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Evidence for a quiet revolution: seasonal variation in colonies of the specialist tansy aphid, Macrosiphoniella tanacetaria (Kaltenbach) (Hemiptera: Aphididae) studied using microsatellite markers

Published online by Cambridge University Press:  10 November 2010

H.D. Loxdale ,
B. Massonnet ,
G. Schöfl  and
W.W. Weisser
H.D. Loxdale*
Affiliation:
Institute of Ecology, Friedrich-Schiller-University, Dornburger Str. 159, D-07743 Jena, Germany Department of Entomology, Max Planck Institute for Chemical Ecology, Hans-Knöll Strasse 8, D-07745 Jena, Germany
B. Massonnet
Affiliation:
Institute of Ecology, Friedrich-Schiller-University, Dornburger Str. 159, D-07743 Jena, Germany
G. Schöfl
Affiliation:
Department of Entomology, Max Planck Institute for Chemical Ecology, Hans-Knöll Strasse 8, D-07745 Jena, Germany Department of Cell and Molecular Biology, Leibniz Institute for Natural Product Research and Infection Biology (Hans Knöll Institute), Beutenbergstrasse 11a, D-07745 Jena, Germany
W.W. Weisser
Affiliation:
Institute of Ecology, Friedrich-Schiller-University, Dornburger Str. 159, D-07743 Jena, Germany
*
*Authors for correspondence Fax: 00 49 3641 949402 E-mail: Hugh.Loxdale@uni-jena.de
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Abstract

In cyclical parthenogens, clonal diversity is expected to decrease due to selection and drift during the asexual phase per number of asexual generations. The decrease in diversity may be counteracted by immigration of new genotypes. We analysed temporal variation in clonal diversity in colonies of the monophagous tansy aphid, Macrosiphoniella tanacetaria (Kaltenbach), sampled four times over the course of a growing season. In a related field study, we recorded aphid colony sizes and the occurrence of winged dispersers throughout the season. The number of colonies increased from April, when asexual stem mothers hatched from the sexually produced eggs, to the end of June. The proportion of colonies with winged individuals also increased over this period. After a severe reduction in colony sizes in late summer, a second expansion phase occurred in October when sexuals were produced. At the season's end, the only winged forms were males. A linked genetic study showed that the number of microsatellite multilocus genotypes and genetic variability assessed at three polymorphic loci per colony decreased from June to October. Overall, the relatedness of wingless to winged individuals within colonies was lower than average relatedness among wingless individuals, suggesting that winged forms mainly originated in different colonies. The results demonstrate that patterns of genetic diversity within colonies can be explained by the antagonistic forces of clonal selection, migration and genetic drift (largely due to midsummer population bottlenecks). We further suggest that the males emigrate over comparatively longer distances than winged asexual females.

Keywords

aphidspecialisttansymetapopulationgenetic diversitymicrosatellitesrelatednessdispersalclonal selection
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 101 , Issue 2 , April 2011 , pp. 221 - 239
Copyright
Copyright © Cambridge University Press 2010

