Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-20T03:33:22.117Z Has data issue: false hasContentIssue false
  • English
  • Français

Seasonal and annual genotypic variation and the effect of climate on population genetic structure of the cereal aphid Sitobion avenae in northern France

Published online by Cambridge University Press:  13 December 2007

C.-A. Dedryver ,
J.-F. Le Gallic ,
L. Haack ,
F. Halkett ,
Y. Outreman  and
J.-C. Simon
C.-A. Dedryver*
Affiliation:
UMR 1099 INRA-Agrocampus Rennes ‘Biologie des Organismes et des Populations appliquée à la Protection des Plantes’ (BiO3P), Domaine de la Motte, F35653Le Rheu, France
J.-F. Le Gallic
Affiliation:
UMR 1099 INRA-Agrocampus Rennes ‘Biologie des Organismes et des Populations appliquée à la Protection des Plantes’ (BiO3P), Domaine de la Motte, F35653Le Rheu, France
L. Haack
Affiliation:
UMR 1099 INRA-Agrocampus Rennes ‘Biologie des Organismes et des Populations appliquée à la Protection des Plantes’ (BiO3P), Domaine de la Motte, F35653Le Rheu, France
F. Halkett
Affiliation:
UMR 1099 INRA-Agrocampus Rennes ‘Biologie des Organismes et des Populations appliquée à la Protection des Plantes’ (BiO3P), Domaine de la Motte, F35653Le Rheu, France
Y. Outreman
Affiliation:
UMR 1099 INRA-Agrocampus Rennes ‘Biologie des Organismes et des Populations appliquée à la Protection des Plantes’ (BiO3P), Domaine de la Motte, F35653Le Rheu, France
J.-C. Simon
Affiliation:
UMR 1099 INRA-Agrocampus Rennes ‘Biologie des Organismes et des Populations appliquée à la Protection des Plantes’ (BiO3P), Domaine de la Motte, F35653Le Rheu, France
*
*Author for correspondence Fax: 0033 223 485 150 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Changes in the genetic structure and genotypic variation of the aphid Sitobion avenae collected from cereal crops in northern France were examined by analysing variation at five microsatellite loci across several years and seasons. Little regional and temporal differentiation was detected, as shown by very low FST among populations. Repeated genotypes, significant heterozygote deficits, positive FIS values and frequent linkage disequilibria were found in nearly all samples, suggesting an overall pattern of reproductive mode variation in S. avenae populations. In addition, samples from Brittany (Bretagne) showed greater signs of asexual reproduction than those from the north of France, indicating a trend toward increasing sexuality northward. These patterns of reproductive variation in S. avenae are consistent with theoretical models of selection of aphid reproductive modes by climate. Contrasting with little changes in allelic frequencies, genotypic composition varied substantially in time and, to a lesser extent, in space. An important part of changes in genotypic arrays was due to the variation in frequency distribution of common genotypes, i.e. those that were found at several instances in the samples. Genotypic composition was also shown to vary according to climate, as genotypic diversity in spring was significantly correlated with the severity of the previous winter and autumn. We propose that the genetic homogeneity among S. avenae populations shown here across large temporal and spatial scales is the result of two forces: (i) migration conferred by high dispersal capabilities, and (ii) selection over millions of hectares of cereals (mostly wheat) bred from a narrow genetic base.

Keywords

crop pestsmicrosatellitesclonal diversitygenetic differentiationreproductive strategiesdispersaloverwintering
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 98 , Issue 2 , April 2008 , pp. 159 - 168
Copyright
Copyright © Cambridge University Press 2007

