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Inferring the population structure of Myzus persicae in diverse agroecosystems using microsatellite markers

  • Juan Antonio Sanchez (a1), Michelangelo La-Spina (a1), Pedro Guirao (a2) and Fernando Cánovas (a1) (a3)

Diverse agroecosystems offer phytophagous insects a wide choice of host plants. Myzus persicae is a polyphagous aphid common in moderate climates. During its life cycle it alternates between primary and secondary hosts. A spatial genetic population structure may arise due to environmental factors and reproduction modes. The aim of this work was to determine the spatial and temporal genetic population structure of M. persicae in relation to host plants and climatic conditions. For this, 923 individuals of M. persicae collected from six plant families between 2005 and 2008 in south-eastern Spain were genotyped for eight microsatellite loci. The population structure was inferred by neighbour-joining, analysis of molecular variance (AMOVA) and Bayesian analyses. Moderate polymorphism was observed for the eight loci in almost all the samples. No differences in the number of alleles were observed between primary and secondary hosts or between geographical areas. The proportion of unique genotypes found in the primary host was similar in the north (0.961 ± 0.036) and the south (0.987 ± 0.013), while in the secondary host it was higher in the north (0.801 ± 0.159) than in the south (0.318 ± 0.063). Heterozygosity excess and linkage disequilibrium suggest a high representation of obligate parthenogens in areas with warmer climate and in the secondary hosts. The FST-values pointed to no genetic differentiation of M. persicae on the different plant families. FST-values, AMOVA and Bayesian model-based cluster analyses pointed to a significant population structure that was related to primary and secondary hosts. Differences between primary and secondary hosts could be due to the overrepresentation of parthenogens on herbaceous plants.

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*Author for correspondence: Juan Antonio Sanchez Phone: +34 968 362787 Fax: +34 968 366792 E-mail:;
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Barker, J.S.F. (2005) Population structure and host-plant specialization in two Scaptodrosophila flower-breeding species. Heredity 94, 129138.
Berlocher, S.H. & Feder, J.L. (2002) Sympatric speciation in phytophagous insects: moving beyond controversy? Annual Review of Entomology 47, 773815.
Birky, C.W. (1996) Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics 144, 427437.
Blackman, R.L. (1971). Variation in the photoperiodic response within natural populations of Myzus persicae (Sulz.). Bulletin of Entomological Research 60, 533546.
Blackman, R.L. (1972) The inheritance of life-cycle differences in Myzus persicae (Sulz.) (Hem., Aphididae). Bulletin of Entomological Research 62, 281294.
Blackman, R.L. (1974) Life-cycle variation of Myzus persicae (Sulz.) (Hom., Aphididae) in different parts of the world, in relation to genotype and environment. Bulletin of Entomological Research 63, 595607.
Blackman, R.L. (1987) Morphological discrimination of a tobacco-feeding form of Myzus persicae (Sulzer) (Hemiptera: Aphididae), and a key to New World Myzus (Nectarosiphon) species. Bulletin of Entomological Research 77, 713730.
Blackman, R.L. & Eastop, V.F. (2000) Aphids on the world's crop: and identification and information guide. Chicherter, UK, John Wiley and Sons Ltd.
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, 161165.
Blackman, R.L., Malarky, G., Margaritopoulos, J.T. & Tsitsipis, J.A. (2007) Distribution of common genotypes of Myzus persicae (Hemiptera: Aphididae) in Greece, in relation to life cycle and host plant. Bulletin of Entomological Research 97, 253263.
Carroll, S.P. & Boyd, C. (1992) Host race radiation in the soapberry bug natural history with the history. Evolution 46, 10521069.
Cavalli-Sforza, L.L. & Edwards, A.W.F. (1967) Phylogenetic analysis: models and estimation procedures. American Journal of Human Genetics 19, 233257.
De Barro, P.J., Sherratt, T.N., Brookes, C.P.David, O. & Maclean, N. (1995) 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 B: Biological Sciences 262, 321327.
