The potential role of chromosome telomere resetting consequent upon sex in the population dynamics of aphids: An hypothesis

Biological Journal of the Linnean Society

Volumn 90, Issue 4, 2007, Pages 719-728

  Lushai, Gugs ^a   Loxdale, Hugh D ^a,b  

^a ROTHAMSTED RESEARCH   (United Kingdom)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Aphid; Asexual; Eukaryote clone; Evolution; Mutational load; Red Queen hypothesis; Sexual; Telomeres

Indexed keywords

ADAPTIVE RADIATION; APHID; ASEXUAL REPRODUCTION; CHROMOSOME; CLONE; GENETIC VARIATION; MUTATION; POPULATION DYNAMICS; POPULATION STRUCTURE; RECOMBINATION; RED QUEEN HYPOTHESIS; REPRODUCTIVE STRATEGY; SEXUAL REPRODUCTION;

APHIDIDAE; BDELLOIDA; EUKARYOTA; MAMMALIA; ROTIFERA;

EID: 33947427876     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2007.00760.x     Document Type: Article

References (86)

1. Arkhipova IR. 2005. Mobile genetic elements and sexual reproduction. Cytogenetic and Genome Research 110: 372-382.
2. Arkhipova IR, Meselson M. 2000. Transposable elements in sexual and ancient asexual taxa. Proceedings of the National Academy of Sciences of the United States of America 97: 14473-14477.
3. Arkhipova IR, Meselson M. 2005. Diverse DNA transposons in rotifers of the class Bdelloidea. Proceedings of the National Academy of Sciences of the United States of America 102: 11781-11786.
4. Arkhipova IR, Morrison HG. 2001. Three retrotransposon families in the genome of Giardia lamblia: two telomeric, one dead. Proceedings of the National Academy of Sciences of the United States of America 98: 14497-14502.
5. Bell G. 1982. The masterpiece of nature: the evolution and genetics of sexuality. Berkeley, CA: University of California Press.
6. Biessmann H, Walter MF, Mason JM. 1997. Drosophila telomere elongation. Ciba Foundation Symposium 211: 53-67.
7. Birky CW. 1996. Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics 144: 427-437.
8. Birky CW, Wolf C, Maughan H, Hebertson L, Henry E. 2005. Speciation and selection without sex. Hydrobiologia 546: 29-45.
9. Blackburn EH. 2000. Telomere states and cell fates. Nature 408: 53-56.
10. Blackman RL. 1980. Chromosomes and parthenogenesis in aphids. In: Blackman RL, Hewitt GM, Ashburner M, eds. Insect cytogenetics, 10th symposium of the Royal Entomological Society. Oxford: Blackwell Scientific Publications, 133-148.
11. Blackman RL, Eastop VF. 2000. Aphids on the world's crops: an identification and information guide, 2nd edn. Chichester: John Wiley and Sons Ltd.
12. 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 84: 254-260.
13. Briggs H. 2003. Goodbye Dolly. Available at: http://news.bbc.co.uk/1/hi/sci/tech/2764069.stm (see also Dolly the sheep clone dies young. Available at: http://news.bbc.co.uk/1/hi/sci/tech/2764039. stm).
14. Chan SRWL, Blackburn EH. 2004. Telomeres and telomerase. Philosophical Transactions of the Royal Society, Biological Sciences 359: 109-121.
15. Chaplin JA, Havel JE, Herbert PDN. 1997. Sex and Ostracods. Trends in Ecology and Evolution 9: 435-439.
16. Crease TJ, Stanton DJ, Hebert PDN. 1989. Polyphyletic origins of asexuality in Daphnia pulex. 2. Mitochondrial-DNA variation. Evolution 43: 1016-1026.
17. D'Souza TG, Storhas M, Schuklenberg H, Beukeboom LW, Michiels NK. 2004. Occasional sex in an 'asexual' polyploid hermaphrodite. Proceedings of the Royal Society of London Series B, Biological Sciences 271: 1001-1007.
18. Darwin CR. 1876. Autobiography. London: Watts, 154.
19. Delmotte F, Leterme N, Bonhomme J, Rispe C, Simon J-C. 2001. Multiple routes to asexuality in an aphid. Proceedings of the Royal Society of London Series B, Biological Sciences 268: 2291-2299.
20. Delmotte F, Sabater-Munoz B, Prunier-Leterme N, Latorre A, Sunnucks P, Rispe C, Simon J-C. 2003. Phylogenetic evidence for hybrid origins of asexual lineages in an aphid species. Evolution 57: 1291-1303.
21. Dixon AFG. 1998. Aphid ecology, 2nd edn. London: Chapman & Hall.
22. Fenton B, Malloch G, Germa F. 1998. A study of variation in rDNA ITS regions shows that two haplotypes coexist within a single aphid genome. Genome 41: 337-345.
23. Fontaneto D, Melone G, Ricci C. 2005. Connectivity and nestedness of the meta-community structure of moss dwelling bdelloid rotifers along a stream. Hydrobiologia 542: 131-136.
24. Frydrychova R, Grossmann P, Trubac P, Vitkova M, Marec FE. 2004. Phylogenetic distribution of TTAGG telomeric repeats in insects. Genome 47: 163-178.
25. Frydrychova R, Marec F. 2002. Repeated losses of TTAGG telomere repeats in evolution of beetles (Coleoptera). Genetica 115: 179-187.
26. 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.
27. Haack L, Simon J-C, Gautheir 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.
28. Hamilton WD, Axelrod R, Tanese R. 1990. Sexual reproduction as an adaptation to resist parasites (a review). Proceedings of the National Academy of Sciences of the United States of America 87: 3566-3573.
29. Haussmann MF, Winkler DW, Vleck CM. 2005. Longer telomeres associated with higher survival in birds. Biology Letters 1: 212-214.
30. Havel JE, Hebert PDN, Delorme LD. 1990. Genotypic diversity of asexual ostracoda from a low arctic site. Journal of Evolutionary Biology 3: 391-410.
31. Hayflick L. 1965. The limited in vitro lifespan of human diploid cell strains. Experimental Cell Research 37: 614-636.
32. Helden AJ, Dixon AFG. 2002. Life-cycle variation in the aphid Sitobion avenae: costs and benefits of male production. Ecological Entomology 27: 692-701.
33. Hickey DA. 1982. Selfish DNA: a sexually-transmitted nuclear parasite. Genetics 101: 519-531.
34. Horne DJ, Baltanas A, Paris G. 1998. Geographical distribution of reproductive modes in living non-marine Ostracods. In: Martens K, ed. Sex and parthenogenesis: evolutionary ecology of reproductive modes in non-marine Ostracods. Leiden: Backhuys Publications, 77-99.
35. Imms AD. 1970. A general textbook of entomology, 9th rev. edn. London: Methuen & Co Ltd.
36. Jokela J, Lively CM, Dybdahl MF, Fox JA. 2003. Genetic variation in sexual and clonal lineages of a freshwater snail. Biological Journal of the Linnean Society 79: 165-181.
37. Jones S. 1996. In the blood: god, genes and destiny. London: Harper-Collins.
38. Kirk KE, Harmon BP, Reichardt IK, Sedat JW, Blackburn EH. 1997. Block in anaphase chromosome separation caused by telomerase template mutation. Science 275: 1478-1481.
39. Kohiyama M, Hiraga S, Matic I, Radman M. 2003. Bacterial sex: playing voyeurs 50 years later. Science 301: 802-803.
40. Kondrashov AS. 1988. Deleterious mutations and the evolution of sexual reproduction. Nature 336: 435-441.
41. Kondrashov AS. 1993. Classification of hypotheses on the advantage of amphimixis. Journal of Heredity 84: 372-387.
42. de Lange T, Jacks T. 1999. For better of worse? Telomerase inhibition and cancer. Cell 98: 273-275.
43. Lanza RP, Cibellim JB, Blackwellm C, Cristofalom VJ, Francis MK, Baerlocher GM, Mak J, Schertzer M, Chavez EA, Sawyer N, Lansdorp PM, West MD. 2000. Extension of cell life-span and telomere length in animals cloned from senescent somatic cells. Science 288: 665-669.