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

Basky, Z. & Harrington, R. (2000) Cereal aphid flight activity in Hungary and England compared by suction traps. Journal of Pest Science 73, 70–74.CrossRefGoogle Scholar
Blackman, R.L. (1971) Variation in the photoperiodic response within natural populations of Myzus persicae Sulz. Bulletin of Entomological Research 60, 533–546.CrossRefGoogle ScholarPubMed
Blackman, R.L. (1974) Aphids. 169 pp. London, Ginn & Co Ltd.Google Scholar
Caillaud, C.M., Dedryver, C.A., Di Pietro, J.P., Simon, J.C., Fima, F. & Chaubet, B. (1995) Clonal variability in the response of Sitobion avenae (Homoptera: Aphididae) to resistant wheat lines. Bulletin of Entomological Research 85, 189–195.CrossRefGoogle Scholar
De Barro, P.J., Sherratt, T.N., Brookes, C.P., David, O. & Maclean, N. (1995a) Spatial and temporal genetic variation in British field populations of the grain aphid Sitobion avenae (Hemiptera: Aphididae) studied using RAPD-PCR. Proceedings of the Royal Society of London Series B 262, 321–327.Google ScholarPubMed
De Barro, P.J., Sherratt, T.N., Carvalho, G.R., Nicol, D., Iyengar, A. & Maclean, N. (1995b) 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 comparison of life history traits associated with sexuality. Ecological Entomology 23, 123–132.CrossRefGoogle Scholar
Dedryver, C.-A., Hullé, M., Le Gallic, J.-F., Caillaud, M. & Simon, J.-C. (2001) Coexistence in space and time of sexual and asexual populations of the cereal aphid Sitobion avenae. Oecologia 128, 379–388.CrossRefGoogle ScholarPubMed
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, 711–723.CrossRefGoogle ScholarPubMed
Dixon, A.F.G. (1998) Aphid Ecology. 2nd edn.300 pp. London, Chapman and 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., 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, 1475–1487.CrossRefGoogle ScholarPubMed
Frantz, A., Plantegenest, M. & Simon, J.-C. (2006) Temporal habitat variability and the maintenance of sex in host populations of the pea aphid. Proceedings of the Royal Society of London Series B 273, 2887–2891.Google ScholarPubMed
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, 1867–1877.CrossRefGoogle ScholarPubMed
Gomez, A. & Carvalho, G.R. (2000) Sex, parthenogenesis and genetic structure of rotifers: microsatellite analysis of contemporary and resting egg bank populations. Molecular Ecology 9, 203–214.CrossRefGoogle ScholarPubMed
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, 143–152.CrossRefGoogle ScholarPubMed
Haack, L., Simon, J.-C., Gauthier, J.-P., Plantegenest, M. & Dedryver, C.-A. (2000) Evidence for predominant clones in a cyclically parthenogenetic organism provided by combined demographic and genetic analyses. Molecular Ecology 9, 2055–2066.CrossRefGoogle Scholar
Halkett, F., Simon, J.-C. & Balloux, F. (2005) Tackling the population genetics of clonal and partially clonal organisms. Trends in Ecology and Evolution 20, 194–201.CrossRefGoogle ScholarPubMed
Hand, S.C. & Wratten, S.D. (1985) Production of sexual morphs by the monoecious cereal aphid Sitobion avenae. Entomologia Experimentalis et Applicata 38, 239–247.CrossRefGoogle Scholar
Ivey, C.T. & Richards, J. (2001) Genotypic diversity and clonal structure of Everglades sawgrass, Cladium jamaicense (Cyperaceae). International Journal of Plant Science 162(6), 1327–1335.CrossRefGoogle Scholar
Jenkins, R.L., Loxdale, H.D., Brookes, C.P. & Dixon, A.F.G. (1999) The major carotenoid pigments of the grain aphid Sitobion avenae (F.) (Hemiptera: Aphididae). Physiological Entomology 24, 171–178.CrossRefGoogle Scholar
Kunert, G., Otto, S., Röse, U.S.R., Gershenzon, J. & Weisser, W. (2005) Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecology Letters 8, 596–603.CrossRefGoogle Scholar
Lees, A.D. (1959) The role of photoperiod and temperature in the determination of parthenogenetic and sexual forms in the aphid Megoura viciae Buckton. I. The influence of those factors on apterous virginoparae and their progeny. Journal of Insect Physiology 3, 92–117.CrossRefGoogle Scholar
Llewellyn, K.S., Loxdale, H.D., Harrington, R., Brookes, C.P., Clark, S.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
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.CrossRefGoogle ScholarPubMed
Loxdale, H.D., Tarr, I.J., Weber, C.P., Brookes, C.P., Digby, P.G. & Castañera, P. (1985) Electrophoretic study of enzymes from cereal aphid populations. III. Spatial and temporal genetic variation of Sitobion avenae F. (Hemiptera: Aphididae). Bulletin of Entomological Research 75, 121–141.CrossRefGoogle Scholar
