Skip to main content
SpringerLink
Log in

Niche Inheritance: A Possible Basis for Classifying Multiple Inheritance Systems in Evolution

  • Published:
Biological Theory Aims and scope Submit manuscript

Abstract

The theory of niche construction adds a second general inheritance system, ecological inheritance, to evolution (Odling-Smee et al. 2003). Ecological inheritance is the inheritance, via an external environment, of one or more natural selection pressures previously modified by niche-constructing organisms. This addition means descendant organisms inherit genes, and biotically transformed selection pressures in their environments, from their ancestors. The combined inheritance is called niche inheritance. Niche inheritance is used as a basis for classifying the multiple genetic and non-genetic, inheritance systems currently being proposed as possibly significant in evolution (e.g., Jablonka and Lamb 2005). Implications of niche inheritance for the relationship between evolution and development (EvoDevo) are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Amundson R (2005) The Changing Role of the Embryo in Evolutionary Thought. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Balter M (2005) Are humans still evolving? Science 309: 234–237.

    Article  Google Scholar 

  • Bekenstein JD (2003) Information in the holographic universe. Scientific American (August): 59–65.

  • Bergstrom CT, Lachmann M (2004) Shannon information and biological fitness. Information Theory Workshop. IEEE. 50–54.

  • Bird A (2002) DNA methylation patterns and epigenetic memory. Genes and Development 16: 6–21.

    Article  Google Scholar 

  • Bird A (2007) Perceptions of epigenetics. Nature 447: 396–398.

    Article  Google Scholar 

  • Boni MF, Feldman MW (2005) Evolution of antibiotic resistance by human and bacterial niche construction. Evolution 59: 477–491.

    Google Scholar 

  • Boogert NJ, Paterson DM, Laland KN (2006) The implications of niche construction and ecosystem engineering for conservation biology. BioScience 56: 570–578.

    Article  Google Scholar 

  • Borenstein E, Kendal J, Feldman M (2006) Cultural niche construction in a metapopulation. Theoretical Population Biology 14: 92–104.

    Article  Google Scholar 

  • Boyd R, Richerson PJ (1985) Culture and the Evolutionary Process. Chicago: University of Chicago Press.

    Google Scholar 

  • Cavalli-Sforza LL, Feldman MW (1981) Cultural Transmission and Evolution: A Quantitative Approach. Princeton: Princeton University Press.

    Google Scholar 

  • Charmantier A, Sheldon BC (2006) Testing genetic models of mate choice evolution in the wild. Trends in Ecology and Evolution 21: 417–419.

    Article  Google Scholar 

  • Chase JM, Leibold MA (2003) Ecological Niches: Linking Classical and Contemporary Approaches. Chicago: University of Chicago Press.

    Book  Google Scholar 

  • Combes C (2001) Parasitism: The Ecology and Evolution of Intimate Interactions. Chicago: University of Chicago Press.

    Google Scholar 

  • Davidson EH (2006) The Regulatory Genome: Gene Regulatory Networks in Development and Evolution. Amsterdam: Elsevier.

    Google Scholar 

  • Davies NB, Kilner RM, Noble DG (1998) Nestling cuckoos, cuculus canorus, exploit hosts with begging calls that mimic a brood. Proceedings of the Royal Society London B 265: 673–678.

    Article  Google Scholar 

  • Dawkins R (1976) The Selfish Gene. