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The unstable ‘clone’: evidence from monitoring AFLP-based mutations for short-term clonal genetic variation in two asexual lineages of the grain aphid, Sitobion avenae (F.)

Published online by Cambridge University Press:  24 September 2012

H.D. Loxdale*
Affiliation:
Royal Entomological Society, The Mansion House, Chiswell Green Lane, St Albans, AL2 3NS, UK
S. Vorwerk
Affiliation:
Department of Special Crop Cultivation and Crop Physiology, University of Hohenheim, 70593 Stuttgart, Germany
A. Forneck
Affiliation:
University of Natural Resources & Life Sciences, Department of Crop Sciences, Division of Viticulture and Pomology, Konrad Lorenz Strasse 24, A-3430 Tulln, Vienna, Austria
*
*Author for correspondence E-mail: [email protected]

Abstract

Clones have been in the forefront of biological interest for many years. Even so, open discussions continue to surround the concept of clonality, which has been recently much debated in the scientific literature, both in terms of philosophical meaning as well as empirical determination. Philosophically, the clone is the horizontally produced lineage from a single fertlized egg (e.g. mammals by division of the fertilized egg and representing a single generation) or vertically produced offspring (e.g. aphids representing different successive generations) from a single asexual stem mother (originally for a particular lineage, following hatching of the overwintering sexual egg in the spring); empirically, the aspect of genetic fidelity is also considered important, so-called clones being assumed to have an identical genome among clone mates. In reality of course, such members of a clonal lineage must differ at various regions of the genome, since mutation is a fundamental property of the DNA itself. Yet few studies have so far set out to show this empirically in eukaryotic organisms, which indulge in periods of asexual reproduction, sometimes, as in aphids, over many generations. In the present study, we have investigated asexual lineages of the grain aphid, Sitobion avenae (F.), a global pest of cereals, over five successive generations employing AFLP-PCR molecular techniques. Our main interest was to see how much variation was present in the early generations and if this variation was transmitted through the asexual lineages. By monitoring AFLP-based polymorphisms, we show that, in this aphid species, of a total of 110 individuals from two lineages tested (termed SA and SB), random mutations (band deletions, more rarely additions) were apparent from the third generation onwards, and although some mutations were found to be transmitted transgenerationally, others were rarely transmitted through the particular lineages they were detected in. Using Arlequin v. 2.0, average gene diversity within the lineages was found to be 0.024 ± 0.013 and 0.031 ± 0.016 for SA and SB, respectively. It was also found from the rearing of the lineages that one lineage, SA, was more fecund than the other lineage, SB, over the five generations (N = 818 vs. N = 358 total stem mothers plus nymphs for the two lineages, respectively).

