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Continuous occurrence of intra-individual chromosome rearrangements in the peach potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae)

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Abstract

Analysis of the holocentric mitotic chromosomes of the peach-potato aphid, Myzus persicae (Sulzer), from clones labelled 50, 51 and 70 revealed different chromosome numbers, ranging from 12 to 14, even within each embryo, in contrast to the standard karyotype of this species (2n = 12). Chromosome length measurements, combined with fluorescent in situ hybridization experiments, showed that the observed chromosomal mosaicisms are due to recurrent fragmentations of chromosomes X, 1 and 3. Contrary to what has generally been reported in the literature, X chromosomes were frequently involved in recurrent fragmentations, in particular at their telomeric ends opposite to the nucleolar organizer region. Supernumerary B chromosomes have been also observed in clones 50 and 51. The three aphid clones showed recurrent fissions of the same chromosomes in the same regions, thereby suggesting that the M. persicae genome has fragile sites that are at the basis of the observed changes in chromosome number. Experiments to induce males also revealed that M. persicae clones 50, 51 and 70 are obligately parthenogenetic, arguing that the reproduction by apomictic parthenogenesis favoured the stabilization and inheritance of the observed chromosomal fragments.

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References

  • Blackman RL (1985) Aphid cytology and genetics. Evolution and biosystematics of aphids. In: Proceedings of the international symposium at Jablonna, Ossolineum, Wroclaw, pp 170–237

  • Blackman RL (1987) Morphological discrimination of a tobacco-feeding form from Myzus persicae (Sulzer) (Hemiptera: Aphididae), and a key to New World Myzus (Nectarosiphon) species. Bull Entomol Res 77:713–730

    Article  Google Scholar 

  • Blackman RL (1988) Stability of a multiple X chromosome system and associated B chromosomes in birch aphids (Euceraphis spp.; Homoptera: Aphididae). Chromosoma 96:318–324

    Article  Google Scholar 

  • Blackman RL, Spence JM, Normark BB (2000) High diversity of structurally heterozygous karyotypes and rDNA arrays in parthenogenetic aphids of the genus Trama (Aphididae: Lachninae). Heredity 12:254–260

    Article  Google Scholar 

  • Brown G, Blackman RL (1988) Karyotype variation in the corn leaf aphid, Rophalosiphon maidis (Fitch), species complex (Hemiptera, Aphididae) in relation to host plant and morphology. Bull Entomol Res 78:351–363

    Article  Google Scholar 

  • Cáceres M, Ranz JM, Barbadilla A, Long M, Ruiz A (1999) Generation of a widespread Drosophila inversion by a transposable element. Science 285:415–418

    Article  PubMed  Google Scholar 

  • Camacho JPM (2005) B chromosomes. In: Gregory TR (ed) The evolution of the genome. Elsevier Academic Press, Burlington, pp 223–289

    Chapter  Google Scholar 

  • Crema R (1979) Egg viability and sex determination in Megoura viciae (Homoptera, Aphididae). Entomol Exp Appl 26:152–156

    Article  Google Scholar 

  • De Barro PJ, Sherratt TN, David O, Maclean N (1995) An investigation of the differential performance of clones of the aphid S. avenae on two hosts. Oecologia 104:379–385

    Article  Google Scholar 

  • Delmotte F, Leterme N, Bonhomme J, Rispe C, Simon JC (2001) Multiple routes to asexuality in an aphid species. Proc R Soc Biol Sci B 268:2291–2299

    Article  CAS  Google Scholar 

  • Devonshire AL, Field LM, Foster SP, Moores GD, Williamson MS, Blackman RL (1999) The evolution of insecticide resistance in the peach–potato aphid, Myzus persicae. In: Denholm I, Pickett JA, Devonshire AL (eds) Insecticide resistance: from mechanisms to management. CABI Publishing, Wallingford, pp 1–9

    Google Scholar 

  • Dixon AFG (1989) Parthenogenetic reproduction and the rate of increase in aphids. In: Minks A, Harrewijn P (eds) Aphids, their biology, natural enemies and control, vol A. Elsevier, The Netherlands, pp 269–287

    Google Scholar 

  • Donlon TA, Magenis RE (1983) Methyl green is a substitute for distamycin A in the formation of distamycin A/DAPI C-bands. Hum Genet 65:144–146

    Article  PubMed  CAS  Google Scholar 

  • Fenton B, Woodford JAT, 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. Mol Ecol 7:1475–1487

    Article  PubMed  CAS  Google Scholar 

  • Fenton B, Margaritopoulos JT, Malloch G, Foster SP (2010) Micro-evolutionary change in relation to insecticide resistance in the peach-potato aphid, Myzus persicae. Ecol Entomol 35:131–146

    Article  Google Scholar 

  • Field LM, Blackman RL (2003) Insecticide resistance in the aphid Myzus persicae (Sulzer): chromosome location and epigenetic effects on esterase gene expression in clonal lineages. Biol J Linn Soc 79:107–113

