, Volume 12, Issue 5, pp 387–396

Potential for clonal animals in longevity and ageing studies

Review Article


Ageing is defined as a decline in reproductive and/or somatic performance over time, and as such is experienced by most organisms. Evolutionary theories explain ageing as a consequence of reduced selection pressure against mutations and reduced allocation to somatic maintenance in post-reproductive individuals. In addition, the fecundity of younger age-groups makes a more significant contribution than infinite maintenance of the parental body to the production of subsequent generations. However, in clonal animals, as well as in plants that reproduce by agametic cloning, the adult body is itself a reproductive unit that increases its fitness as a function of genet size. Given the apparent longevity of many such clonal organisms, species undergoing agametic cloning are often assumed to be non-ageing and even potentially immortal. Here, we present a brief overview of ageing in organisms undergoing agametic cloning, focusing on animals and molecular investigation. We discuss molecular and evolutionary aspects of ageing or non-ageing with respect to selection in clonal species. Of particular relevance to the search for potential mechanistic processes behind longevity is the notion that clonal organisms are frequently smaller than their obligate sexual counterparts. In conclusion, we find that while clonal animals also commonly age, evolutionary arguments together with empirical evidence suggest that they are likely to be long-lived and stress resistant at the genet level. However, theoretical modeling continues to predict the possibility of immortality, if the contribution from sexual reproduction is low. Future in-depth study of long-lived clones should present an excellent opportunity to discover novel mechanisms for renewal and long-term somatic maintenance and health.


Colonial Ageing Telomeres Telomerase Cell proliferation Asexual reproduction Rejuvenation Phylogeny Agametic cloning Regression 


  1. Agrawal AF (2006) Evolution of sex: why do organisms shuffle their genotypes? Curr Biol 16:R696–R704PubMedCrossRefGoogle Scholar
  2. Åkesson B, Rice SA (1992) 2 new Dorvillea species (Polychaeta, Dorvilleidae) with obligate asexual reproduction. Zool Scr 21:351–362CrossRefGoogle Scholar
  3. Ally D, Ritland K, Otto SP (2010) Aging in a long-lived clonal tree. PLoS Biol 8:e1000454PubMedCrossRefGoogle Scholar
  4. Alvarado AS (2000) Regeneration in the metazoans: why does it happen? Bioessays 22:578–590CrossRefGoogle Scholar
  5. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  6. Anthony KRN, Svane I (1994) Effects of flow habitat on body size and reproductive patterns in the sea anemone Metridium senile (L.) in the Gullmarsfjord, Sweden. Mar Ecol Prog Ser 113:257–269CrossRefGoogle Scholar
  7. Anthony KRN, Svane I (1995) Effects of substratum instability on locomotion and pedal laceration in Metridium senile (Anthozoa: Actinaria). Mar Ecol Prog Ser 124:171–180CrossRefGoogle Scholar
  8. Ballarin L, Schiavon F, Manni L (2010) Natural apoptosis during the blastogenetic cycle of the colonial ascidian Botryllus schlosseri: a morphological analysis. Zool Sci 27:96–102PubMedCrossRefGoogle Scholar
  9. Barker MF, Scheibling R, Mladenov P (1991) Seasonal changes in population structure of the fissiparousasteroids Allostichaster insignis (Farquhar) and Coscinasterias calamaria (Gray). In: Scalera-Liaci L, Canicatti C (eds) Echinoderm research. AA Balkema, Rotterdam, pp 191–196Google Scholar
  10. Bell G (1984) Measuring the cost of reproduction. II. The correlation structure of the life tables of five freshwater invertebrates. Evolution 38:314–326CrossRefGoogle Scholar
  11. Bell G, Wolfe L (1985) Sexual and asexual reproduction in a natural population of Hydra pseudoligactis. Can J Zool 63:851–856CrossRefGoogle Scholar
  12. Bely AE, Nyberg KG (2009) Evolution of animal regeneration: re-emergence of a field. Trends Ecol Evol 25:161–170PubMedCrossRefGoogle Scholar