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2012

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References

Austin, A.B.M., Tatchell, G.M., Harrington, R. & Bale, J.S. (1991) A method for rearing cereal aphids in a small space. Entomologia Experimentalis et Applicata 61, 9193.Google Scholar
Benjak, A., Konradi, J., Blaich, R. & Forneck, A. (2006) Different DNA extraction methods can cause different AFLP profiles in grapevine (Vitis vinifera L.). Vitis 45, 1521.Google Scholar
Blackman, R.L. (1971) Variation in the photoperiodic response within natural populations of Myzus persicae (Sulz.). Bulletin of Entomological Research 60, 533546.Google Scholar
Blackman, R.L. (1980) Chromosomes and parthenogenesis in aphids. pp. 133148in Blackman, R.L., Hewitt, G.M. & Ashburner, M. (Eds) Insect Cytogenetics. Proceedings of the Royal Entomological Society Symposium No. 10, Oxford, 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
Cáceres, M., Ranz, J.M., Barbadilla, A., Long, M. & Ruiz, A. (1999) Generation of a widespread Drosophila inversion by a transposable element. Science 285, 415418.CrossRefGoogle ScholarPubMed
de Witte, L.C. & Stöcklin, J. (2010) Longevity of clonal plants: why it matters and how to measure it. Annals of Botany 106, 859870.Google Scholar
Dixon, A.F.G. (1989) Parthenogenetic reproduction and the rate of increase in aphids. pp. 269287in Minks, A. & Harrewijn, P. (Eds) Aphids, Their Biology, Natural Enemies and Control, vol. A. Amsterdam, The Netherlands, Elsevier.Google Scholar
Dombrovsky, A., Arthaud, L., Ledger, T.N., Tares, S. & Robichon, A. (2009) Profiling the repertoire of phenotypes influenced by environmental cues that occur during asexual reproduction. Genome Research 19, 20522063.Google Scholar
Endersby, J. (2008) A Guinea Pig's History of Biology: The Plants and Animals Who Taught Us the Facts of Life. London, UK, Arrow Books Ltd.Google Scholar
Forneck, A., Walker, M.A. & Blaich, R. (2001) Ecological and genetic aspects of grape phylloxera Daktulosphaira vitifoliae Fitch (Hemiptera: Phylloxeridae) performance on rootstock hosts. Bulletin of Entomological Research 91, 445451.CrossRefGoogle ScholarPubMed
Goldstein, D.B. & Schlötterer, C. (1999) Microsatellites: Evolution and Applications. Oxford, UK, Oxford University Press.CrossRefGoogle Scholar
Graham-Rowe, D. (2012) USB stick can sequence DNA in seconds. New Scientist online. 22nd February, 2012. Available online at http://www.newscientist.com/article/dn21495-usb-stick-can-sequence-dna-in-seconds.html (accessed 31 July 2012).Google Scholar
Hand, S.C. (1989) The overwintering of cereal aphids on Gramineae in southern England, 1977–1980. Annals of Applied Biology 115, 1729.Google Scholar
Harrington, R. (1994) Aphid layer (letter). Antenna 18, 50.Google Scholar
Hughes, R.N. (1989) A Functional Biology of Clonal Animals. London, UK, Chapman & Hall.Google Scholar
Kondrashov, A.S. (1988) Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435441.Google Scholar
Kondrashov, A.S. (1993) Classification of hypotheses on the advantage of amphimixis. Journal of Heredity 84, 372387.CrossRefGoogle ScholarPubMed
Li, Y.-C., Korol, A.B., Fahima, T., Beiles, A. & Nevo, E. (2002) Microsatellites: genomic distribution putative functions and mutational mechanisms: a review. Molecular Ecology 11, 24532465.Google Scholar
Llewellyn, K.S. (2000) Genetic structure and dispersal of cereal aphid populations. PhD thesis, University of Nottingham, Nottingham, UK.Google Scholar
Loxdale, H.D. (2008a) The nature and reality of the aphid clone – genetic variation, adaptation and evolution. Agricultural and Forest Entomology 10, 8190.Google Scholar
Loxdale, H.D. (2008b) Was Dan Janzen (1977) right about aphid clones being a ‘super-organism’, i.e. a single ‘evolutionary individual’? New insights from the use of molecular marker systems. Mitteilungen der Deutschen Gesellschaft für Allgemeine und Angewandte Entomologie 16, 437449.Google Scholar
Loxdale, H.D. (2009) What's in a clone: the rapid evolution of aphid asexual lineages in relation to geography, host plant adaptation and resistance to pesticides. pp. 535557in Schön, I., Martens, K. & van Dijk, P.J. (Eds) Lost Sex: The Evolutionary Biology of Parthenogenesis. Berlin, Germany, Springer-Verlag.CrossRefGoogle Scholar
Loxdale, H.D. (2010) Rapid genetic changes in natural insect populations. Royal Entomological Society Celebratory Meeting Insect Evolution Below the Species Level: Ecological Specialization and the Origin of Species, 22 April 2009. Loxdale, H.D., Claridge, M.F. & Mallet, J. (Eds) Ecological Entomology (special issue) 35, 155164.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, 316.Google Scholar
