History and Philosophy of the Life Sciences

, Volume 37, Issue 4, pp 430–448 | Cite as

Extended inheritance from an organizational point of view

  • Gaëlle PontarottiEmail author
Original Paper


In this paper, I argue that the increasing data about non-genetic inheritance requires the construction of a new conceptual framework that should complement the inclusive approaches already discussed in the literature. More precisely, I hold that this framework should be epistemologically relevant for evolutionary biologists in capturing the limits of extended inheritance and in reassessing the boundaries of biological systems that transmit traits to their offspring. I outline the first elements of an organizational account of extended inheritance. In this account, the category of inherited factors is neither restricted to genes nor extended to stable resources related to trans-generational similarities. Instead, it includes persisting constitutive elements appearing as difference makers for heterogeneous organizational constraints, namely for heterogeneous constitutive parts whose specific role is to harness flows of matter and energy across generations of clearly delimited extended organized systems. This both inclusive and restrictive framework opens an additional way to apprehend how extended inheritance may affect evolutionary trajectories.


Extended inheritance Stable resources Extended organization Persisting organizational constraints 



I wish to thank Jean Gayon, Michel Morange, Matteo Mossio, Andrew Mac Farland, James Di Frisco and two anonymous reviewers, whose comments enabled to greatly improve earlier versions of the manuscript. I also thank IHPST and Université Paris 1 Panthéon Sorbonne.


