trifolii. Estimates of mtDNA divergence are in the range of conspecific to closely congeneric, as compared with other insects including aphids. We developed simple diagnostic DNA tests to distinguish the two pest aphids.

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Type
Original Articles
Information
Bulletin of Entomological Research , Volume 87 , Issue 4 , August 1997 , pp. 425 - 436
Copyright
Copyright © Cambridge University Press 1997

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References

Avise, J.C. (1989) Gene trees and organismal histories: a phylogenetic approach to population biology. Evolution 43, 1192–1208.CrossRefGoogle ScholarPubMed
Beckenbach, A., Wei, Y.W. & Liu, H. (1993) Relationships in the Drosophila obscura species group, inferred from mitochondrial cytochrome oxidase II sequences. Molecular Biology and Evolution 10, 619–634.Google Scholar
Black, W.C., DuTeau, N.M., Puterka, G.J., Nechols, J.R. & Pettorini, J.M. (1992) Use of the random amplified polymorphic DNA polymerase chain reaction (RAPD-PCR) to detect DNA polymorphisms in aphids (Homoptera: Aphididae). Bulletin of Entomological Research 82, 151–159.CrossRefGoogle Scholar
Blackman, R.L., Halbert, S.E. & Carroll, T.W. (1990) Association between karyotype and host plant in corn leaf aphid (Homoptera: Aphididae) in the northwestern United States. Environmental Entomology 19, 609–611.CrossRefGoogle Scholar
Brown, J.M., Pellmyr, O., Thompson, J.N. & Harrison, R.G. (1994) Phylogeny of Greya (Lepidoptera: Prodoxidae), based on nucleotide sequence variation in mitochondrial cytochrome oxidase I and II: congruence with morphological data. Molecular Biology and Evolution 11, 128–141.Google ScholarPubMed
Brown, P.A. & Blackman, R.L. (1988) Karyotype variation in the corn leaf aphid, Rhopalosiphum maidis (Fitch), species complex (Hemiptera: Aphididae) in relation to host plant and morphology. Bulletin of Entomological Research 78, 351–363.CrossRefGoogle Scholar
Brown, W.V., Watson, J.A.L., Carter, F.L., Lacey, M.J., Barrett, R.A. & McDaniel, C.A. (1990) Preliminary examination of cuticular hydrocarbons as chemotaxonomic characters for some Australian species of Coptotermes (Isoptera: Rhinotermitidae). Sociobiology 16, 305–328.Google Scholar
Brown, W.V., Watson, J.A.L. & Lacey, M.J. (1996) A chemotaxonomic survey using cuticular hydrocarbons of some species of the Australian harvester termite genus Drepanotermes (Isoptera: Termitidae). Sociobiology 27, 181–197.Google Scholar
Carver, M. (1978) The scientific nomenclature of the spotted alfalfa aphid (Homoptera: Aphididae). Journal of the Australian Entomological Society 17, 287–288.CrossRefGoogle Scholar
De Barro, P.J., Sherratt, T.N., Brookes, C.P., David, O. & Maclean, N. (1995a) 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 of London. Series B 262, 321–327.Google ScholarPubMed
De Barro, P.J., Sherratt, T.N., Carvalho, G.R., Nicol, D., Iyengar, A. & Maclean, N. (1995b) Geographic and micro-geographic genetic differentiation in two aphid species over southern England using the multilocus (GATA)4 probe. Molecular Ecology 4, 375–384.CrossRefGoogle Scholar
DeSalle, R., Freedman, T., Prager, E.M. & Wilson, A.C. (1987) Tempo and mode of sequence evolution in mitochondrial DNA of Hawaiian Drosophila. Journal of Molecular Evolution 26, 157–164.Google Scholar
Dickson, R.C. (1959) On the identity of the spotted alfalfa aphid in North America. Annals of the Entomological Society of America 52, 63–68.CrossRefGoogle Scholar
Dickson, R.C., Laird, E.F.J. & Pesho, G.R. (1955) The spotted alfalfa aphid (yellow clover aphid on alfalfa). Hilgardia 24, 93–118.CrossRefGoogle Scholar
Dillwith, J.W., Bergman, D.K., Fargo, W.S., Puterka, G.J. & Peters, D.C. (1991) Cuticular hydrocarbons of greenbug biotypes. pp. 297in Peters, D.C., Webster, J.A. & Chlouber, C.S. (Eds) Aphid–plant interactions: populations to molecules. Oklahoma State University.Google Scholar
Eastop, V.F. (1973) Biotypes of aphids. pp. 40–51in Lowe, A.D. (Ed.) Perspectives in aphid biology. The Entomological Society of New Zealand, Bulletin No. 2.Google Scholar
Fenton, B., Birch, A.N.E., Malloch, G., Woodford, J.A.T. & Gonzalez, C. (1994) Molecular analysis of ribsomal DNA from the aphid Amphorophora idaei and an associated fungal organism. Insect Molecular Biology 3, 183–189.CrossRefGoogle Scholar
Franzmann, B.A., Scattini, W.J., Rynne, K.P. & Johnson, B. (1979) Lucerne aphid effects of 18 pasture legumes in Southern Queensland: a glasshouse study. Australian Journal of Experimental Agriculture and Animal Husbandry 19, 59–63.CrossRefGoogle Scholar
