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Longitudinal clines in the frequency distribution of ‘super-clones’ in an aphid crop pest

  • A. Gilabert (a1), C.-A. Dedryver (a1), S. Stoeckel (a1), M. Plantegenest (a2) and J.-C. Simon (a1)...


Parthenogenesis is the main mode of reproduction of aphids. Their populations are therefore composed of clones whose frequency distribution varies in space and time. Previous population genetic studies on aphids have highlighted the existence of highly abundant clones (‘super-clones’), distributed over large geographic areas and persisting over time. Whether the abundance of ‘super-clones’ results from their ecological success or from stochastic forces, such as drift and migration, is an open question. Here, we looked for the existence of clines in clonal frequency along a climatic gradient in the cereal aphid Rhopalosiphum padi (Linnaeus, 1758) and examined the possible influence of geographical distance and environmental variables in the buildup and maintenance of such clonal clines. We investigated the spatial distribution of the commonest genotypes of R. padi by sampling populations along an east–west transect in maize fields in the northern half of France in both spring and late summer. Individual aphids were genotyped at several polymorphic loci, allowing the assessment of frequency distributions of multilocus genotypes (MLGs) across the cropping season. We found several MLGs showing longitudinal clines in their frequency distribution in both spring and summer. In particular, two dominant asexual genotypes of R. padi showed inverted geographical clines, which could suggest divergent adaptations to environmental conditions. We concluded that while the distribution of some ‘super-clones’ of R. padi seems most likely driven by the action of migration and genetic drift, selection could be also involved in the establishment of longitudinal clines of others.


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Allen, D.E. & Lynch, M. (2012) The effect of variable frequency of sexual reproduction on the genetic structure of natural population of a cyclical parthenogen. Evolution 66, 919926.
Arnaud-Haond, S. & Belkhir, K. (2007) Genclone: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Molecular Ecology Notes 7, 1517.
Arnaud-Haond, S., Duarte, C.M., Diaz-Almela, E., Marba, N., Sintes, T. & Serrao, E.A. (2012) Implications of extreme life span in clonal organisms: millenary clones in meadows of the threatened seagrass Posidonia oceanica . PLoS ONE 7, e30454.
Belkhir, K., Borsa, P., Chiki, L., Raufaste, N. & Bonhomme, F. (2004) GENETIX, logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome, Populations, Interactions. CNRS UMR 5171, Université de Montpellier II, Montpellier, France.
Campitelli, B.E. & Stinchcombe, J.R. (2013) Testing potential selective agents acting on leaf shape in Ipomoea hederacea: predictions based on an adaptive leaf shape cline. Ecology and Evolution 3, 24092423.
Castañeda, L.E., Figueroa, C.C., Fuentes-Contreras, E., Niemeyer, H.M. & Nespolo, R.F. (2010) Physiological approach to explain the ecological success of ‘superclones’ in aphids: Interplay between detoxification enzymes, metabolism and fitness. Journal of Insect Physiology 56, 10581064.
Dedryver, C.A. (1983) Evolution des populations de Rhopalosiphum padi L. sur son hôte primaire, Prunus padus L., dans deux stations du nord et de l'ouest de la France. Agronomie 3, 18.
Delmotte, F., Leterme, N., Gauthier, J.P., Rispe, C. & Simon, J.C. (2002) Genetic architecture of sexual and asexual populations of the aphid Rhopalosiphum padi based on allozyme and microsatellite markers. Molecular Ecology 11, 711723.
Fenton, B., Kasprowicz, L., Malloch, G. & Pickup, J. (2010) Reproductive performance of asexual clones of the peach-potato aphid (Myzus persicae, Homoptera: Aphididae), colonising Scotland in relation to host plant and field ecology. Bulletin of Entomological Research 100, 451460.
Fievet, V., Dedryver, C.-A., Plantegenest, M., Simon, J.-C. & Outreman, Y. (2007) Aphid colony turn-over influences the spatial distribution of the grain aphid Sitobion avenae over the wheat growing season. Agricultural and Forest Entomology 9, 125134.
Gilabert, A., Simon, J.C., Mieuzet, L., Halkett, F., Stoeckel, S., Plantegenest, M. & Dedryver, C.A. (2009) Climate and agricultural context shape reproductive mode variation in an aphid crop pest. Molecular Ecology 18, 30503061.
Gilabert, A., Simon, J.-C., Dedryver, C.-A. & Plantegenest, M. (2014) Do ecological niches differ between sexual and asexual lineages of an aphid species? Evolutionary Ecology 28, 10951104.
Halkett, F., Plantegenest, M., Prunier-Leterme, N., Mieuzet, L., Delmotte, F. & Simon, J.C. (2005) Admixed sexual and facultatively asexual aphid lineages at mating sites. Molecular Ecology 14, 325336.
Halkett, F., Plantegenest, M., Bonhomme, J. & Simon, J.C. (2008) Gene flow between sexual and facultatively asexual lineages of an aphid species and the maintenance of reproductive mode variation. Molecular Ecology 17, 29983007.
Hoffmann, A.A. & Weeks, A.R. (2007) Climatic selection of genes and traits after a 100 year-old invasion: a critical look at the temperate-tropical clines in Drosophila melanogaster from eastern Australia. Genetica 129, 133147.
Hullé, M., Coquio, S. & Laperche, V. (1994) Patterns in flight phenology of a migrant cereal aphid species. Journal of Applied Ecology 31, 4958.
Jankowski, T. & Straile, D. (2004) Allochronic differentiation among Daphnia species, hybrids and backcrosses: the importance of sexual reproduction for population dynamics and genetic architecture. Journal of Evolutionary Biology 17, 312321.
Karley, A.J., Parker, W.E., Pitchford, J.W. & Douglas, A.E. (2004) The mid-season crash in aphid populations: why and how does it occur? Ecological Entomology 29, 383388.
Le Ralec, A., Anselme, C., Outreman, Y., Poirié, M., van Baaren, J., Le Lann, C. & van Alphen, J.J.M. (2010) Evolutionary ecology of the interactions between aphids and their parasitoids. Comptes Rendus Biologies 333, 554565.
Loxdale, H.D. & Lushai, G. (2007) Population genetic issues: the unfolding story using molecular markers. pp. 3167 in Van Emden, H.F. and Harrington, R. (Eds) Aphids as Crop Pests. CABI, Wallingford, Oxford, UK.
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 Review 68, 291311.
Lukasik, P., Hancock, E.L., Ferrari, J. & Godfray, H.C.J. (2011) Grain aphid clones vary in frost resistance, but this trait is not influenced by facultative endosymbionts. Ecological Entomology 36, 790793.
Mashanova, A., Gange, A.C. & Jansen, V.A.A. (2008) Density-dependent dispersal may explain the mid-season crash in some aphid populations. Population Ecology 50, 285292.