  1. Aiello, L., & Wheeler, P. (1995). The expensive-tissue hypothesis: The brain and the digestive system in human and primate evolution. Current Anthropology, 6(2), 199–221.CrossRefGoogle Scholar
  2. Aizawa, K., & Adams, F. (2009). Why the mind is still in the head. In P. Robbins & M. Aydede (Eds.), The Cambridge handbook of situated cognition (pp. 78–95). Cambridge: Cambridge University Press.Google Scholar
  3. Bonduriansky, R. (2012). Rethinking heredity, again. Trends in Ecology & Evolution, 27(6), 330–336.CrossRefGoogle Scholar
  4. Bonduriansky, R., & Day, T. (2009). Nongenetic inheritance and its evolutionary implications. Annual Review of Ecology Evolution and Systematics, 40, 103–112.CrossRefGoogle Scholar
  5. Bossdorf, O., Richards, C., & Pigliucci, M. (2008). Epigenetics for ecologists. Ecology Letters, 11(2), 106–115.Google Scholar
  6. Boyd, R., & Richerson, P. J. (2005). The origin and evolution of cultures. Oxford : Oxford University Press.Google Scholar
  7. Chiu, L., & Gilbert, S. F. (2015). The birth of the holobiont: Multi-species birthing through mutual scaffolding and niche construction. Biosemiotics, 8(2), 191–210.CrossRefGoogle Scholar
  8. Danchin, E., et al. (2011). Beyond DNA: Integrating inclusive inheritance into an extended theory of evolution. Nature Review Genetics, 12(7), 475–486.CrossRefGoogle Scholar
  9. Darwin, C. (1882). Rôle des vers de terre dans la formation de la terre végétale, Paris. Hachette Livre, BnF.
  10. Dedeine, F., et al. (2001). Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proceedings in National Academic Sciences, 98(11), 6247–6252.CrossRefGoogle Scholar
  11. Feldman, M., & Laland, K. (1996). Gene-culture coevolutionary theory. Trends in Ecology & Evolution, 11(11), 453–457.CrossRefGoogle Scholar
  12. Galef, B., & Laland, K. (2005). Social learning in animals: Empirical studies and theoretical models. BioScience, 55(6), 489–499.CrossRefGoogle Scholar
  13. Gayon, J. (2000). From measurement to organization: A philosophical scheme for the history of the concept of heredity. In P. Beurton, R. Falk, & H. J. Rheinberger (Eds.), Concept of the gene in development and evolution: Historical and epistemological perspectives (pp. 69–90). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  14. Gilbert, S., Sapp, J., & Tauber, A. (2012). A symbiotic view of life: We have never been individuals. Quarterly Review of Biology, 87(4), 325–341.CrossRefGoogle Scholar
  15. Gould, S. J. (1980). Sociobiology and the theory of natural selection. In G. W. Barlow & J. Silverberg (Eds.), Sociobiology: Beyond nature/nurture? (pp. 257–269). Boulder: Westview Press Inc.Google Scholar
  16. Gould, S. J., & Lewontin, R. (1979). The spandrels of san marco and the panglossian paradigm: A critique of the adaptationist programme. Proceedings of the Royal Society of London, B205, 581–598.CrossRefGoogle Scholar
  17. Griesemer, J. (2000). Development, culture, and the units of inheritance. In Philosophy of science, supplement: Proceedings of the 1998 biennial meetings of the philosophy of science association (pp. S348–S368).Google Scholar
  18. Griffiths, P. (2001). Genetic information: A metaphor in search of a theory. Philosophy of Science, 68(3), 394–412.CrossRefGoogle Scholar
  19. Griffiths, P. E., & Gray, R. (1994). Developmental systems and evolutionary explanation. Journal of Philosophy, 91(6), 277–304 (Cited in Hull, D., & Ruse, M. (Eds.). 1998. The Philosophy of Biology. 117–145).Google Scholar
  20. Griffiths, P., & Gray, R. (1997). Replicator II: Judgment day. Biology and Philosophy, 12(4), 471–492.CrossRefGoogle Scholar
  21. Griffiths, P., & Gray, R. (2004). The developmental systems perspective: Organism-environment systems as units of evolution. In K. Preston & M. Pigliucci (Eds.), Phenotypic integration: Studying the ecology and evolution of complex phenotypes (pp. 409–431). Oxford and New York: Oxford University Press.Google Scholar
  22. Griffiths, P., & Stotz, K. (2013). Genetics and philosophy: An introduction. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  23. Hansen, A., & Moran, N. (2011). Aphid genome expression reveals host–symbiont cooperation in the production of amino acids. Proceedings in National Academic Sciences, USA, 108, 2849–2854.CrossRefGoogle Scholar
  24. Helantera, H., & Uller, T. (2010). The price equation and extended inheritance. Philosophy and Theory in Biology, 2, 1–17.CrossRefGoogle Scholar
  25. Hoffmann, A. A., & Turelli, M. (1997). Cytoplasmic incompatibility in insects. In S. L. O’Neill, A. A. Hoffmann, & J. H. Werren (Eds.), Influential passengers (pp. 42–80). Oxford: Oxford University Press.Google Scholar
  26. Hooper, L., et al. (2012). Interactions between the microbiota and the immune system. Science, 336, 1268–1273.CrossRefGoogle Scholar
  27. Hull, D. (1980). Individuality and selection. Annual Review of Ecology and Systematics, 11, 311–332.CrossRefGoogle Scholar
  28. Huneman, P. (2013). Causal parity and externalisms: Extensions in life and mind. Minds and Machines, 23(3), 377–404.CrossRefGoogle Scholar
  29. Jablonka, E. (2002). Information: Its interprétation, it’s inheritance and its sharing. Philosophy of Science, 69, 578–605.CrossRefGoogle Scholar
  30. Jablonka, E., & Lamb, M. (2005). Evolution in four dimensions. Cambridge: MIT Press.Google Scholar
  31. Jacob, F. (1970). La logique du vivant, une histoire de l’hérédité (p. 9). Paris: Gallimard.Google Scholar
  32. Kamra, D. N. (2005). Rumen microbial ecosystem. Current Science, 89(1), 124–135.Google Scholar
  33. Kant, E. (1993). [1790], Critique de la faculté de juger (pp. 294–303). Paris: Vrin.Google Scholar
  34. Laland, K., Odling-Smee, J., & Feldman, M. (1999). Evolutionary consequences of niche construction and their implications for ecology. Proceedings in National Academic Sciences USA, 96, 10242–10247.CrossRefGoogle Scholar
  35. Laland, K., Odling-Smee, J., & Feldman, M. (2000). Niche construction, biological evolution, and cultural change. Behavioural and brain sciences, 23, 131–175.CrossRefGoogle Scholar
  36. Lewontin, R. (1970). Units of selection. Annual Review of Ecology and Systematics, 1, 1–18.CrossRefGoogle Scholar
  37. Lewontin, R. (1983). Gene, organism, and environment. Cambridge: Cambridge University Press.Google Scholar
  38. Mameli, M. (2004). Non genetic selection and non genetic inheritance. British Journal for the Philosophy of Science, 55(1), 35–75.CrossRefGoogle Scholar
  39. Mameli, M. (2005). The inheritance of features. Biology and Philosophy, 20(2–3), 365–399.CrossRefGoogle Scholar
  40. Margulis, L., & Sagan, D. (2001). The beast with five genomes. Natural History, 110(5), 38–41.Google Scholar
  41. McFall-Ngai, M. J. (2002). Unseen forces: The influence of bacteria on animal development. Developmental Biology, 242(1), 1–14.CrossRefGoogle Scholar
  42. Mesoudi, A., et al. (2013). Is non-genetic inheritance just a proximate mechanism? A corroboration of the extended evolutionary synthesis. Biological Theory, 7, 189–195.CrossRefGoogle Scholar
  43. Moreno A. (2014). On the origin of autonomy: from chemical to biological organization. In Oral presentation at the workshop boundaries and levels of biological systems.Google Scholar
  44. Mossio, M., & Moreno, A. (2010). Organisational closure in biological organisms. History and Philosophy of the Life Sciences, 32(2–3), 269–288.Google Scholar
  45. Mossio, M., Saborido, C., & Moreno, A. (2009). An organizational account of biological functions. British Journal for the Philosophy of Science, 60(4), 813–841.CrossRefGoogle Scholar
  46. Newman, S. A., & Muller, G. B. (2000). Epigenetic mechanisms of character origination. Journal of Experimental Zoology, 288(4), 304–317.CrossRefGoogle Scholar
  47. Nyholm, S. V., & Mc Fall-Ngai, M. J. (2004). The winnowing: Establishing the squid-vibrio symbiosis. Nature Review Microbiology, 2, 632–642.CrossRefGoogle Scholar
  48. Odling-Smee, J. (2010). Niche inheritance. In M. Pigliucci & G. B. Muller (Eds.), Evolution, the extended synthesis (pp. 175–207). Cambridge: MIT Press.CrossRefGoogle Scholar
  49. Odling-Smee, J., Laland, K., & Feldman, M. (2003). Niche construction: The neglected process in evolution. Princeton: Princeton University Press.Google Scholar
  50. Okasha, S. (2006). Evolution and the levels of selection. Oxford: Oxford University Press.CrossRefGoogle Scholar
  51. Oyama, S. (2000a). Evolution’s eye: A systems view of the biology-culture divide (pp. 77–95). Durham: Duke University Press.CrossRefGoogle Scholar
  52. Oyama, S. (2000b). Causal democracy and causal contributions in developmental system theory. Philosophy of Science, 67, S332–S347.CrossRefGoogle Scholar
  53. Pocheville, A. (2010). La niche ecologique, concepts, modèles, applications. PhD Thesis, Paris.
  54. Richards, C., Bossdorf, O., & Pigliucci, M. (2010). What role does heritable epigenetic variation play in phenotypic evolution? BioScience, 60(3), 232–237.CrossRefGoogle Scholar
  55. Rosenberg, E., & Zilber-Rosenberg, I. (2008). From bacterial bleaching to the hologenome theory of evolution. In Proceedings of the 11th international coral reef symposium (pp. 273–278). Ft Lauderale, Florida.Google Scholar
  56. Rosenberg, E., & Zilber-Rosenberg, I. (2011). Symbiosis and development: The hologenome concept. Birth Defects Research (Part C), 93, 56–66.CrossRefGoogle Scholar
  57. Rosenberg, E., et al. (2007). The role of microorganims in coral health, disease and evolution. Nature Reviews Microbiology, 5, 355–362.CrossRefGoogle Scholar
  58. Shea, N. (2007). Representation in the genome and in other inheritance systems. Biology and Philosophy, 22, 313–331.CrossRefGoogle Scholar
  59. Slatkin, M. (2009). Epigenetic inheritance and the missing heritability problem. Genetics, 182(3), 845–850.CrossRefGoogle Scholar
  60. Sober, E. (1984). The nature of selection: Evolutionary theory in philosophical focus. Chigaco: University of Chicago Press.Google Scholar
  61. Sterelny, K. (2001). Niche construction, developmental systems and the extended replicator. In S. Oyama, P. Griffiths, & R. Gray (Eds.), Cycles of contingency: Developmental systems and evolution (pp. 333–349). Cambridge: MIT Press.Google Scholar
  62. Sterelny, K., Smith, K., & Dickinson, M. (1996). The extended replicator. Biology and Philosophy, 11(3), 377–403.CrossRefGoogle Scholar
  63. Stotz, K. (2008). The ingredients for a postgenomic synthesis of nature and nurture. Philosophical Psychology, 21(3), 359–381.CrossRefGoogle Scholar
  64. Stotz, K. (2010). Human nature and cognitive-developmental niche construction. Phenomenology and the Cognitive Sciences, 9, 483–501.CrossRefGoogle Scholar
  65. Szathmary, E., & Maynard-Smith, J. (1995). The major evolutionary transitions. Nature, 374(6519), 227–232.CrossRefGoogle Scholar
  66. Teixeira, L., et al. (2008). The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biology, 6(12), 2753–2763.CrossRefGoogle Scholar
  67. Turelli, M., & Hoffmann, A. A. (1991). Rapid spread of an inherited incompatibility factor in California Drosophila. Nature, 353(6343), 440–442.CrossRefGoogle Scholar
  68. Turner, J. S. (2004). Extended phenotypes and extended organisms. Biology and Philosophy, 19(3), 327–352.CrossRefGoogle Scholar
  69. West, M. J., & King, A. P. (1987). Settling nature and nurture into an ontogenetic niche. Developmental Psychobiology, 20(5), 549–562.CrossRefGoogle Scholar
  70. Wilson, D. S. (1997). Biological communities as Functionally Organized Units. Ecology, 78(7), 2018–2024.CrossRefGoogle Scholar
  71. Wilson, D. S., & Sober, E. (1989). Reviving the superorganism. Journal of Theoretical Biology, 136(3), 337–356.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2015

Authors and Affiliations

  1. 1.IHPSTUniversité Paris 1 Panthéon SorbonneParisFrance

Personalised recommendations