Hostname: page-component-7c8c6479df-24hb2 Total loading time: 0 Render date: 2024-03-28T03:38:50.677Z Has data issue: false hasContentIssue false

Insecticide use and competition shape the genetic diversity of the aphid Aphis gossypii in a cotton-growing landscape

Published online by Cambridge University Press:  15 February 2011

T. Brévault*
Affiliation:
CIRAD, UPR 102, F-34398 Montpellier, France Department of Entomology, University of Arizona, Tucson, AZ 85721, USA
J. Carletto
Affiliation:
INRA, UMR IBSV, F-06903 Sophia-Antipolis, France AFSSA, F-06902 Sophia-Antipolis, France
J. Tribot
Affiliation:
CIRAD, UPR 102, F-34398 Montpellier, France IRAD, PRASAC-ARDESAC, Cotton Program, Garoua, Cameroon
F. Vanlerberghe-Masutti
Affiliation:
INRA, UMR IBSV, F-06903 Sophia-Antipolis, France INRA, UMR CBGP, F-34988 Montferrier-sur-Lez, France
*
*Author for correspondence Fax: 33 (0)4 67 61 56 66 E-mail: brevault@cirad.fr

Abstract

Field populations of the cotton aphid, Aphis gossypii Glover, are structured into geographically widespread host races. In the cotton-producing regions of West and Central Africa (WCA), two genotypes have been repeatedly detected within the cotton host race, one of which (Burk1) is prevalent (>90%) and resistant to several insecticides, as opposed to the second one (Ivo). Here, we conducted whole plant and field cage experiments to test hypotheses for such low genetic diversity, including selection from insecticide treatments, interclonal competition and adaptation to host plant, or climatic conditions. To assess the genetic diversity of immigrant aphids, alatae were trapped and collected on cotton and relay host plants (okra and roselle) in the early cropping season. Individuals were genotyped at eight specific microsatellite loci and characterized by a multilocus genotype (MLG). When independently transferred from cotton (Gossypium hirustum L.) leaf discs to whole plants (G. hirsutum and G. arboreum, roselle and okra), Ivo and Burk1 performed equally well. When concurrently transferred from cotton leaf discs to the same plant species, Ivo performed better than Burk1, indicating that competition favoured Ivo. This was also the case on G. hirsutum growing outdoors. Conversely, Burk1 prevailed when cotton plants were sprayed with insecticides. In experiments where aphids were allowed to move to neighbouring plants, Burk1 was better represented than Ivo on low-populated plants, suggesting that dispersal may be a way to avoid competition on crowded plants. Most cotton aphids collected on cotton or relay host plants in the early cropping season were Burk1 (>90%), indicating high dispersal ability and, probably reflecting high frequency on host plants from which they dispersed. In the agricultural landscape of WCA, the use of broad-range insecticides on both cotton and relay host plants has led to the prevalence of one genotype of A. gossypii resistant to different classes of insecticides. Deployment of widespread and integrated pest management strategies are needed to restore cotton aphid control.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Achaleke, J., Vaissayre, M. & Brévault, T. (2009) Evaluating pyrethroid alternatives for the management of cotton bollworms and resistance in Cameroon. Experimental Agriculture 45, 3546.CrossRefGoogle Scholar
Beasley, J.O. (1940) The origin of American tetraploid Gossypium species. American Naturalist 74, 285286.CrossRefGoogle Scholar
Blackman, R.L. & Eastop, V.F. (1984) Aphids on the World's Crops: An Identification and Information Guide. Chichester, UK, John Wiley & Sons.Google Scholar
Brévault, T., Carletto, J., Linderme, D. & Vanlerberghe-Masutti, F. (2008) Genetic diversity of the cotton aphid Aphis gossypii in the unstable environment of a cotton growing area. Agricultural and Forest Entomology 10, 215223.CrossRefGoogle Scholar