  13. Berrill NJ (1935) Studies in tunicate development. IV. Asexual reproduction. Philos Trans R Soc Lond B 225:327–379CrossRefGoogle Scholar
  14. Bishop JDD, Manríquez PH, Hughes RN (2000) Water-borne sperm trigger vitellogenic egg growth in two sessile marine invertebrates. Proc R Soc Lond B 267:1165–1169CrossRefGoogle Scholar
  15. Blackstone NW, Jasker BD (2003) Phylogenetic considerations of clonality, coloniality and mode of germline development in animals. J Exp Zool (Mol Dev Evol) 297B:35–47CrossRefGoogle Scholar
  16. Bollmann FM (2008) The many faces of telomerase: emerging extra telomeric effects. Bioessays 30:728–732PubMedCrossRefGoogle Scholar
  17. Bosch TC (2009) Hydra and the evolution of stem cells. Bioessays 31:478–486PubMedCrossRefGoogle Scholar
  18. Brock MA, Strehler BL (1963) Studies on the comparative physiology of aging. IV. Age and mortality of some marine Cnidaria in the laboratory. J Gerontol 18:23–28PubMedGoogle Scholar
  19. Cui Y, Chen RS, Wong WH (2000) The coevolution of cell senescence and diploid sexual reproduction in unicellular organisms. Proc Natl Acad Sci USA 97:3330–3335PubMedCrossRefGoogle Scholar
  20. de Witte LC, Stöcklin J (2010) Longevity of clonal plants: why it matters and how to measure it. Ann Bot 106:859–870PubMedCrossRefGoogle Scholar
  21. Emson RH, Wilkie IC (1980) Fission and autotomy in echinoderms. Oceanogr Mar Biol Annu Rev 18:155–250Google Scholar
  22. Finch CF (1990) Longevity senescence and the genome. University of Chicago Press, ChicagoGoogle Scholar
  23. Finch CF (2009) Update on slow ageing and negligible senescence—a mini-review. Gerontology 55:307–313PubMedCrossRefGoogle Scholar
  24. Gami MS, Wolkow CA (2006) Studies of Caenorhabditis elegans DAF-2/insulin signaling reveal targets for pharmacological manipulation of lifespan. Aging Cell 5:31–37PubMedCrossRefGoogle Scholar
  25. Gardner SN, Mangel M (1997) When can a clonal organism escape senescence? Am Nat 150:462–490PubMedCrossRefGoogle Scholar
  26. Geller JB, Fitzgerald LJ, King CE (2005) Fission in sea anemones: Integrative studies of life cycle evolution. Integr Comp Biol 45:615–622PubMedCrossRefGoogle Scholar
  27. Hausdorf B, Helmkampf M, Nesnidal MP, Bruchhaus I (2010) Phylogenetic relationships within the lophophorate lineages (Ectoprocta, Brachiopoda and Phoronida). Mol Phylogenet Evol 55:1121–1127PubMedCrossRefGoogle Scholar
  28. Heilbronn LK, Ravussin E (2003) Calorie restriction and aging: review of the literature and implications for studies in humans. Am J Clin Nutr 78:361–369PubMedGoogle Scholar
  29. Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguñà J, Bailly X, Jondelius U, Wiens M, Müller WEG, Seaver E, Wheeler WC, Martindale MQ, Giribet G, Dunn CW (2009) Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc R Soc Lond B 276:4261–4270CrossRefGoogle Scholar
  30. Hernroth B, Farahani F, Brunborg G, Dupont S, Dejmek A, Nilsson Sköld H (2010) Possibility of mixed progenitor cells in sea star arm regeneration. J Exp Zool (Mol Dev Evol) 314B:457–468CrossRefGoogle Scholar
  31. Hsu CY, Chiu YC, Hsu WL, Chan YP (2008) Age-related markers assayed at different developmental stages of the annual fish Nothobranchius rachovii. J Gerontol A Biol Sci Med Sci 63:1267–1276PubMedGoogle Scholar
  32. Hughes RN (2005) Lessons in modularity: the evolutionary ecology of colonial invertebrates. Sci Mar 69:169–179CrossRefGoogle Scholar
  33. Hughes TP, Jackson JBC (1980) Do corals lie about their age? Some demographic consequences of partial mortality, fission and fusion. Science 209:713–715PubMedCrossRefGoogle Scholar
  34. Iwama H, Ohyashiki K, Ohyashiki JH, Hayashi S, Yahata N, Ando K, Toyama K, Hoshika A, Takasaki M, Mori M, Shay JW (1998) Telomeric length and telomerase activity vary with age in peripheral blood cells obtained from normal individuals. Hum Genet 102:397–402PubMedCrossRefGoogle Scholar