44. Llewellyn KS, Loxdale HD, Harrington R, Brookes CP, Clark SJ, 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.
45. Lloyd D, Ralphs JR, Harris JC. 2002. Giardia intestinalis, a eukaryote without hydrogenosomes, produces hydrogen. Microbiology 148: 727-733.
46. Loxdale HD, Hardie J, Halbert S, Foottit R, Kidd NAC, Carter CI. 1993. The relative importance of short- and long-range movement of flying aphids. Biological Reviews 68: 291-311.
47. Loxdale HD, Lushai G. 2003a. Rapid changes in clonal lineages: the death of a 'sacred cow'. Biological Journal of the Linnean Society 79: 3-16.
48. Loxdale HD, Lushai G. 2003b. Maintenance of aphid clonal lineages: images of immortality. Infection, Genetics and Evolution 3: 259-269.
49. Loxdale HD, Lushai G. 2007. Population genetics issues: the unfolding story revealed using molecular markers. In: van Emden HF, Harrington R, eds. Aphids as crop pests. CABI millennium volume. Oxford: CABI.
50. Loxdale HD, van Dijk PJ, Ricci C. 2005. PARTNER IV-European Science Foundation (ESF) ? Linnean Society joint meeting 'the paradox of asexuality: an evaluation', 22-24 September 2005. Available at: http://www.nioo.knaw.nl/networks/partner/welcome.htm.
51. Lundblad V. 2002. Telomere maintenance without telomerase. Oncogene 21: 522-531.
52. Lushai G, Loxdale HD. 2002. The biological improbability of a clone (mini-review). Genetical Research, Cambridge 79: 1-9.
53. Lushai G, Loxdale HD, Allen JA. 2003a. The dynamic clonal genome and its adaptive potential. Biological Journal of the Linnean Society 79: 193-208.
54. Lushai G, Markovitch O, Loxdale HD. 2002. Host-based genotype variation in insects revisited. Bulletin of Entomological Research 92: 159-164.
55. Lushai G, Smith DAS, Gordon IJ, Goulson D, Allen JA, Maclean N. 2003b. Incomplete sexual isolation in sympatry between subspecies of the butterfly Danaus chrysippus (L.) and the creation of a hybrid zone. Heredity 90: 236-246.
56. Lynch M. 1984. Destabilizing hybridization, general-purpose genotypes and geographic parthenogenesis. Quarterly Review of Biology 59: 257-290.
57. Lynch M, Blanchard JL. 1998. Deleterious mutation accumulation in organelle genomes. Genetica 103: 29-39.
58. Lynch M, Burger R, Butcher D, Gabriel W. 1993. The mutational meltdown in asexual populations. Journal of Heredity 84: 339-344.
59. Lynch M, Latta L, Hicks J, Giorgianni M. 1998. Mutation, selection, and the maintenance of life-history variation in a natural population. Evolution 52: 727-733.
60. Mark-Welch DB, Meselson M. 2000. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288: 1211-1215.
61. Martens K, Rossetti G, Horn DJ. 2003. How ancient are ancient asexuals? Proceedings of the Royal Society London Series B, Biological Sciences 270: 723-729.
62. McEachern MJ, Krauskopf A, Blackburn EH. 2000. Telomeres and their control. Annual Review of Genetics 34: 331-358.
63. Monaghan P, Haussmann MF. 2006. Do telomere dynamics link lifestyle and lifespan? Trends in Ecology and Evolution 21: 47-53.
64. Muller HJ. 1964. The relation of recombination to mutational advance. Mutation Research 1: 2-9.
65. Normark BB. 1999. Evolution in a putatively ancient asexual aphid lineage: recombination and rapid karyotype change. Evolution 53: 1458-1469.
66. Normark BB, Judson O, Moran N. 2003. Genomic signatures of ancient asexual lineages. Biological Journal of the Linnean Society 79: 69-84.
67. Pearson H. 2003. Adult clones in sudden death shock: pig fatalities highlight cloning dangers. Nature (online). Available at: http://www.nature.com/nsu/030825/030825-2.html.