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, 291–311.CrossRefGoogle Scholar
Lushai, G., Markovitch, O. & Loxdale, H.D. (2002) Hostbased genotype variation in insects revisited. Bulletin of Entomological Research 92, 159–164.CrossRefGoogle ScholarPubMed
Papura, D., Simon, J.C., Halkett, F., Delmotte, F., Le Gallic, J.F. & Dedryver, C.-A. (2003) Predominance of sexual reproduction in Romanian populations of the aphid Sitobion avenae inferred from phenotypic and genetic structure. Heredity 90, 397–404.CrossRefGoogle ScholarPubMed
Piélou, E.C. (1969) An Introduction to Mathematical Ecology. 286 pp. New York, Wiley-Interscience.Google Scholar
Plumb, R.T. (1983) Barley yellow dwarf virus-a global problem. pp. 185–198. in Plumb, R.T. & Thresh, J.M. (Eds) Plant Virus Epidemiology. Oxford, UK, Blackwell Scientific Publications.Google Scholar
Powell, S.J. & Bale, J.S. (2004) Cold shock injury and ecological costs of rapid cold hardening in the grain aphid Sitobion avenae (Hemiptera: Aphididae). Journal of Insect Physiology 50, 277–284.CrossRefGoogle ScholarPubMed
Raymond, M. & Rousset, F. (1995) Genepop, a population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248–249.CrossRefGoogle Scholar
Rispe, C. & Pierre, J.-S. (1998) Coexistence between cyclical parthenogens, obligate parthenogens, and intermediates in a fluctuating environment. Journal of Theoretical Biology 195, 97–110.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.CrossRefGoogle Scholar
S-Plus 6.2 (2002) Insightful Corporation, Seattle, WA.Google Scholar
Schneider, S., Klueffer, J.M., Roessli, D. & Excoffier, L. (2000) Arlequin ver. 2000: A Software for Population Genetic Data Analysis. Genetics and Biometry Laboratory, University of Geneva. Switzerland.Google Scholar
Shufran, K.A., Black, W.C. IV & Margolies, D.C. (1991) DNA fingerprinting to study spatial and temporal distributions of an aphid, Schizaphis graminum (Homoptera: Aphididae). Bulletin of Entomological Research 81, 303–313.CrossRefGoogle Scholar
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, 531–545.CrossRefGoogle ScholarPubMed
Simon, J.-C., Rispe, C. & Sunnucks, P. (2002) Ecology and evolution of sex in aphids. Trends in Ecology and Evolution 17, 34–39.CrossRefGoogle 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 Ecology and Evolution 13, 510–524.Google ScholarPubMed
Sunnucks, P., England, P.R., Taylor, A.C. & Hales, D.F. (1996) Microsatellite and chromosome evolution of parthenogenetic Sitobion aphids in Australia. Genetics 144, 747–756.CrossRefGoogle ScholarPubMed
Sunnucks, P., De Barro, P.J., Lushai, G., Maclean, N. & Hales, D.F. (1997) Genetic structure of an aphid studied using microsatellite: cyclic parthenogenesis, differentiated lineages, and host specialization. Molecular Ecology 6, 1059–1073.CrossRefGoogle ScholarPubMed
Tagu, D., Sabater-Munoz, B. & Simon, J.-C. (2005) Deciphering the reproductive polyphenism in aphids. Invertebrate Reproduction and Development 48, 71–80.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, 905–914.CrossRefGoogle Scholar
Vereijken, P.H. (1979) Feeding and multiplication of three cereal aphid species and their effect on yield of winter wheat. 58 pp. Agricultural Research Report 88, PUDOC, Wageningen Nederlands.Google Scholar
Vialatte, A., Dedryver, C.-A., Simon, J.C., Galman, M. & Plantegenest, M. (2005) Limited genetic exchanges between populations of an insect pest living on uncultivated and related cultivated host plants. Proceedings of the Royal Society of London Series B 272, 1075–1082.Google ScholarPubMed
Vorburger, C. (2006) Temporal dynamics of genotypic diversity reveals strong clonal selection in the aphid Myzus persicae. Journal of Evolutionary Biology 19, 97–107.CrossRefGoogle ScholarPubMed
Weber, G. (1985) On the ecological genetics of Sitobion avenae (F.) (Hemiptera, Aphididae). Zeitschrift für Angewandte Entomologie 100, 100–110.CrossRefGoogle Scholar
Weir, B.S. (1990) Genetic Data Analysis. 377 pp. Sunderland, MA, Sinauer.Google Scholar
Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.Google ScholarPubMed
Williams, C.T. (1980) Low temperature mortality of cereal aphids. IOBC/WPRS Bulletin 3(4), 63–66.Google Scholar
Wilson, A.C.C., Sunnucks, P. & Hales, D.F. (2003) Heritable genetic variation and potential for adaptive evolution in asexual aphids (Aphidoidea). Biological Journal of the Linnean Society 79, 115–135.CrossRefGoogle Scholar
Wright, S. (1969) Evolution and the Genetics of Populations. Vol. 2. The Theory of Gene Frequencies. 533 pp. Chicago, IL, USA, University of Chicago Press.Google Scholar