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Genotypic diversity of the cotton-melon aphid Aphis gossypii (Glover) in Tunisia is structured by host plants

Published online by Cambridge University Press:  07 February 2008

K. Charaabi ,
J. Carletto ,
P. Chavigny ,
M. Marrakchi ,
M. Makni  and
F. Vanlerberghe-Masutti
K. Charaabi
Affiliation:
Laboratoire de Génétique Moléculaire, Immunologie et Biotechnologie, Faculté des Sciences de Tunis, 2092 El Manar, Tunisia
J. Carletto
Affiliation:
UMR 1112 INRA UNSA, équipe ‘Biologie des Populations en Interaction’, 06903 Sophia Antipolis, France
P. Chavigny
Affiliation:
UMR 1112 INRA UNSA, équipe ‘Biologie des Populations en Interaction’, 06903 Sophia Antipolis, France
M. Marrakchi
Affiliation:
Laboratoire de Génétique Moléculaire, Immunologie et Biotechnologie, Faculté des Sciences de Tunis, 2092 El Manar, Tunisia
M. Makni
Affiliation:
Laboratoire de Génétique Moléculaire, Immunologie et Biotechnologie, Faculté des Sciences de Tunis, 2092 El Manar, Tunisia
F. Vanlerberghe-Masutti*
Affiliation:
UMR 1112 INRA UNSA, équipe ‘Biologie des Populations en Interaction’, 06903 Sophia Antipolis, France
*
*Author for correspondence Fax: +33 492 386 401 E-mail: [email protected]
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Abstract

The study of intraspecific variation with respect to host plant utilization in polyphagous insects is crucial for understanding evolutionary patterns of insect-plant interactions. Aphis gossypii (Glover) is a cosmopolitan and extremely polyphagous aphid species. If host plant species or families constitute selective regimes to these aphids, genetic differentiation and host associated adaptation may occur. In this study, we describe the genetic structure of A. gossypii collected in six localities in Tunisia on different vegetable crops, on citrus trees and on Hibiscus. The aim was to determine if the aphid populations are structured in relation to the host plants and if such differentiation is consistent among localities. The genetic variability of A. gossypii samples was examined at eight microsatellite loci. We identified only 11 multilocus genotypes among 559 individuals. Significant deviations from Hardy-Weinberg equilibrium, linkage disequilibria and absence of recombinant genotypes, confirmed that A. gossypii reproduces by continuous apomictic parthenogenesis. Genetic differentiation between localities was not significant, whereas a strong differentiation was observed between host plant families (0.175<FST<0.691). The great majority of aphids exhibited one of three predominant multilocus genotypes that were repeatedly and respectively associated to the three plant families, Cucurbitaceae, Solanaceae and Rutaceae, demonstrating host specialization in A. gossypii. These specialized genotypes were simultaneously found with other clones on Hibiscus, suggesting that this perennial host could act as a refuge plant between two vegetable crop seasons.

Keywords

aphidAphis gossypiigenetic structurehost-plant specializationmicrosatelliteobligate parthenogenesis
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 98 , Issue 4 , August 2008 , pp. 333 - 341
Copyright
Copyright © 2008 Cambridge University Press