    Article  Google Scholar 

  • Foster SP, Devine G, Devonshire AL (2007) Insecticide resistance. In: Van Emden HF, Harrington R (eds) Aphids as crop pests. CABI, UK, pp 261–286

    Chapter  Google Scholar 

  • Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, Cambridge

    Google Scholar 

  • Hales D (1989) The chromosomes of Scoutedenia lutea (Homopteraa, Aphididae, Greenidinae) with an account of meiosis in the male. Chromosoma 98:295–300

    Article  PubMed  CAS  Google Scholar 

  • Hales D, Wilson ACC, Spence JM, Blackman RL (2000) Confirmation that Myzus antirrhinii (Macchiati) occurs in Australia using morphometrics, microsatellite typing and analysis of novel karyotypes by fluorescent in situ hybridization. Aust J Entomol 39:123–129

    Article  Google Scholar 

  • Janzen DH (1977) What are dandelions and aphids? Am Nat 111:586–589

    Article  Google Scholar 

  • Jenkins RL (1991) Colour and symbionts of aphids. PhD thesis, University of East Anglia, UK

  • John B (1983) The role of chromosome change in the evolution of orthopteroid insects. In: Sharma AK, Sharma A (eds) Chromosomes in evolution of eukaryotic groups, vol I. CRC Press, Boca Raton, pp 1–110

    Google Scholar 

  • Khuda-Bukhsh AR, Pal NB (1985) Cytogenetical studies on aphids (Homoptera: Aphididae) from India: I. Karyomorphology of eight species of Aphis. Entomologia 10:171–177

    Google Scholar 

  • Lauritzen M (1982) Q- and G-band identification of two chromosomal rearrangements in the peach-potato aphids Myzus persicae (Sulzer), resistant to insecticides. Hereditas 97:95–102

    Article  Google Scholar 

  • Losey JE, Ives AR, Harmon J, Ballantyne F, Brown C (1997) A polymorphism maintained by opposite patterns of parasitism and predation. Nature 388:269–272

    Article  CAS  Google Scholar 

  • Loxdale HD (2007) Population genetic issues: the unfolding story revealed using molecular markers. In: Van Emden HF, Harrington R (eds) Aphids as crop pests. CABI Millennium Volume, CABI, UK, pp 31–67

    Chapter  Google Scholar 

  • Loxdale HD (2008a) 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. Mitt DGaaE 16:437–449

    Google Scholar 

  • Loxdale HD (2008b) The nature and reality of the aphid clone: genetic variation, adaptation and evolution. Agric For Entomol 10:81–90

    Article  Google Scholar 

  • Loxdale HD (2009) What’s in a clone: the rapid evolution of aphid asexual lineages in relation to geography, host plant adaptation and resistance to pesticides. In: Schon I, Martens K, van Dijk P (eds) Lost sex: the evolutionary biology of parthenogenesis. Springer, Heidelberg, pp 535–557

    Google Scholar 

  • Loxdale HD (2010a) Setting the scene… meeting up with Darwin and Wallace. Ecol Entomol 35:1–9

    Article  Google Scholar 

  • Loxdale HD (2010b) Rapid genetic changes in natural insect populations. Ecol Entomol 35:155–164

    Article  Google Scholar 

  • Loxdale HD, Lushai G (2003) Rapid changes in clonal lines: the death of a ‘sacred cow’. Biol J Linn Soc 79:3–16

    Article  Google Scholar 

  • Loxdale HD, Lushai G (2007) Population genetic issues: the unfolding story revealed using molecular markers. In: Van Emden HF, Harrington R (eds) Aphids as crop pests. CABI Millennium Volume, CABI, UK, pp 31–67

    Chapter  Google Scholar 

  • Lushai G, Loxdale HD, Brookes CP, von Mende N, Harrington R, Hardie J (1997) Genotypic variation among different phenotypes within aphid clones. Proc R Soc Lond B 264:725–730

    Article  CAS  Google Scholar 

  • Lushai G, De Barro PJ, Sherratt TN, Maclean N (1998) Genetic variation within a parthenogenetic lineage. Insect Mol Biol 7:337–344

    Article  PubMed  CAS  Google Scholar 

  • Lushai G, Loxdale H, Allen JA (2003) The dynamic clonal genome and its adaptive potential. Biol J Linn Soc 79:193–208

    Article  Google Scholar 

  • Mandrioli M, Bizzaro D, Giusti M, Manicardi GC, Bianchi U (1999a) The role of rDNA genes in X chromosomes association in the aphid Acyrthosiphon pisum. Genome 42:381–386

    PubMed  CAS  Google Scholar 

  • Mandrioli M, Bizzaro D, Manicardi GC, Gionghi D, Bassoli L, Bianchi U (1999b) Cytogenetic and molecular characterization of a highly repeated DNA sequence in the peach potato aphid Myzus persicae. Chromosoma 108:436–442

    Article  PubMed  CAS  Google Scholar 

  • Mandrioli M, Bizzaro D, Giusti M, Manicardi GC, Bianchi U (1999c) NOR heteromorphism within a parthenogenetic lineage of the aphid Megoura viciae. Chromosom Res 7:157–162