Del Campo, M.L., Via, S. & Caillaud, M.C. (2003) Recognition of host-specific chemical stimulants in two sympatric host races of the pea aphid Acyrthosiphon pisum. Ecological Entomology 28, 405412.
Delmotte, F., Leterme, N., Bonhomme, J., Rispe, C. & Simon, J.C. (2001) Multiple routes to asexuality in an aphid species. Proceedings of the Royal Society B: Biological Sciences 268, 22912299.
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.
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 B: Biological Sciences 353, 16771684.
Edwards, O.R. (2001) Interspecific and intraspecific variation in the performance of three pest aphid species on five grain legume hosts. Entomologia Experimentalis et Applicata 100, 2130.
Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 26112620.
Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics 1, 4750.
Feder, J.L., Berlocher, S.H. & Opp, S.B. (1998) Sympatric host-race formation and speciation in Rhagoletis (Diptera: Tephritidae): a tale of two species for Charles D. pp. 408441in Mopper, S. & Strauss, S.Y. (Eds) Genetic structure and local adaptation in natural insect populations. New York, USA, Chapman and Hall.
Fenton, B., Woodford, J.A.T. & Malloch, G. (1998) Analysis of clonal diversity of the peach-potato aphid, Myzus persicae (Sulzer), in Scotland, UK and evidence for the existence of a predominant clone. Molecular Ecology 7, 14751487.
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, 392401.
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.
Goudet, J. (2002) FSTAT, a program to estimate and test gene diversities and fixation indices (Version Available online at
Guillemaud, T., Mieuzet, L. & Simon, J.C. (2003) Spatial and temporal genetic variability in French populations of the peach-potato aphid, Myzus persicae. Heredity 91, 143152.
Hales, D. F., Wilson, A.C.C., Sloane, M.A., Christophesimon, J., Legallic, J.F. & Sunnucks, P. (2002) Lack of detectable genetic recombination on the X chromosome during the parthenogenetic production of female and male aphids. Genetical Research 79, 203209.
Hawthorne, D.J. & Via, S. (2001) Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412, 904907.
Langella, O. (1999) Populations, 1.2.32. Available online at
Malloch, G., Highet, F., Kasprowicz, L., Pickup, J., Neilson, R. & Fenton, B. (2006) Microsatellite marker analysis of peach-potato aphids (Myzus persicae, Homoptera: Aphididae) from Scottish suction traps. Bulletin of Entomological Research 96, 573582.
Margaritopoulos, J.T., Mamuris, Z. & Tsitsipis, J.A. (1998) Attempted discrimination of Myzus persicae and Myzus nicotianae (Homoptera: Aphididae) by random amplified polymorphic DNA polymerase chain reaction technique. Annals of the Entomological Society of America 91, 602607.
Margaritopoulos, J.T., Tsitsipis, J.A., Zintzaras, E. & Blackman, R.L. (2000) Host-correlated morphological variation of Myzus persicae (Hemiptera: Aphididae) populations in Greece. Bulletin of Entomological Research 90, 233244.
Margaritopoulos, J.T., Blackman, R.L., Tsitsipis, J.A. & Sannino, L. (2003) Co-existence of different host-adapted forms of the Myzus persicae group (Hemiptera: Aphididae) in southern Italy. Bulletin of Entomological Research 93, 131135.
Margaritopoulos, J.T., Malarky, G., Tsitsipis, J.A. & Blackman, R.L. (2007a) Microsatellite DNA and behavioural studies provide evidence of host-mediated speciation in Myzus persicae (Hemiptera: Aphididae). Biological Journal of the Linnean Society 91, 687702.
Margaritopoulos, J.T., Shigehara, T., Takada, H. & Blackman, R.L. (2007b) Host-related morphological variation within Myzus persicae group (Homoptera: Aphididae) from Japan. Applied Entomology and Zoology 42, 329335.
Martínez-Torres, D., Simon, J.C., Fereres, A. & Moya, A. (1996) Genetic variation in natural populations of the aphid Rhopalosiphum padi as revealed by maternally inherited markers. Molecular Ecology 5, 659670.