Carletto, J., Lombaert, E., Chavigny, P., Brévault, T., Lapchin, L. & Vanlerberghe-Masutti, F. (2009) Ecological specialization of the aphid Aphis gossypii Glover on cultivated host plants. Molecular Ecology 18, 21982212.CrossRefGoogle ScholarPubMed
Carletto, J., Martin, T., Vanlerberghe-Masutti, F. & Brévault, T. (2010) Insecticide resistance traits differ among and within host races in Aphis gossypii. Pest Management Science 66, 301307.CrossRefGoogle ScholarPubMed
Charaabi, K., Carletto, J., Chavigny, P., Marrakchi, M., Makni, M. & Vanlerberghe-Masutti, F. (2008) Genotypic diversity of the cotton-melon aphid Aphis gossypii (Glover) in Tunisia is structured by host plants. Bulletin of Entomological Research 98, 333341.CrossRefGoogle ScholarPubMed
De Barro, P.J. (1992) The role of temperature, photoperiod, crowding and plant-quality on the production of alate viviparous females of the bird cherry-oat aphid, Rhopalosiphum padi. Entomologia Experimentalis et Applicata 65, 205214.CrossRefGoogle Scholar
Deguine, J.P., Martin, J., Merlier, H. & Leclant, F. (1997) Inventaire des plantes-hôtes d'Aphis gossypii Glover (Hemiptera, Aphididae) en Afrique. 18 pp. Montpellier, Documents de travail du CIRAD-CA.Google Scholar
Ebert, T.A. & Cartwright, B. (1997) Biology and ecology of Aphis gossypii Glover (Homoptera: Aphididae). Southwestern Entomologist 22, 116153.Google Scholar
Fenton, B., Malloch, G., Woodford, J.A.T., Foster, S.P., Anstead, J., Denholm, I., King, L. & Pickup, J. (2005) The attack of the clones: tracking the movement of insecticide-resistant peach-potato aphids Myzus persicae (Hemiptera: Aphididae). Bulletin of Entomological Research 95, 483494.CrossRefGoogle Scholar
Ferrari, J., Muller, C.B., Kraaijeveld, A.R. & Godfray, H.C.J. (2001) Clonal variation and covariation in aphid resistance to parasitoids and a pathogen. Evolution 55, 18051814.Google Scholar
Foster, S.P., Harrington, R., Dewar, A.M., Denholm, I. & Devonshire, A.L. (2002) Temporal and spatial dynamics of insecticide resistance in Myzus persicae (Hemiptera: Aphididae). Pest Management Science 58, 895907.CrossRefGoogle ScholarPubMed
Foster, S.P., Denholm, I., Thompson, R., Poppy, G.M. & Powell, W. (2005) Reduced response of insecticide-resistant aphids and attraction of parasitoids to aphid alarm pheromone; a potential fitness trade-off. Bulletin of Entomological Research 95, 3746.CrossRefGoogle ScholarPubMed
Foster, S.P., Tomiczek, M., Thompson, R., Denholm, I., Poppy, G., Kraaijeveld, A.R. & Powell, W. (2007) Behavioural side-effects of insecticide resistance in aphids increase their vulnerability to parasitoid attack. Animal Behaviour 74, 621632.CrossRefGoogle Scholar
Friedenberg, N.A. (2003) Determinism in a transient assemblage: the roles of dispersal and local competition. American Naturalist 162, 586596.CrossRefGoogle Scholar
Fuller, S.J., Chavigny, P., Lapchin, L. & Vanlerberghe-Masutti, F. (1999) Variation in clonal diversity in glasshouse infestations of the aphid, Aphis gossypii Glover in southern France. Molecular Ecology 8, 18671877.CrossRefGoogle ScholarPubMed
Griffiths, E. & Wratten, S.D. (1979) Intra- and inter-specific differences in cereal aphid low-temperature tolerance. Entomologia Experimentalis et Applicata 26, 161167.CrossRefGoogle Scholar
Henter, H.J. & Via, S. (1995) The potential for coevolution in a host-parasitoid system. 1. Genetic variation within an aphid population in susceptibility to a parasitic wasp. Evolution 49, 427438.Google Scholar
Inaizumi, M. (1980) Studies on the life-cycle and polymorphism of Aphis gossypii Glover (Homoptera, Aphididae). Special Bulletin of the College of Agriculture, Utsunomiya University 37, 1132.Google Scholar