    Article  CAS  Google Scholar 

  • Mandrioli M, Azzoni P, Lombardo G, Manicardi GC (2011) Composition and epigenetic markers of heterochromatin in the aphid Aphis nerii (Hemiptera: Aphididae). Cytogenet Genome Res 133:67–77

    Article  PubMed  CAS  Google Scholar 

  • Martens K, Loxdale HD, Schön I (2009) The elusive clone—in search of its true nature and identity. In: Schon I, Martens K, van Dijk P (eds) Lost sex: the evolutionary biology of parthenogenesis. Springer, Heidelberg, pp 187–200

    Google Scholar 

  • Monti V, Giusti M, Bizzaro D, Manicardi GC, Mandrioli M, Rivi M (2011) Presence of a functional (TTAGG) n telomere-telomerase system in aphids. Chromosom Res 19:625–633

    Article  CAS  Google Scholar 

  • Monti V, Mandrioli M, Rivi M, Manicardi GC (2012) The vanishing clone: occurrence of repeated chromosome fragmentations in the aphid Myzus persicae (Homoptera, Aphididae). Biol J Linn Soc 105:350–358

    Article  Google Scholar 

  • Schweizer D (1976) Reverse fluorescent chromosome banding with chromomycin and DAPI. Chromosoma 58:307–324

    Article  PubMed  CAS  Google Scholar 

  • Shufran KA, Mayo ZB, Crease TJ (2003) Genetic changes within an aphid clone: homogenization of rDNA intergenic spacers after insecticide selection. Biol J Linn Soc 79:101–105

    Article  Google Scholar 

  • Soumalainen E, Saura A, Lokki J (1987) Cytology and evolution in parthenogenesis. CRC Press, Boca Raton

    Google Scholar 

  • Spence JM, Blackman RL (1998) Chromosomal rearrangements in the Myzus persicae group and their evolutionary significance. In: Nieto Nafria JM, Dixon AFG (eds) Aphids in natural and managed ecosystem. Universidad de Leon, Secretario de Publicaciones, Leon, pp 113–118

    Google Scholar 

  • Spence JM, Blackman RL, Testa JM, Ready PD (1998) A 169 bp tandem repeat DNA marker for subtelomeric heterochromatin and chromosomal rearrangements in aphids of the Myzus persicae group. Chromosom Res 6:167–175

    Article  CAS  Google Scholar 

  • Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306

    Article  PubMed  CAS  Google Scholar 

  • Terradot L, Simon JC, Leterne N, Bourdin D, Wilson ACC, Guatier JP, Robert Y (1999) Molecular characterization of clones of the Myzus persicae complex differing in their ability to transmit the potato leafroll lutovirus (PLRV). Bull Entomol Res 89:255–263

    Article  Google Scholar 

  • Van Emden HF, Harrington R (2007) Aphids as crop pests. CABI, UK

    Book  Google Scholar 

  • van Toor RF, Fenton B, Malloch GL, Anderson EA, Dawson G (2012) Survival of sensitive and insecticide resistant genotypes of Myzus persicae on potato crops following application of different insecticide classes. Pest Manag Sci (in press)

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Whitman DW, Agrawal A (2009) What is phenotypic plasticity and why is it important? In: Whitman DW, Ananthakrishnan TN (eds) Phenotypic plasticity of insects: mechanisms and consequences. Science Publishers, Enfield, pp 1–63

    Chapter  Google Scholar 

  • Wool D, Hales DF (1997) Phenotypic plasticity in Australian cotton aphid: host plant effects on morphological variation. Ann Entomol Soc Am 90:316–328

    Google Scholar 

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Acknowledgments

We are greatly indebted to Dr. Emanuele Mazzoni (Università Cattolica di Piacenza, Italy) for sending us the aphid strains. This work was supported by the grant “F.A.R.” from the University of Modena and Reggio Emilia (M. M.) and by the grant “Experimental approach to the study of evolution” from the Department of Animal Biology of the University of Modena and Reggio Emilia (M. M.).

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  1. Dipartimento di Biologia, Università di Modena e Reggio Emilia, Via Campi 213/D, 41125, Modena, Italy

    Valentina Monti, Giorgia Lombardo & Mauro Mandrioli

  2. Dipartimento di Scienze Agrarie e degli Alimenti, Università di Modena e Reggio Emilia, Reggio Emilia, Italy

    Valentina Monti & Gian Carlo Manicardi

  3. Royal Entomological Society, The Mansion House, Chiswell Green Lane, St. Albans, UK

    Hugh D. Loxdale

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  1. Valentina Monti
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  2. Giorgia Lombardo
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  3. Hugh D. Loxdale
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  4. Gian Carlo Manicardi
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  5. Mauro Mandrioli
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Correspondence to Mauro Mandrioli.

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Monti, V., Lombardo, G., Loxdale, H.D. et al. Continuous occurrence of intra-individual chromosome rearrangements in the peach potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Genetica 140, 93–103 (2012). https://doi.org/10.1007/s10709-012-9661-x

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