Loxdale, H.D. & Lushai, G. (2007) Population genetic issues: the unfolding story revealed using molecular markers. pp. 3167in van Emden, H.F. & Harrington, R. (Eds) CABI Millennium Volume: Aphids as Crop Pests. Wallingford, UK, CABI.CrossRefGoogle Scholar
Lushai, G. & Loxdale, H.D. (2002) The biological improbability of a clone (mini-review). Genetical Research, Cambridge 79, 19.Google Scholar
Lushai, G., Loxdale, H.D. & Allen, J.A. (2003) The dynamic clonal genome and its adaptive potential. Biological Journal of the Linnean Society 79, 193208.Google Scholar
Martens, K., Loxdale, H.D. & Schön, I. (2009) The elusive clone – in search of its true nature and identity. pp. 187200in Schön, I., Martens, K. & van Dijk, P.J. (Eds) Lost Sex: The Evolutionary Biology of Parthenogenesis. Berlin, Germany, Springer-Verlag.Google Scholar
Mittapalli, O., Rivera-Vega, L., Bhandary, B., Bautista, M.A., Mamidala, P., Michel, A.P., Shukle, R.H. & Mian, M.A.R. (2011) Cloning and characterization of mariner-like elements in the soybean aphid, Aphis glycines Matsumura. Bulletin of Entomological Research 101, 697704.CrossRefGoogle ScholarPubMed
Monti, V., Mandrioli, M., Rivi, M. & Manicardi, G.C. (2012a) The vanishing clone: karyotypic evidence for extensive intraclonal genetic variation in the peach potato aphid, Myzus persicae (Hemiptera: Aphididae). Biological Journal of the Linnean Society 105, 350358.Google Scholar
Monti, V., Lombardo, G., Loxdale, H.D., Manicardi, G.C. & Mandrioli, M. (2012b) Continuous occurrence of intra-individual chromosome rearrangements in the peach-potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Genetica 140, 93103.Google Scholar
Moran, N.A. (1992) The evolution of aphid life-cycles. Annual Review of Entomology 37, 321348.CrossRefGoogle Scholar
Muller, H.J. (1964) The relation of recombination to mutational advance. Mutation Research 1, 29.Google Scholar
Reusch, T.B.H. & Boström, C. (2011) Widespread genetic mosaicism in the marine angiosperm Zostera marina is correlated with clonal reproduction. Evolutionary Ecology 25, 899913.Google Scholar
Richardson, M.L., Lagos, D.M., Mitchell, R.F., Hartman, G.L. & Voegtlin, D.J. (2011) Life history and morphological plasticity of the soybean aphid, Aphis glycines. Entomologia Experimentalis et Applicata 140, 139145.Google Scholar
Schneider, S., Roessli, D. & Excoffier, L. (2000) Arlequin. A software for population genetics data analysis. Version 2.0 Switzerland: University of Geneva. Available online at http://popgen.unibe.ch/software/arlequin/software/2.000/manual/Arlequin.pdf (accessed 31 July 2012).Google Scholar
Schön, I., Martens, K. & van Dijk, P. (Eds) (2009) Lost Sex: The Evolutionary Biology of Parthenogenesis. Berlin, Germany, Springer Press.Google Scholar
Simon, J.-C., Rispe, C. & Sunnucks, P. (2002) Ecology and evolution of sex in aphids. Trends in Ecology and Evolution 17, 3439.Google Scholar
Simon, J.-C., Delmotte, F., Rispe, C. & Crease, T. (2003) Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biological Journal of the Linnean Society 79, 151163.CrossRefGoogle Scholar
Suomalainen, E., Saura, A., Lokki, J. & Teeri, T. (1980) Genetic polymorphism and evolution in parthenogenetic animals. 9. Absence of variation within parthenogenetic aphid clones. Theoretical & Applied Genetics 57, 129132.Google Scholar
The International Aphid Genomics Consortium (2010) Genome Sequence of the Pea Aphid Acyrthosiphon pisum. PLoS Biology 8(2), e1000313.Google Scholar
Trybush, S., Hanley, S., Cho, K.H., Jahodova, S., Grimmer, M., Emelianov, I., Bayon, C. & Karp, A. (2006) Getting the most out of fluorescent amplified fragment length polymorphism. Canadian Journal of Botany-Revue Canadienne de Botanique 84, 13471354.Google Scholar
van Emden, H.F. (2009) Artificial diet for aphids – thirty years’ experience. Redia 92, 163167.Google Scholar
Vickerman, G.P. & Wratten, S.D. (1979) The biology and pest status of cereal aphids (Hemiptera, Aphididae) in Europe: a review. Bulletin of Entomological Research 69, 132.Google Scholar
Vorwerk, S. & Forneck, A. (2006) Reproductive mode of grape phylloxera (Daktulosphaira vitifoliae, Homoptera: Phylloxeridae) in Europe: molecular evidence for predominantly asexual populations and a lack of gene flow between them. Genome 49, 678687.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, 660667.Google Scholar
Webber, H.J. (1903) New horticultural and agricultural terms. Science 18, 501503.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, 16551666.Google Scholar
Wool, D. & Hales, D.F. (1997) Phenotypic plasticity in Australian cotton aphid (Homoptera: Aphididae): host plant effects on morphological variation. Annals of the Entomological Society of America 90, 316328.Google Scholar