Massonnet, B., Simon, J.-C. & Weisser, W.W. (2002) Metapopulation structure of the specialized herbivore Macrosiphoniella tanacetaria (Homoptera, Aphididae). Molecular Ecology 11, 25112521.
Niklasson, M., Tomiuk, J. & Parker, E.D. (2004) Maintenance of clonal diversity in Dipsa bifurcata (Fallen, 1810) (Diptera: Lonchopteridae). I. Fluctuating seasonal selection moulds long-term coexistence. Heredity 93, 6271.
Paaby, A.B., Blacket, M.J., Hoffmann, A.A. & Schmidt, P.S. (2010) Identification of a candidate adaptive polymorphism for Drosophila life history by parallel independent clines on two continents. Molecular Ecology 19, 760774.
Paulson, M.D., Houston, A.I., McNamara, J.M. & Payne, R.J.H. (2009) Seasonal dispersal of pests: one surge or two? Journal of Evolutionary Biology 22, 11931202.
Piffaretti, J., Clamens, A.L., Vanlerberghe-masutti, F., Gupta, R.K., Call, E., Halbert, S. & Jousselin, E. (2013) Regular or covert sex defines two lineages and worldwide superclones within the leaf-curl plum aphid (Brachycaudus helichrysi, Kaltenbach). Molecular Ecology 22, 39163932.
Pinkhaus, O., Schwerin, S., Pirow, R., Zeis, B., Buchen, I., Gigengack, U., Koch, M., Horn, W. & Paul, R.J. (2007) Temporal environmental change, clonal physiology and the genetic structure of a Daphnia assemblage (D. galeata-hyalina hybrid species complex). Freshwater Biology 52, 15371554.
Polechová, J. & Barton, N. (2011) Genetic drift widens the expected cline but narrows the expected cline width. Genetics 189, 227235.
Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945959.
R Development Core Team (2012) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Rieux, A., Lenormand, T., Carlier, J., de Lapeyre de Bellaire, L. & Ravigné, V. (2013) Using neutral cline decay to estimate contemporary dispersal: a generic tool and its application to a major crop pathogen. Ecology Letters 16, 721730.
Rispe, C., Simon, J.-C. & Pierre, J.-S. (1996) Fitness comparison between clones differing in their ability to produce sexuals in the aphid Rhopalosiphum padi . Entomologia Experimentalis et Applicata 80, 469474.
Samis, K.E., Murren, C.J., Bossdorf, O., Donohue, K., Fenster, C.B., Malmberg, R.L., Purugganan, M.D. & Stinchcombe, J.R. (2012) Longitudinal trends in climate drive flowering time clines in North American Arabidopsis thaliana . Ecology and Evolution 2, 11621180.
Simon, J.C., Dedryver, C.A. & Pierre, J.S. (1991) Identifying bird cherry-oat aphid Rhopalosiphum padi emigrants, alate exules and gynoparae: application of multivariate methods to morphometric and anatomical features. Entomologia Experimentalis et Applicata 59, 267277.
Simon, J.-C., Rispe, C. & Sunnucks, P. (2002) Ecology and evolution of sex in aphids. Trends in Ecology & Evolution 17, 3439.
Vasemagi, A. (2006) The adaptive hypothesis of clinal variation revisited: single-locus clines as a result of spatially restricted gene flow. Genetics 173, 24112414.
Vialatte, A., Dedryver, C.A., Camus, D. & Plantegenest, M. (2005) Vers un OAD de traitement des pucerons des épis au printemps. Compte-rendus de la VIIeme conférence internationale sur les ravageurs en agriculture. (CD-Rom Acariens-CIRA: 2-905550-02-3). Montpellier, France.
Vorburger, C. (2004) Cold tolerance in obligate and cyclical parthenogens of the peach-potato aphid, Myzus persicae . Ecological Entomology 29, 498505.
Vorburger, C. (2006) Temporal dynamics of genotypic diversity reveal strong clonal selection in the aphid Myzus persicae . Journal of Evolutionary Biology 19, 97107.
Vorburger, C., Lancaster, M. & Sunnucks, P. (2003a) Environmentally related patterns of reproductive modes in the aphid Myzus persicae and the predominance of two ‘superclones’ in Victoria, Australia. Molecular Ecology 12, 34933504.
Vorburger, C., Sunnucks, P. & Ward, S.A. (2003b) Explaining the coexistence of asexuals with their sexual progenitors: no evidence for general-purpose genotypes in obligate parthenogens of the peach-potato aphid, Myzus persicae . Ecology Letters 6, 10911098.
Vrijenhoek, R.C. (1979) Factors affecting clonal diversity and coexistence. American Zoologist 19, 787797.
Waits, L.P., Luikart, G. & Taberlet, P. (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Molecular Ecology 10, 249256.
Weeks, A.R. & Hoffmann, A.A. (1998) Intense selection of mite clones in a heterogeneous environment. Evolution 52, 13251333.


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Longitudinal clines in the frequency distribution of ‘super-clones’ in an aphid crop pest

  • A. Gilabert (a1), C.-A. Dedryver (a1), S. Stoeckel (a1), M. Plantegenest (a2) and J.-C. Simon (a1)...


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