  35. Kaltz O, Bell G (2002) The ecology and genetics of fitness in Chlamydomonas. XII. Repeated sexual episodes increase rates of adaptation to novel environments. Evolution 56:1743–1753PubMedGoogle Scholar
  36. Karakashian SJ, Lanners HN, Rudzinska MA (1984) Cellular and clonal aging in the suctorian protozoan Tokophyra infusionum. Mech Age Dev 26:217–229CrossRefGoogle Scholar
  37. Kawamura K, Fujiwara S (1995) Establishment of cell lines from multipotent epithelial sheet in the budding tunicate, Polyandrocarpa misakiensis. Cell Struct Funct 20:97–106PubMedCrossRefGoogle Scholar
  38. Kinugawa C, Murakami T, Okamura K, Yajima A (2000) Telomerase activity in normal ovaries and premature ovarian failure. Tohoku J Exp Med 190:231–238PubMedCrossRefGoogle Scholar
  39. Kirkwood TB, Austad SN (2000) Why do we age? Nature 408:233–238PubMedCrossRefGoogle Scholar
  40. Laird DJ, Weissman IL (2004) Telomerase maintained in self-renewing tissues during serial regeneration of the urochordate Botryllus schlosseri. Dev Biol 273:185–194PubMedCrossRefGoogle Scholar
  41. Laird DJ, De Tomaso AW, Weissman IL (2005) Stem cells are units of natural selection in a colonial ascidian. Cell 123:1351–1360PubMedCrossRefGoogle Scholar
  42. Lauzon RJ, Rinkevich B, Patton CW, Weissman IL (2000) A morphological study of nonrandom senescence in a colonial urochordate. Biol Bull 198:367–378PubMedCrossRefGoogle Scholar
  43. Longo VD, Finch CE (2003) Evolutionary medicine: from dwarf model systems to healthy centenarians? Science 299:1342–1346PubMedCrossRefGoogle Scholar
  44. Martínez DE (1998) Mortality patterns suggest lack of senescence in hydra. Exp Gerontol 33:217–225PubMedCrossRefGoogle Scholar
  45. Martínez DE (2002) Senescence and rejuvenation in asexual metazoans. In: Hughes RN (ed) Reproductive biology of invertebrates. Progress in asexual reproduction, vol XI. Oxford & IBH Publishing, New Delhi, pp 115–140Google Scholar
  46. Martínez DE, Levinton JS (1992) Asexual metazoans undergo senescence. Proc Natl Acad Sci USA 89:9920–9923PubMedCrossRefGoogle Scholar
  47. Medawar PB (1952) An unsolved problem of biology. HK Lewis, London, pp 1–24Google Scholar
  48. Nilsson Sköld H, Obst M, Sköld M, Åkesson B (2009) Stem cells in asexual reproduction of marine invertebrates. In: Rinkevich B, Matranga V (eds) Stem cells in marine organisms. Springer, Berlin, pp 105–138CrossRefGoogle Scholar
  49. Nilsson Sköld H, Asplund ME, Wood CA, Bishop JD (2011a) Telomerase deficiency in a colonial ascidian after prolonged asexual propagation. J Exp Zool (Mol Dev Evol) 314B. doi:10.1002/jez.b.21399
  50. Nilsson Sköld H, Stach T, Herbst E, Bishop J, Thorndyke M (2011b) The pattern of cell proliferation during budding in the colonial ascidian Diplosoma listerianum. Biol Bull (August issue) (in press)Google Scholar
  51. Paps J, Baguna J, Riutort M (2009a) Bilaterian phylogeny: A broad sampling of 13 nuclear genes provides a new Lophotrochozoa phylogeny and supports a paraphyletic basal Acoelomorpha. Mol Biol Evol 26:2397–2406PubMedCrossRefGoogle Scholar
  52. Paps J, Baguna J, Riutort M (2009b) Lophotrochozoa internal phylogeny: new insights from an up-to-date analysis of nuclear ribosomal genes. Proc R Soc Lond B 276:1245–1254Google Scholar
  53. Pick KS, Philippe H, Schreiber F, Erpenbeck D, Jackson DJ, Wrede P, Wiens M, Alie A, Morgenstern B, Manuel M, Worheide G (2010) Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol Biol Evol 27:1983–1987PubMedCrossRefGoogle Scholar
  54. Quyn AJ, Appleton PL, Carey FA, Steele RJC, Barker N, Clevers H, Ridgway RA, Sansom OJ, Näthke IS (2010) Spindle orientation bias in gut epithelial stem cell compartments is lost in precancerous tissue. Cell Stem Cell 6:175–181PubMedCrossRefGoogle Scholar
  55. Rabinowitz C, Rinkevich B (2004) In vitro delayed senescence of extirpated buds from zooids of the colonial tunicate Botryllus schlosseri. J Exp Biol 207:1523–1532PubMedCrossRefGoogle Scholar