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References

Addicott, J.F. (1978) The population dynamics of aphids on fireweed: a comparison of local populations and metapopulations. Canadian Journal of Zoology 56, 2554–2564.Google Scholar
Ankersmit, G.W., Bell, C., Dijkman, H., Mace, N., Rietstra, S., Schröder, J. & de Visser, C. (1986) Incidence of parasitism by Aphidius rhopalosiphi in colour forms of the aphid Sitobion avenae. Entomologia Experimentalis et Applicata 40, 223–229.CrossRefGoogle Scholar
Bale, J.S., Ponder, K.L. & Pritchard, J. (2007) Coping with stress. pp. 287–309 in van Emden, H.F. & Harrington, R. (Eds) Aphids as Crop Pests. Wallingford, UK, CABI.CrossRefGoogle Scholar
Blackman, R.L. (1980) Chromosomes and parthenogenesis in aphids. pp. 133–148 in Blackman, R.L., Hewitt, G.M. & Ashburner, M. (Eds) Insect Cytogenetics (Proceedings of the Royal Entomological Society Symposium No. 10). Oxford, UK, Blackwell.Google Scholar
Blackman, R.L. & Eastop, V.F. (2000) Aphids on the World's Crops: an Identification and Information Guide. 2nd edn. Chichester, UK, Wiley.Google Scholar
Braendle, C. & Weisser, W.W. (2001) Variation in escape behaviour of red and green clones of the pea aphid. Journal of Insect Behaviour 14, 497–509.Google Scholar
Coyne, J.A. & Orr, H.A. (2004) Speciation. Sunderland, MA, Sinauer Associates Inc.Google Scholar
De Barro, P.J., Sherratt, T.N., Carvalho, G.R., Nicol, D., Iyengar, A. & Maclean, N. (1994) An analysis of secondary spread by putative clones of Sitobion avenae within a Hampshire wheat field using the multilocus (GATA)4 probe. Insect Molecular Biology 3, 253–260.Google Scholar
De Barro, P.J., Sherratt, T.N., Carvalho, G.R., Nicol, D., Iyengar, A. & Maclean, N. (1995a) 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
De Barro, P.J., Sherratt, T.N., Brookes, C.P., David, O. & Maclean, N. (1995b) Spatial and temporal variation in British field populations of the grain aphid Sitobion avenae (F.) (Hemiptera: Aphididae) studied using RAPD-PCR. Proceedings of the Royal Society, London, Series B 262, 321–327.Google ScholarPubMed
De Barro, P.J., Sherratt, T.N., David, O. & Maclean, N. (1995c) An investigation of the differential performance of clones of the aphid S. avenae on two hosts. Oecologia 104, 379–385.CrossRefGoogle Scholar
Dixon, A.F.G. (1998) Aphid Ecology. 2nd edn. London, UK, Chapman & Hall.Google Scholar
Excoffier, L., Smouse, P.E. & Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes – Application to human mitochondrial-DNA restriction data. Genetics 131, 479–491.CrossRefGoogle ScholarPubMed
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, 483–494.Google Scholar
Fenton, B., Margaritopoulos, J.T., Malloch, G. & Foster, S.P. (2010) Micro-evolutionary change in relation to insecticide resistance in the Peach-potato aphid, Myzus persicae. Ecological Entomology 35 (Suppl. 1), 131–146.CrossRefGoogle 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 (Sulzer). Pest Management Science 58, 895–907.Google Scholar
Fuller, S.J., Chavigny, P., Lapchin, L. & Vanlerberghe-Massuti, F. (1999) Variation in a clonal diversity in glasshouse infections of the Aphis gossypii Glover in Southern France. Molecular Ecology 8, 1867–1877.CrossRefGoogle Scholar
Haack, L., Simon, J.-C., Gauthier, J.P., Plantegenest, M. & Dedryver, C.A. (2000) Predominance of generalist clones in a cyclically parthenogenetic organism evidenced by combined demographic and genetic analyses. Molecular Ecology 9, 2055–2066.Google Scholar
Harrington, R. & Taylor, L.R. (1990) Migration for survival – fine-scale population redistribution in an aphid, Myzus persicae. Journal of Animal Ecology 59, 1177–1193.Google Scholar
Heie, O.E. (1980–95) The Aphidoidea of Fennoscandia and Denmark, Parts I–VI. Fauna Entomologica Scandinavica. Denmark, Klampenborg.Google Scholar
Henter, H.J. & Via, S. (1995) The potential for co-evolution in a host-parasitoid system. I. Genetic variation within an aphid population in susceptibility to a parasitoid wasp. Evolution 49, 427–438.Google Scholar
