Advertisement

Theory in Biosciences

, Volume 129, Issue 2–3, pp 125–133 | Cite as

Saltational symbiosis

  • Jan SappEmail author
Original Paper
First Online:

Abstract

Symbiosis has long been associated with saltational evolutionary change in contradistinction to gradual Darwinian evolution based on gene mutations and recombination between individuals of a species, as well as with super-organismal views of the individual in contrast to the classical one-genome: one organism conception. Though they have often been dismissed, and overshadowed by Darwinian theory, suggestions that symbiosis and lateral gene transfer are fundamental mechanisms of evolutionary innovation are borne out today by molecular phylogenetic research. It is time to treat these processes as central principles of evolution.

Keywords

Evolution Symbiosis Saltationism Lamarckism Darwinism Superorganism Horizontal gene transfer 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

I am grateful to Nathalie Gontier and the reviewers for their helpful comments on an earlier version of this paper. I also thank the Social Science and Humantities Research Council of Canada for support of my work.

References

  1. Allee WC, Emerson AE, Park O, Park T, Schmidt KP (1949) Principles of animal ecology. WB Saunders, PhiladelphiaGoogle Scholar
  2. Allsopp A (1969) Phylogenetic relationships of the procaryota and the origin of the eucaryotic cell. New Phytol 68:591–612CrossRefGoogle Scholar
  3. Bateson W (1913) Problems of genetics. Yale University Press, New HavenGoogle Scholar
  4. Bernard N (1902) Études sur la tubérisation. Rev Gen Bot 14:5–25Google Scholar
  5. Bernard N (1909) Remarques sur l’immunité chez les plantes. Bull Inst Pasteur 12:369–386Google Scholar
  6. Buchanan M (2009) Collectivist revolution in evolution. Nature Physics 5:531CrossRefGoogle Scholar
  7. Buchner P (1965) Endosymbiosis of animals with plant microorganisms (trans: Mueller B). Interscience Publishers, New YorkGoogle Scholar
  8. Burnet FM (1933) Recent work on the biological nature of bacteriophages. Trans R Soc Trop Med Hyg 26:409–416CrossRefGoogle Scholar
  9. Caullery M (1952) Parasitism and symbiosis (trans: Averilm Lysaght). Sidgwick and Jackson, LondonGoogle Scholar
  10. D’ Herelle F (1926) The bacteriophage and its behavior (trans: Smith GH). Williams and Wilkins, BaltimoreGoogle Scholar
  11. D’Herelle F (1931) Bacterial mutations. YJBM 4:55–57Google Scholar
  12. Darwin C (1859) On the origin of species, with an introduction by Ernst Mayr, facsimile edition of 1859. Harvard University Press, Cambridge 1964Google Scholar
  13. Daubin V, Ochman H (2004) Start-up entities in the origin of new genes. Curr Opin Genet Dev 6:616–619CrossRefGoogle Scholar
  14. De Bary A (1879) Die Erscheinung der Symbiose, Vortrag auf der Versammlung der Naturforsher und Aertze zu Cassel. Verlag von Karl J. Trubner, Strassburg, pp. 1–30, 21–22Google Scholar
  15. De Bary A (1887) Comparative morphology and biology of the fungi mycetozoa and bacteria (trans: Garnsey HEF, revised: Balfour IB). The Clarendon Press, OxfordGoogle Scholar
  16. Dennett D, Coyne J, Dawkins R (2009) Darwin was right. New Sci 201:24CrossRefGoogle Scholar
  17. Dubos R (1961) Integrative and creative aspects of infection. In: Pollard M (ed) Perspectives in virology, vol 2. Burgess Publishing, Minneapolis, pp 200–205Google Scholar
  18. East EM (1934) The nucleus-plasma problem, Am Nat 68:289–303, 402–439Google Scholar
  19. Gladyshev EA, Meselson M, Arkhipoval IR (2008) Massive horizontal gene transfer in bdelloid rotifers. Science 320:1210–1213CrossRefPubMedGoogle Scholar
  20. Gogarten P, Doolittle WF, Lawrence JG (2002) Prokaryotic evolution in light of gene transfer, molecular biology and evolution 19:2226–2238Google Scholar
  21. Goksøyr J (1967) Evolution of eucaryotic cells. Nature 214:1167CrossRefGoogle Scholar
  22. Goldenfeld N, Woese C (2007) Biology’s next revolution. Nature 445:369CrossRefPubMedGoogle Scholar
  23. Gould SJ (1977) Ontogeny and phylogeny. Harvard University Press, Cambridge, MAGoogle Scholar
  24. Gray MW, Doolittle WF (1982) Has the endosymbiont hypothesis been proven? Micro Rev 46:1–42Google Scholar
  25. Gregory FG (1951) A discussion on symbiosis involving micro-organisms—general discussion. Proc R Soc Lond B 139:202–203CrossRefGoogle Scholar
  26. Griffith F (1928) The significance of pneumococcal types. J Hygiene 27:113–159CrossRefGoogle Scholar
  27. Hambly E, Suttle CA (2005) The viriosphere, diversity, and genetic exchange within phage communities. Curr Opin Microbiol 8:444–450CrossRefPubMedGoogle Scholar
  28. Hartman H, Fedorov A (2002) The origin of the eukaryotic cell: a genomic investigation. PNAS 99:1420–1425CrossRefPubMedGoogle Scholar
  29. Hayes W (1952) Recombination in Bact coli K-12: unidirectional transfer of genetic material. Nature 159:118–119CrossRefGoogle Scholar
  30. Hayes W (1953) Observations on a transmissible agent determining sexual differentiation in Bact coli. J Gen Micro 8:72–88Google Scholar
  31. Hendrix RW, Lawrence JG, Hatfull GF, Casjens S (2000) The origins and ongoing evolution of viruses. Trends Microbiol 8:504–507CrossRefPubMedGoogle Scholar
  32. Hotopp JCD et al (2007) Widespread horizontal gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317:1753–1756CrossRefPubMedGoogle Scholar
  33. Huxley J (1942) Evolution: the modern synthesis. Allen and Unwin, LondonGoogle Scholar
  34. Jain R, Rivera MC, Lake JA (1999) Lateral gene transfer among genomes: the complexity hypothesis. PNAS USA 96:3801–3806CrossRefPubMedGoogle Scholar
  35. Kropotkin P (1915) Mutual aid: a factor of evolution. William Heinemann, LondonGoogle Scholar
  36. Kurland CG (2005) Paradigm lost. In: Sapp J (ed) Microbial phylogeny and evolution. Oxford University Press, New York, pp 207–223Google Scholar
  37. Lawrence JG, Ochman H (1998) Molecular archaeology of the Escherichia coli genome. PNAS USA 95:9413–9417CrossRefPubMedGoogle Scholar
  38. Lawton G (2009) Uprooting Darwin’s tree. New Scientist 201:34–39CrossRefGoogle Scholar
  39. Lederberg J (1952) Cell genetics and hereditary symbiosis. Phys Rev 32:403–430Google Scholar
  40. Lederberg J, Tatum E (1946) Gene recombination in Escherichia coli. Nature 158:558CrossRefGoogle Scholar
  41. Limoges C (1994) Milne-Edwards, Darwin, Durkheim and division of labor: a case study in reciprocal conceptual exchanges between the social and natural sciences. In: Cohen IB (ed) The relations between the natural sciences and the social sciences. Princeton University Press, Princeton, pp 317–343Google Scholar
  42. Lin GG, Li JM (2009) Sequence identity between the genomes of humans and viruses. Intervirology 52:196–200CrossRefPubMedGoogle Scholar
  43. Löwer R, Löwer J, Kurth R (1999) The viruses in all of us: characteristics and biological significance of human endogenous retrovirus sequences. PNAS 93:5177–5184CrossRefGoogle Scholar
  44. Maynard Smith J, Szathmáry E (1999) The origins of life. From the birth of life to the origin of language. Oxford University Press, New YorkGoogle Scholar
  45. Mérejkovsky C (1920) La Plante considére comme un complexe symbiotique. Bulletin de la Société Naturelles 6:17–98Google Scholar
  46. Merezhkowsky C (1910) Theorie der zwei Plasmaarten als Grundlage der Symbiogenese, einer neuen Lehre von der Entstehung der Organismen. Biol Zent Bl 30: 277–303; 321–347; 353–367Google Scholar
  47. Meyer KF (1925) The `bacterial symbiosis’ in the concretion deposits of certain operculate land mollusks of the families Cyclostomatidae and Annularidea. J Infect Dis 36:1–107Google Scholar
  48. Nardon P, Grenier A-M (1991) Serial endosymbiosis theory and weevil evolution: the role of symbiosis. In: Margulis M, Fester R (eds) Symbiosis as a source of evolutionary innovation. The MIT Press, Cambridge, pp 153–169Google Scholar
  49. Nikoh N, Tanaka K, Shibata F, Kondo N, Hizume M, Shimada M, Fukatsu T (2008) Wolbachia genome integrated in an insect chromosome: evolution and fate of horizontally transferred endosymbiont genes. Genome Res 18:272–280CrossRefPubMedGoogle Scholar