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References

Ahmad, M., Arif, M.I. & Denholm, I. (2003) High resistance of field populations of the cotton aphid Aphis gossypii Glover (Homoptera: Aphididae) to pyrethroid insecticides in Pakistan. Journal of Economic Entomology 96, 875–878.Google Scholar
Andrews, M.C., Callaghan, A., Field, L.M., Williamson, M.S. & Moores, G.D. (2004) Identification of mutations conferring insecticide-insensitive AChE in the cotton-melon aphid, Aphis gossypii Glover. Insect Molecular Biology 13, 555–561.Google Scholar
Anstead, J.A., Burd, J.D. & Shufran, K.A. (2002) Mitochondrial DNA sequence divergence among Schizaphis graminum (Hemiptera: Aphididae) clones from cultivated and nom-cultivated hosts: haplotype and host associations. Bulletin of Entomological Research 92, 17–24.Google Scholar
Ben Halima-Kamel, M. & Ben Hamouda, M.H. (2004) Aphids of fruit trees in Tunisia. pp. 119–123in Simon, J.C., Dedryver, C.A., Rispe, C. & Hullé, M. (Eds) Aphids in a New Millenium. Paris, INRA Editions.Google Scholar
Blackman, R.L. (1972) The inheritance of life cycle differences in Mysus persicae (Sulz) (Hem., Aphididae). Bulletin of Entomological Research 62, 281–294.CrossRefGoogle Scholar
Blackman, R.L. & Eastop, V.F. (1984) Aphids in the World's Crops: An Identification Guide. 466 pp. Chichester, UK, John Wiley and Sons.Google Scholar
Brévault, T., Carletto, J., Linderme, D. & Vanlerberghe-Masutti, F.Genetic diversity of the cotton aphid, Aphis gossypii, in the unstable environment of a cotton growing area. Agricultural and Forest Entomology, in press.Google 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
Caillaud, M.C. & Via, S. (2000) Specialized feeding behavior influences both ecological specialization and assortative mating in sympatric host races of pea aphids. The American Naturalist 156, 606–621.Google Scholar
De Barro, P.J., Sherratt, T.N., Carvalho, G.R., Nicol, D., Iyengar, A. & Maclean, N. (1995) Geographic and microgeographic genetic differentiation in two aphid species over southern England using the multilocus (GATA)4 probe. Molecular Ecology 4, 375–382.CrossRefGoogle Scholar
Dedryver, C.A., Le Gallic, J.F., Gauthier, J.P. & Simon, J.C. (1998) Life-cycle in the cereal aphid Sitobion avenae F. polymorphism and comparaison of life history traits associated with sexuality. Ecological Entomology 23, 123–132.Google Scholar
Deguine, J.-P., Martin, J. & Leclant, F. (1999) Extreme polyphagy of Aphis gossypii Glover (Hemiptera: Aphididae) during the dry season in northern Cameroon. Insect Science and its Application 19, 23–36.Google Scholar
Delorme, R., Augé, D., Bethenod, M.-T. & Villatte, F. (1997) Insecticide resistance in a strain of Aphis gossypii from Southern France. Pesticide Science 49, 90–96.Google Scholar
Devonshire, A.L., Field, L.M., Foster, S.P., Moores, G.D., Williamson, M.S. & Blackman, R.L. (1998) The evolution of insecticide resistance in the peach–potato aphid, Myzus persicae. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 353, 1677–1684.CrossRefGoogle Scholar
Dixon, A.F.G. (1985) Aphid Ecology. 157 pp. New York, Chapman and Hall.Google Scholar
Doyle, J.J. & Doyle, J.L. (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Photochemistry Bulletin 19, 11–15.Google Scholar
Ebert, T.A. & Cartwright, B. (1997) Biology and ecology of Aphis gossypii Glover (Homoptera: Aphididae). Southwestern Entomologist 22, 116–153.Google Scholar
Frantz, A., Plantegenest, M., Mieuzet, L. & Simon, J.C. (2006) Ecological specialization correlates with genotypic differentiation in sympatric host-populations of the pea aphid. Journal of Evolutionary Biology 19, 392–401.Google Scholar
Fuller, S.J., Chavigny, P., Lapchin, L. & Vanlerberghe-Masutti, F. (1999) Variation in clonal diversity in glasshouse infestations of the aphid, Aphis gossypii, in southern France. Molecular Ecology 8, 1867–1877.CrossRefGoogle ScholarPubMed
Goudet, J. (1995) Fstat version 1.2: a computer program to calculate Fstatistics. Journal of Heredity 86, 485–486.Google Scholar
Goudet, J. (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version2.9.3). Available from http://www2.unil.ch/popgen/softwares/fstat.htmGoogle Scholar
Guldemond, J.A., Tiggs, W.T. & De Vrijer, P.W.F. (1994) Host races of Aphis gossypii (Homoptera, Aphididae) on cucumber and chrysanthemum. Environmental Entomology 23, 1235–1240.CrossRefGoogle Scholar
Hawthorne, D.J. & Via, S. (2001) Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412, 904–907.Google Scholar
Hosoda, A., Hama, H., Suzuki, K. & Ando, Y. (1993) Insecticide resistance of the cotton aphid Aphis gossypii Glover, III. Host preference and organophosphorous susceptibility. Japanese Journal of Applied Entomology and Zoology 37, 83–90 (in Japanese with English summary).Google Scholar
Jin, L. & Chakraborty, R. (1993) Estimation of genetic distance and coefficient of gene diversity from single-probe multilocus DNA fingerprinting data. Molecular Biology and Evolution 11, 120–127.Google Scholar
Kondrashov, A.S. (1988) Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435–440.Google Scholar
Kondrashov, A.S. (1993) Classification of hypotheses on the advantages of amphixis. Journal of Heredity 84, 372–387.Google Scholar
Leclant, F. & Deguine, J.P. (1994) Cotton aphids. pp. 285–323in Matthews, G.A. & Tunstall, J.P. (Eds) Insect pests of cotton. Wallingforg, UK, CAB International.Google Scholar
Llewellyn, K.S., Loxdale, H.D., Harrington, C.P., Brookes, P., Clark, 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, 21–34.CrossRefGoogle ScholarPubMed
Loxdale, H.D. & Lushai, G. (2003) Rapid changes in clonal lineages: the death of a ‘sacredcow’. Biological Journal of the Linnean Society 79, 3–16.Google Scholar
Lushai, G. & Loxdale, H.D. (2002) The biological improbability of a clone. Genetical Research 79, 1–9.Google Scholar
Lushai, G., Markovitch, O. & Loxdale, H.D. (2002) Host-based genotype variation in insects revisited. Bulletin of Entomological Research 92, 159–164.Google Scholar
Lushai, G., Loxdale, H.D. & Allen, J.A. (2003) The dynamic clonal genome and its adaptive potential. Biological Journal of the Linnean Society 79, 193–208.CrossRefGoogle Scholar
Lynch, M. (1984) Destabilizing hybridization, general-purpose genotypes and geographic parthenogenesis. Quarterly Review of Biology 59, 257–290.Google Scholar
Maynard Smith, J. (1978) The Evolution of Sex. 242 pp. Cambridge, Cambridge University Press.Google Scholar
Miller, N.J., Birley, A.J., Overall, A.D.J. & Tatchell, G.M. (2003) population genetic structure of the lettuce root aphid, Pemphigus bursarius (L.), in relation to geographic distance, gene flow and host plant usage. Heredity 91, 217–223.Google Scholar
Owusu, E.O., Kim, C.S., Horiike, M. & Hirano, C. (1996) Comparative biological and enzymatic studies on some host-adapted populations of melon and cotton aphid, Aphis gossypii (Homoptera: Aphididae). Journal of Agricultural Science 126, 449–453.Google Scholar
Raymond, M. & Rousset, F. (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248–249.CrossRefGoogle Scholar
Rispe, C., Pierre, J.S., Simon, J.C. & Gouyon, P.H. (1998) Models of sexual and asexual coexistence in aphids based on constraints. Journal of Evolutionary Biology 11, 685–701.Google Scholar
Ruiz-Montoya, L., Núñez-Farfán, J. & Vargas, J. (2003) Host-associated genetic structure of Mexican populations of the cabbage aphid Brevicoryne brassicae L. (Homoptera: Aphididae). Heredity 91, 415–421.Google Scholar
Shufran, K.A., Burd, J.D., Anstead, J.A. & Lushai, G. (2000) Mitochondrial DNA sequence divergence among green bug (Homoptera: Aphididae) biotypes: evidence for host-adapted races. Insect Molecular Biology 9, 179–184.CrossRefGoogle Scholar
Simon, J.C., Carre, S., Boutin, M., Prunier-Leterme, N., Sabater-Munoz, B., Latorre, A. & Bournoville, R. (2003) Host-based divergence in populations of the pea aphid: insights from nuclear markers and the prevalence of facultative symbionts. Proceedings of the Royal Society of London, Series B: Biological Sciences 270, 1703–1712.Google Scholar
Stroyan, H.L.G. (1984) Aphids − Pterocommatinae and Aphidinae (Aphidini). Homoptera, Aphididae. Handbooks for the identification of British insects, Volume 2, Part 6. 232 pp. London, Royal Entomological Society of London.Google Scholar
Sunnucks, P., De Barro, P.J., Lushai, G., Maclean, N. & Hales, D.F. (1997a) Genetic structure of an aphid studied using microsatellite: cyclic parthenogenesis, differentiated lineages, and host specialization. Molecular Ecology 6, 1059–1073.Google Scholar
Sunnucks, P., Driver, F., Brown, W.V., Carver, M., Hales, D.F. & Milne, W.M. (1997b) Biological and genetic characterization of morphologically similar Therioaphis trifolii (Hemiptera: Aphididae) with different host utilization. Bulletin of Entomological Research 87, 425–436.Google Scholar
Vanlerberghe-Masutti, F. & Chavigny, P. (1998) Host-based genetic differentiation in the aphid Aphis gossypii Glover, evidenced from RAPD fingerprints. Molecular Ecology 7, 905–914.CrossRefGoogle Scholar
Vanlerberghe-Masutti, F., Chavigny, P. & Fuller, S.J. (1999) Characterisation of microsatellite loci in aphid, Aphis gossypii Glover. Molecular Ecology 8, 693–695.CrossRefGoogle Scholar
Vanoverbeke, J. & De Meester, L. (1997) Among-population genetic differentiation in the cyclical parthenogen Daphnia magna (Crustacea, Anomopoda) and its relation to geographic distance and clonal diversity. Hydrobiologia 360, 135–142.Google Scholar
Via, S. (1991) The genetic structure of host adaptation in a special patchwork − demographic variability among reciprocally transplanted pea aphid clones. Evolution 45, 827–852.Google Scholar
Via, S., Bouck, A.C. & Skillman, S. (2000) Reproductive isolation between divergent races of pea aphids on two hosts. II. Selection against migrants and hybrids in the parental environments. Evolution 54, 1626–1637.Google ScholarPubMed
Vrijenhoek, R.C. (1998) Animal clones and diversity. Are natural clones generalists or specialists? Bioscience 48, 617–629.Google Scholar
Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.Google Scholar
White, M.J.D. (1978) Modes of Speciation. 455 pp. San Francisco, W. H. Freeman.Google Scholar
Wool, D., Hales, D. & Sunnucks, P. (1995) Host-plant relationships of Aphis gossypii Glover (Hemiptera, Aphididae) in Australia. Journal of the Australian Entomological Society 34, 265–271.Google Scholar
Zamoum, T., Simon, J.C., Crochard, D., Ballanger, Y., Lapchin, L., Vanlerberghe-Masutti, F. & Guillemaud, T. (2005) Does insecticide alone account for the low genetic variability of asexually reproducing populations of the peach-potato aphid Myzus persicae? Heredity 94, 630–639.Google Scholar