Hodgson, C. (1991) Dispersal of wingless aphids (Homoptera: Aphididae) from their host plant and its significance. Bulletin of Entomological Research 81, 417–427.CrossRefGoogle Scholar
Jin, L. & Chakraborty, R. (1994) Estimation of genetic distance and coefficient of gene diversity from single probe multilocus DNA fingerprint data. Molecular Biology and Evolution 11, 120–127.Google Scholar
Kasprowicz, L., Malloch, G., Pickup, J. & Fenton, B. (2008) Spatial and temporal dynamics of Myzus persicae clones in fields and suction traps. Agricicultural and Forest Entomology 10, 91–100.CrossRefGoogle Scholar
Langella, O. (1999) POPULATIONS, v. 1.2.30. Available online at http://bioinformatics.org/project/?group_id=84.Google Scholar
Llewellyn, K.S., Loxdale, H.D., Harrington, R., Clark, S.J. & Sunnucks, P. (2004) Evidence for gene flow and local clonal selection in field populations of the grain aphid (Sitobion avenae) in Britain revealed using microsatellites. Heredity 93, 143–153.Google Scholar
Lombaert, E., Boll, R. & Lapchin, L. (2006) Dispersal strategies of phytophagous insects at a local scale: adaptive potential of aphids in an agricultural environment. BMC Evolutionary Biology 6, Art. no. 75. Available online at http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1622755.Google Scholar
Losey, J.E. & Denno, R.F. (1998) Interspecific variation in the escape responses of aphids: effect on risk of predation from foliar-foraging and ground-foraging predators. Oecologia 115, 245–252.CrossRefGoogle ScholarPubMed
Losey, J.E., Ives, I.R., Harmon, J., Ballantyne, F. & Brown, C. (1997) A polymorphism maintained by opposite patterns of parasitism and predation. Nature 388, 269–272.Google Scholar
Loxdale, H.D. (2008) The nature and reality of the aphid clone – genetic variation, adaptation and evolution. Agricultural and Forest Entomology 10, 81–90.CrossRefGoogle Scholar
Loxdale, H.D. & Brookes, C.P. (1990) Genetic stability within and restricted migration (gene flow) between local populations of the blackberry-grain aphid Sitobion fragariae in south-east England. Journal of Animal Ecology 59, 495–512.Google Scholar
Loxdale, H.D. & Lushai, G. (2003) Rapid changes in clonal lines: the death of a ‘sacred cow’. Biological Journal of the Linnean Society 79, 3–16.CrossRefGoogle Scholar
Loxdale, H.D. & Lushai, G. (2007) Population genetic issues: the unfolding story revealed using molecular markers. pp. 31–67 in van Emden, H.F. & Harrington, R. (Eds) Aphids as Crop Pests. Wallingford, UK, CABI.Google Scholar
Loxdale, H.D., Kigathi, R. & Weisser, W.W. (2009). Paucity of microsatellite genotypes (MLGs=‘clones’) in tansy aphids. (Proceedings of the 8th International Symposium on Aphids, Catania, Sicily, Italy, June 8–12, 2009) Redia (special issue) 92, 51–56.Google Scholar
Loxdale, H.D., Massonnet, B. & Weisser, W.W. (2010) Why are there so few aphid clones? Bulletin of Entomological Research 100, 613–622.Google Scholar
Lushai, G., De Barro, P.J., David, O., Sherratt, T.N. & Maclean, N. (1998) Genetic variation within parthenogenetic lineages. Insect Molecular Ecology 7, 337–344.CrossRefGoogle 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
Massonnet, B. (2002) Metapopulation structure and population genetics of monophagous aphids on tansy (Tanacetum vulgareL.). PhD thesis, University of Basel, Basel, Switzerland.Google Scholar
Massonnet, B. & Weisser, W.W. (2004) Patterns of genetic differentiation between populations of the specialised herbivore Macrosiphoniella tanacetaria (Homoptera: Aphididae). Heredity 93, 577–584.CrossRefGoogle ScholarPubMed
Massonnet, B., Leterme, N., Simon, J.-C. & Weisser, W.W. (2001) Characterization of microsatellite loci in the aphid species Macrosiphoniella tanacetaria (Homoptera, Aphididae). Molecular Ecology Notes 1, 14–15.CrossRefGoogle Scholar
Massonnet, B., Simon, J.-C. & Weisser, W.W. (2002) Metapopulation structure of the specialized aphid Macrosiphoniella tanacetaria (Homoptera, Aphididae). Molecular Ecology 11, 2511–2521.Google Scholar