Fukatsu, T. & Ishikawa, H. (1994) Differentiation of aphid clones by arbitrarily primed polymerase chain reaction (AP-PCR) DNA fingerprinting. Molecular Ecology 3, 187–192.Google Scholar
Gilbert, D. (1992) SeqApp-1.9. Via anonymous ftp to ftp.bio.indiana.edu, in folder/molbio/seqapp, as seqapp.hqx.Google Scholar
Hales, D.F., Tomiuk, J., Wöhrmann, K. & Sunnucks, P. (1997) Evolutionary and genetic aspects of aphid biology: a review. European Journal of Entomology 94, 1–55.Google Scholar
Holtkamp, R.H., Edge, V.E., Dominiak, B.C. & Walters, P.J. (1992) Insecticide resistance in Therioaphis trifolii f. maculata (Hemiptera: Aphididae) in Australia. Journal of Economic Entomology 85, 1576–1582.Google Scholar
Hughes, R.D., Woolcock, L.T., Roberts, J.A. & Hughes, M.A. (1987) Biological control of spotted alfalfa aphid, Therioaphis trifolii f. maculata, on lucerne crops in Australia, by the introduced parasitic hymenopteran Trioxys complanatus. Journal of Applied Ecology 24, 515–537.CrossRefGoogle Scholar
Liu, H. & Beckenbach, A.T. (1992) Evolution of the mitochondrial cytochrome oxidase II gene among 10 orders of insects. Molecular Phylogenetics and Evolution 1, 41–52.Google Scholar
Lockey, K.H. (1988) Lipids of the insect cuticle: origin, composition and function. Comparative Biochemistry and Physiology 89B, 595–645.Google Scholar
Loxdale, H.D., Hardie, J., Halbert, S., Foottit, R., Kidd, N.A. & Carter, C.I. (1993) The relative importance of short- and long-range movement of flying aphids. Biological Reviews 68, 291–311.CrossRefGoogle Scholar
Maddison, W.P. & Maddison, D.R. (1992) MacClade: analysis of phylogeny and character evolution, version 3.0. Sunderland, Massachusetts, Sinauer Associates.Google Scholar
Milne, W.M. & Wellings, P.W. (1991) Occurrence of sexual morphs of Therioaphis trifolii (Monell) maculata (Hemiptera: Aphididae) in the field. Journal of the Australian Entomological Society 30, 95–96.Google Scholar
Monell, J. (1882) Notes on Aphididae. Canadian Entomologist 14, 13–16.CrossRefGoogle Scholar
Moran, N.A., Baumann, P. & von Dohlen, C. (1994) Use of DNA sequences to reconstruct the history of the association between members of the Sternorrhyncha (Homoptera) and their bacterial endosymbionts. European Journal of Entomology 91, 79–83.Google Scholar
Moritz, C., Dowling, T.E. & Brown, W.M. (1987) Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annual Review of Ecology and Systematics 18, 269–292.Google Scholar
Passlow, T. (1977) The spotted alfalfa aphid, a new pest of lucerne. Queensland Agricultural Journal 103, 329–330.Google Scholar
Peters, D.C. & Painter, R.H. (1957) A general classification of available seeded legumes as hosts for three aphids of the ‘yellow clover aphids complex’. Journal of Economic Entomology 50, 231–235.Google Scholar
Peters, D.C. & Painter, R.H. (1958) Studies on the biologies of three related legume aphids in relation to their host plants. Kansas Agricultural Experimental Station Technical Bulletin 93, 44.Google Scholar
Puterka, G.J. & Peters, D.C. (1990) Sexual reproduction and inheritance of virulence in the greenbug (Schizaphis graminum (Rondani). pp. 289–318in Campbell, R.K. & Eikenbary, R.D. (Eds) Aphid plant genotype interactions. Amsterdam, Elsevier.Google Scholar
Puterka, G.J., Black, W.C. IV, Steiner, W.M. & Burton, R.L. (1993) Genetic variation and phylogenetic relationships among worldwide collections of the Russian wheat aphid, Diuraphis noxia (Mordvilko), inferred from allozyme and RAPD-PCR markers. Heredity 70, 604–618.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular cloning: a laboratory manual. New York, Cold Spring Harbor Laboratory Press.Google Scholar
Sokal, R.R. & Rohlf, F.J. (1981) Biometry. San Francisco, W.H. Freeman & Co.Google Scholar
Sperling, F.A.H. & Hickey, D.A. (1994) Mitochondrial DNA sequence variation in the spruce budworm species complex (Choristoneura: Lepidoptera). Molecular Biology and Evolution 11, 656–665.Google Scholar
Stern, D.L. (1994) A phylogenic analysis of soldier evolution in the aphid family Hormaphididae. Proceedings of the Royal Society of London. Series B 256, 203–209.Google Scholar
Sunnucks, P. & Hales, D.F. (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Molecular Biology and Evolution 13, 510–524.Google Scholar
Welsh, J. & McClelland, M. (1990) Fingerprinting genomes using PCR with arbitrary primers. Nucleic Acids Research 18, 7213–7219.CrossRefGoogle ScholarPubMed
Williams, J.G.K., Rubelik, A.R., Livak, K.J., Rafalski, J.A. & Tingey, S.V. (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Research 18, 6531–6535.Google Scholar
Winship, P.R. (1989) An improved method for directly sequencing PCR amplified material using DMSO. Nucleic Acids Research 17, 1266.Google Scholar