Martínez-Torres, D., Carrio, R., Latorre, A., Simon, J. C., Hermoso, A. & Moya, A. (1997) Assessing the nucleotide diversity of three aphid species by RAPD. Journal of Evolutionary Biology 10, 459477.
Nikolakakis, N.N., Margaritopoulos, J.T. & Tsitsipis, J.A. (2003) Performance of Myzus persicae (Hemiptera: Aphididae) clones on different host-plants and their host preference. Bulletin of Entomological Research 93, 235242.
Page, R.D.M. (1996) Treeview: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences, 12, 357358.
Pritchard, J. K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945959.
R Development Core Team. (2005) A language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria.
Rice, W. R. (1989) Analyzing tables of statistical tests. Evolution 43, 223225.
Rousset, F. (2008) GENEPOP 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8, 103106.
Sanchez, J. A., La-Spina, M., Michelena, J. M., Lacasa, A. & Hermoso de Mendoza, A. (2011) Ecology of the aphid pests of protected pepper crops and their parasitoids. Biocontrol Science and Technology 21, 171188.
Simon, J.C., Baumann, S., Sunnucks, P., Hebert, P.D.N., Pierre, J.S., Le Gallic, J.F. & Dedryver, C.A. (1999) Reproductive mode and population genetic structure of the cereal aphid Sitobion avenae studied using phenotypic and microsatellite markers. Molecular Ecology 8, 531545.
Simon, J.C., Carre, S., Boutin, M., Prunier-Leterme, N., Sabater-Muñoz, 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 B: Biological Sciences 270, 17031712.
Sloane, M. A., Sunnucks, P., Wilson, A.C.C. & Hales, D.F. (2001) Microsatellite isolation, linkage group identification and determination of recombination frequency in the peach-potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Genetical Research 77, 251260.
Sunnucks, P., England, P.R., Taylor, A.C. & Hales, D.F. (1996) Microsatellite and chromosome evolution of parthenogenetic Sitobion aphids in Australia. Genetics 144, 747756.
Sunnucks, P., Barro, P.J.d., Lushai, G., Maclean, N. & Hales, D. (1997) Genetic structure of an aphid studied using microsatellites: cyclic parthenogenesis, differentiated lineages and host specialization. Molecular Ecology 6, 10591073.
Takezaki, N. & Nei, M. (1996) Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144, 389399.
Via, S. (1999) Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 53, 14461457.
Via, S. & Hawthorne, D.J. (2002) The genetic architecture of ecological specialization: correlated gene effects on host use and habitat choice in pea aphids. American Naturalist 159, S76S88.
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, 16261637.
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.
Weber, G. (1985) Genetic-variability in host plant adaptation of the green peach aphid, Myzus persicae. Entomologia Experimentalis et Applicata 38, 4956.
Weber, G. (1986) Ecological genetics of host plant exploitation in the green peach aphid, Myzus persicae. Entomologia Experimentalis et Applicata 40, 161168.
Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistic for the analysis of population structure. Evolution 38, 13581370.
Wilson, A.C.C., Sunnucks, P. & Hales, D.F. (1999) Microevolution, low clonal diversity and genetic affinities of parthenogenetic Sitobion aphids in New Zealand. Molecular Ecology 8, 16551666.
Wilson, A.C.C., Sunnucks, P., Blackman, R.L. & Hales, D.F. (2002) Microsatellite variation in cyclically parthenogenetic populations of Myzus persicae in south-eastern Australia. Heredity 88, 258266.
Wilson, A.C.C., Massonnet, B., Simon, J.C., Prunier-Leterme, N., Dolatti, L., Llewellyn, K.S., Figueroa, C.C., Ramirez, C.C., Blackman, R.L., Estoup, A. & Sunnucks, P. (2004) Cross-species amplification of microsatellite loci in aphids: assessment and application. Molecular Ecology Notes 4, 104109.
Zitoudi, K., Margaritopoulos, J.T., Mamuris, Z. & Tsitsipis, J.A. (2001) Genetic variation in Myzus persicae populations associated with host-plant and life cycle category. Entomologia Experimentalis et Applicata 99, 303311.
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