Massonnet, B., Leterme, N., Simon, J.-C. & Weisser, W.W. (2004) Microsatellite analysis of genetic variation within and between three populations of the aphid Macrosiphoniella tanacetaria in the Alsace region, France. pp. 253–259 in Simon, J.-C., Dedryver, C.-A., Rispe, C. & Hullé, M. (Eds) Aphids in a New Millennium. Versailles, France, INRA Edition.Google Scholar
Nyabuga, F.N., Loxdale, H.D., Heckel, D.G. & Weisser, W.W. (2010) Spatial population dynamics of a specialist aphid parasitoid, Lysiphlebus hirticornis Mackauer (Hymenoptera: Braconidae: Aphidiinae): evidence for philopatry and restricted dispersal. Heredity 104, 1–10. Available online at http://www.nature.com/hdy/journal/vaop/ncurrent/full/hdy2009190a.html.Google Scholar
Pickett, J.A. & Glinwood, R.T. (2007) Chemical ecology. pp. 235–260 in van Emden, H.F. & Harrington, R. (Eds) Aphids as Crop Pests. Wallingford, UK, CABI.Google Scholar
Pinheiro, J.C. & Bates, D.M. (2000) Mixed-Effects Models in S and S-PLUS. New York, USA, Springer-Verlag.Google Scholar
R Development Core Team (2009) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. Available online at http://www.r-project.org/.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.Google Scholar
Rhomberg, L.R., Joseph, S. & Singh, R.S. (1985) Seasonal variation and clonal selection in cyclically parthenogenetic Rose aphids (Macrosiphum rosae). Canadian Journal of Genetics and Cytology 27, 224–232.CrossRefGoogle Scholar
Saccheri, I., Kuussaari, M., Kankare, M., Vikman, P., Fortelius, W. & Hanski, I. (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392, 491–494.Google Scholar
Simon, J.-C., Dedryver, C.-A., Pierre, J.S., Tanguy, S. & Wegorek, P. (1991) The influence of clone and morph on the parameters of intrinsic rate of increase in the cereal aphids Sitobion avenae and Rhopalosiphum padi. Entomologia Experimentalis et Applicata 58, 211–220.Google Scholar
Simon, J.-C., Rispe, C. & Sunnucks, P. (2002) Ecology and evolution of sex in aphids. Trends in Ecology and Evolution 17, 34–39.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
Sunnucks, P., De Barro, P.J., Lushai, G., MacLean, N. & Hales, D.F. (1997) Genetic structure of an aphid studied using microsatellites: cyclic parthenogenesis, differentiated lineages and host specialization. Molecular Ecology 6, 1059–1073.Google Scholar
Sunnucks, P., Chisholm, D., Turak, E. & Hales, D.F. (1998) Evolution of an ecological trait in parthenogenetic Sitobion aphids. Heredity 81, 638–647.Google Scholar
Tatchell, G.M., Plumb, R.T. & Carter, N. (1988) Migration of alate morphs of the bird cherry aphid (Rhopalosiphum padi) and implications for the epidemiology of barley yellow dwarf virus. Annals of Applied Biology 112, 1–11.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, V. (1991) The genetic structure of host plant adaptation in a spatial patchwork: demographic variability among reciprocally transplanted pea aphid clones. Evolution 45, 827–852.CrossRefGoogle Scholar
Vorburger, C. (2006) Temporal dynamics of genotypic diversity reveal strong clonal selection in the aphid Myzus persicae. Journal of Evolutionary Biology 19, 97–107.Google Scholar
Vorwerk, S. & Forneck, A. (2007) Analysis of genetic variation within clonal lineages of grape phylloxera (Daktulosphaira vitifoliae Fitch) using AFLP fingerprinting and DNA sequencing. Genome 50, 660–667.Google Scholar
Wagenitz, G. (Ed.) (1987) Illustrierte Flora von Mitteleuropa: Spermatophyta, Band VI, Angiospermae, Dicotyledones 4. 2nd rev. & extended version. Hegi, G. (Ed.) Berlin, Germany, Paul Parey.Google Scholar
Weir, B.S. & Cockerham, C.C. (1984). Estimating F-statistics for the analysis of population-structure. Evolution 38, 1358–1370.Google Scholar
Weisser, W.W., Braendle, C. & Minoretti, N. (1999) Predator-induced morphological shift in the pea aphid. Proceedings of the Royal Society of London, Series B: Biological Sciences 266, 1175–1181.Google Scholar
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, 1655–1666.Google Scholar