  56. Rinkevich B, Avishay N, Rabinowitz C (2005) UV incites diverse levels of DNA breaks in different cellular compartments of a branching coral species. J Exp Biol 208:843–848CrossRefGoogle Scholar
  57. Rodrigues-Grana L, Calliari D, Tiselius P, Hansson B, Nilsson Sköld H (2010) Gender differences and non-mendelian inheritance of oxidative damage in marine copepods. Mar Ecol Prog Ser 401:1–13CrossRefGoogle Scholar
  58. Ryan JF, Pang K, Mullikin JC, Martindale MQ, Baxevanis AD (2010) The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa. Evodevo 1:10PubMedCrossRefGoogle Scholar
  59. Ryland JS, Bishop JDD (1990) Prevalence of cross-fertilization in the hermaphroditic compound ascidian Diplosoma listerianum. Mar Ecol Prog Ser 61:125–132CrossRefGoogle Scholar
  60. Salo E (2006) The power of regeneration and the stem-cell kingdom: freshwater planarians (Platyhelminthes). Bioessays 28:546–559PubMedCrossRefGoogle Scholar
  61. 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. Proc Natl Acad Sci USA 101:8034–8038PubMedCrossRefGoogle Scholar
  62. Schroeder PC, Hermans CO (1975) Annelida: Polychaeta. In: Giese AC, Pearse JS (eds) Reproduction of marine invertebrates, vol III. Academic Press, NewYork, pp 1–213Google Scholar
  63. Seehuus SC, Norberg K, Gimsa U, Krekling T, Amdam GV (2006) Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proc Natl Acad Sci USA 103:962–967PubMedCrossRefGoogle Scholar
  64. Sköld M, Barker MF, Mladenov PV (2002) Spatial variability in sexual and asexual reproduction of the fissiparous seastar Coscinasterias muricata: the role of food and fluctuating temperature. Mar Ecol Prog Ser 233:143–155CrossRefGoogle Scholar
  65. Sköld M, Wing SR, Mladenov PV (2003) Genetic subdivision of a sea star with high dispersal capability in relation to physical barriers in a fjordic seascape. Mar Ecol Prog Ser 250:163–174CrossRefGoogle Scholar
  66. Sohal RS, Weindruch R (1996) Oxidative stress, caloric restriction, and aging. Science 273:59–63PubMedCrossRefGoogle Scholar
  67. Sonneborn TM (1930) Genetic studies on Stenostomum incaudatum. J Exp Zool (Mol Dev Evol) 57:57–108CrossRefGoogle Scholar
  68. Swalla BJ, Cameron CB, Corley LS, Garey JR (2000) Urochordates are monophyletic within the deuterostomes. Syst Biol 49:52–64PubMedCrossRefGoogle Scholar
  69. Tatarenkov A, Bergström L, Jönsson RB, Serrao EA, Kautsky L, Johannesson K (2005) Intriguing asexual life in marginal populations of the brown seaweed Fucus vesiculosus. Mol Ecol 14:647–651PubMedCrossRefGoogle Scholar
  70. Van Valen L (1973) A new evolutionary law. Evol Theory 1:1–30Google Scholar
  71. Voskoboynik A, Reznick AZ, Rinkevich B (2001) Rejuvenescence and extension of an urochordate life span following a single, acute administration of an anti-oxidant, butylated hydroxytoluene. Mech Ageing Dev 123:1203–1210CrossRefGoogle Scholar
  72. Watanabe H, Hoang VT, Mättner R, Holstein TW (2009) Immortality and the base of multicellular life: lessons from cnidarian stem cells. Semin Cell Dev Biol 20:1112–1114CrossRefGoogle Scholar
  73. Weismann A (1889) Essays upon heredity and kindred biological problems, vol 1. Clarendon Press, Oxford, p 28Google Scholar
  74. Williams GC (1957) Pleiotropy, natural selection and the evolution of senescence. Evolution 11:398–411CrossRefGoogle Scholar
  75. Williams GC (1966) Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am Nat 100:687–690CrossRefGoogle Scholar
  76. Wood JG, Rogina B, Lavu S, Howitz K, Helfand SL, Tatar M, Sinclair D (2004) Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature 430:686–689PubMedCrossRefGoogle Scholar
  77. Yoshida K, Fujisawa T, Hwang JS, Ikeo K, Gojobori T (2006) Degeneration after sexual differentiation in hydra and its relevance to the evolution of aging. Gene 385:64–70PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Marine Ecology-KristinebergUniversity of GothenburgFiskebäckskilSweden
  2. 2.Department of Zoology, Systematics and BiodiversityUniversity of GothenburgGothenburgSweden

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