68. Rawes V, Kipling D, Kill IR, Faragher RGA. 1997.The kinetics of senescence in retinal pigmented epithelial cells: a test for the telomerase hypothesis of ageing? Biochemistry ? Moscow 62: 1291-1295.
69. Rudolph KL, Chang S, Lee HW, Blasco M, Gottlieb GJ, Greider C, DePinho RA. 1999. Longevity, stress response and cancer in aging telomerase-deficient mice. Cell 96: 701-712.
70. Sasaki A, Hamilton WD, Ubeda F. 2002. Clone mixtures and a pacemaker: new facets of Red-Queen theory and ecology. Proceedings of the Royal Society of London Series B, Biological Sciences 269: 761-772.
71. Schaetzlein S, Lucas-Hahn A, Lemme E, Kues WA, Dorsch M, Manns MP, Niemann H, Rudolph KL. 2004. Telomere length is reset during early mammalian embryogenesis. Proceedings of the National Academy of Sciences of the United States of America 101: 8034-8038.
72. Schön I, Gandolfi A, Di Masso E, RossiV, Griffiths HI, Martens K, Butlin RK. 2000. Persistence of asexuality through mixed reproduction in Eucypris virens (Crustacea, Ostracoda). Heredity 84: 161-169.
73. Schön I, Martens K. 2000. Transposable elements and asexual reproduction. Trends in Ecology and Evolution 15: 287-288.
74. Sedivy JM. 1998. Can ends justify the means?: Telomeres and the mechanisms of replicative senescence and immortalization in mammalian cells. Proceedings of the National Academy of Sciences of the United States of America 95: 9078-9081.
75. Shibata T. 2001. Functions of homologous DNA recombination. RIKEN Review 41: 21-23. Available at http://www.riken.go.jp/lab- www/library/publication/review/pdf/No_41/41-021.pdf.
76. Shiels PG, Kind AJ, Campbell KHS, Waddington D, Wilmut I, Colman A, Schnieke AE. 1999. Analysis of telomere lengths in cloned sheep. Nature 399: 316-317.
77. Simon J-C, Baumann S, Sunnucks P, Hebert PDN, Pierre JS, Le Gallic JF, Dedryver CA. 1999. Reproductive mode and population genetic structure of the cereal aphid Sitobion avenae studied using phenotypic and microsatellite markers. Molecular Ecology 8: 531-545.
78. 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: 151-163.
79. Simon J-C, Rispe C, Sunnucks P. 2002. Ecology and evolution of sex in aphids. Trends in Ecology and Evolution 17: 34-39.
80. Spence JM, Blackman RL, Testa JM, Ready PD. 1998. A 169-base pair tandem repeat DNA marker for subtelomeric heterochromatic and chromosomal rearrangements in aphids of the Myzus persicae group. Chromosome Research 6: 167-175.
81. Sunnucks P, Chisholm D, Turak E, Hales DF. 1998. Evolution of an ecological trait in parthenogenetic Sitobion aphids. Heredity 81: 638-647.
82. Sunnucks P, De Barro PJ, Lushai G, Maclean N, Hales D. 1997. Genetic structure of an aphid studied using microsatellites: cyclic parthenogenesis differentiated lineages and host specialisation. Molecular Ecology 6: 1059-1073.
83. Sykorova E, Lim KY, Chase MW, Knapp S, Leitch IJ, Leitch AR, Fajkus J. 2003. The absence of Arabidopsis-type telomeres in Cestrum and closely-related genera Vestia and Sessea (Solanaceae): first evidence from eudicots. The Plant Journal 34: 283-291.
84. Van Doninck K, Schön I, De Bruyn L, Martens K. 2002. A general purpose genotype in an ancient asexual. Oecologia 132: 205-212.
85. Ward SA, Leather SR, Pickup J, Harrington R. 1998. Mortality during dispersal and the cost of host specificity in parasites: how many aphids find hosts? Journal of Animal Ecology 67: 763-773.
86. West SA, Lively CM, Read AF. 1999. A pluralist approach to sex and recombination. Journal of Evolutionary Biology 12: 1003-1012.