Kasprowicz, L., Malloch, G., Pickup, J. & Fenton, B. (2008a) Spatial and temporal dynamics of Myzus persicae clones in fields and suction traps. Agricultural and Forest Entomology 10, 91100.CrossRefGoogle Scholar
Kasprowicz, L., Malloch, G., Foster, S., Pickup, J., Zhan, J. & Fenton, B. (2008b) Clonal turnover of MACE-carrying peach-potato aphids (Myzus persicae (Sulzer), Homoptera: Aphididae) colonizing Scotland. Bulletin of Entomological Research 98, 115124.CrossRefGoogle ScholarPubMed
Liu, X.D., Zhai, B.P., Zhang, X.X. & Zong, J.M. (2005) Impact of transgenic cotton plants on a non-target pest, Aphis gossypii Glover. Ecological Entomology 30, 307315.CrossRefGoogle Scholar
Nibouche, S., Brévault, T., Klassou, C., Dessauw, D. & Hau, B. (2008) Assessment of the resistance of cotton germplasm (Gossypium spp.) to aphids (Homoptera, Aphididae) and leafhoppers (Homoptera: Cicadellidae, Typhlocybinae): methodology and genetic variability. Plant Breeding 127, 376382.CrossRefGoogle Scholar
Rochat, J., Vanlerberghe-Masutti, F., Chavigny, P., Boll, R. & Lapchin, L. (1999) Inter-strain competition and dispersal in aphids: evidence from a greenhouse study. Ecological Entomology 24, 450464.CrossRefGoogle Scholar
Showalter, A.M., Heuberger, S., Tabashnik, B.E. & Carrière, Y. (2009) A primer for using transgenic insecticidal cotton in developing countries. Journal of Insect Science 9, 139.CrossRefGoogle ScholarPubMed
SODECOTON (2007) Rapport d'activités de la campagne agricole 2006. 106 pp. Garoua, Direction de la production agricole.Google Scholar
Stroyan, H.L.G. (1984) Aphids – Pterocommatinae and Aphidinae (Aphidini). Homoptera, Aphididae. Handbooks for the identification of British Insects (vol. 2–6). London, UK, Royal Entomological Society of London.Google Scholar
Tilman, D. (1994) Competition and biodiversity in spatially structured habitats. Ecology 75, 216.CrossRefGoogle Scholar
van Toor, R.F., Foster, S.P., Anstead, J.A., Mitchinson, S., Fentonc, B. & Kasprowicz, L. (2008) Insecticide resistance and genetic composition of Myzus persicae (Hemiptera: Aphididae) on field potatoes in New Zealand. Crop Protection 27, 236247.CrossRefGoogle Scholar
Vanlerberghe-Masutti, F. & Chavigny, P. (1998) Host-based genetic differentiation in the aphid Aphis gossypii Glover, evidenced from RAPD fingerprints. Molecular Ecology 7, 905914.CrossRefGoogle Scholar
von Burg, S., Ferrari, J., Muller, C.B. & Vorburger, C. (2008) Genetic variation and covariation of susceptibility to parasitoids in the aphid Myzus persicae: no evidence for trade-offs. Proceedings of the Royal Society Series B: Biological Sciences 275, 10891094.Google ScholarPubMed
Vorburger, C. (2004) Cold tolerance in obligate and cyclical parthenogens of the peach-potato aphid, Myzus persicae. Ecological Entomology 29, 498505.CrossRefGoogle Scholar
Vorburger, C. (2006) Temporal dynamics of genotypic diversity reveal strong clonal selection in the aphid Myzus persicae. Journal of Evolutionary Biology 19, 97107.CrossRefGoogle ScholarPubMed
Wendel, J.F. & Cronn, R.C. (2003) Polyploidy and the evolutionary history of cotton. Advances in Agronomy 78, 139186.CrossRefGoogle Scholar
Wright, S. (1969) Evolution and the Genetics of Populations. Chicago, IL, USA, University of Chicago Press.Google Scholar
Wu, K.M. & Guo, Y.Y. (2003) Influences of Bacillus thuringiensis Berliner cotton planting on population dynamics of the cotton aphid, Aphis gossypii Glover, in northern China. Environmental Entomology 32, 312318.CrossRefGoogle Scholar
Zamoum, T., Simon, J.C., Crochard, D., Ballanger, Y., Lapchin, L., Vanlerberghe-Masutti, F. & Guillemaud, T. (2005) Does insecticide resistance alone account for the low genetic variability of asexually reproducing populations of the peach-potato aphid Myzus persicae? Heredity 94, 630639.CrossRefGoogle ScholarPubMed