  50. Odum EP (1959) Fundamentals of ecology. WB Saunders, PhiladephliaGoogle Scholar
  51. Portier P (1918) Les symbiotes. Masson, ParisGoogle Scholar
  52. Raff RA, Mahler HR (1972) The non symbiotic origin of mitochondria. Science 177:575–582CrossRefPubMedGoogle Scholar
  53. Raven P (1970) A multiple origin for plastids and mitochondria. Science 169:641–646CrossRefPubMedGoogle Scholar
  54. Reinheimer H (1915) Symbiogenesis: the universal law of progressive evolution. Knapp, Drewett and Sons, WestministerGoogle Scholar
  55. Ryan F (2007) Viruses as symbionts. Symbiosis 44:11–21Google Scholar
  56. Sagan L (1967) On the origin of mitosing cells. J Theor Biol 14:225–274CrossRefGoogle Scholar
  57. Sapp J (1987) Beyond the gene: cytoplasmic inheritance and the struggle for authority in the field of heredity. Oxford University Press, New YorkGoogle Scholar
  58. Sapp J (1994) Evolution by association: a history of symbiosis. Oxford University Press, New YorkGoogle Scholar
  59. Sapp J (1998) Freewheeling centrioles. Hist Phil Life Sci 20:255–290Google Scholar
  60. Sapp J (2002) Paul Buchner and hereditary symbiosis in insects. Intl Micro 5:145–160CrossRefGoogle Scholar
  61. Sapp J (2006) Mitochondria and their host: morphology to molecular phylogeny. In: Martin W, Müller M (eds) Mitochondria and hydrogenosomes. Springer Verlag, Heidelberg, pp 57–84Google Scholar
  62. Sapp J (2009) The new foundations of evolution. On the tree of life. Oxford University Press, New YorkGoogle Scholar
  63. Sapp J, Carrapiço F, Zolotonosov M (2002) Symbiogenesis: the hidden face of Constantin Merezhkowsky. Hist Phil Life Sci 24(2002):413–440CrossRefGoogle Scholar
  64. Schimper AFW (1883) Ueber die Entwicklung der Schlorophyllkörner und Farbkörper. Bot Zeitung 4:105–114Google Scholar
  65. Spencer H (1899) The principles of biology, vol 2. Appelton and Co, New YorkGoogle Scholar
  66. Stanier RY (1970) Some aspects of the biology of cells and their possible evolutionary significance. In: Charles HP, Knight BC (eds) Organization and control in prokaryotic cells. Twentieth symposium of the society for general microbiology. Cambridge University Press, Cambridge, pp 1–38Google Scholar
  67. Taylor FJR (1986) An overview of the status of evolutionary cell symbiosis theories. Ann NY Acad Sci 503:1–16CrossRefGoogle Scholar
  68. Uzzel T, Spolsky C (1974) Mitochondria and plastids as endosymbionts: a revival of special creation? Am Sci 62:334–343Google Scholar
  69. van Beneden PJ (1873) Un mot sur la vie sociale des animaux inferieurs. Bull Acad Roy Belg, série 2(36):779–796Google Scholar
  70. van Beneden PJ (1876) Animal parasites and messmates. Henry S King, LondonGoogle Scholar
  71. Wallin IE (1927) Symbionticism and the origin of species. William and Wilkins, BaltimoreGoogle Scholar
  72. Watasé S (1893) On the nature of cell organization. Biol lect deliv Mar Biol Lab, Wood’s Hole, pp 83–103Google Scholar
  73. Werren JH (2005) Heritable microorganisms and reproductive parasitism. In: Sapp J (ed) Microbial evolution and phylogeny: concepts and controversies. Oxford University Press, New York, pp 290–316Google Scholar
  74. Wilson EB (1925) The cell in development and heredity. Macmillan, New YorkGoogle Scholar
  75. Woese CR (2000) Interpreting the universal phylogenetic tree. PNAS USA 97:8392–8396CrossRefPubMedGoogle Scholar
  76. Woese CR (2002) On the evolution of cells. PNAS USA 99:8742–8747CrossRefPubMedGoogle Scholar
  77. Woese CR, Kandler O, Wheelis M (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. PNAS USA 87:4576–4579CrossRefPubMedGoogle Scholar
  78. Woolhouse WH (1967) A review of the plastids by JTO Kirk and RAE Tilney-Bassett. New Phytol 66:832–833Google Scholar
  79. Zinder N, Lederberg J (1952) Genetic exchange in Salmonella. J Bact 64:679–699CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Department of Biology, Faculty of Science and EngineeringYork UniversityTorontoCanada

Personalised recommendations

Cite article

Buy options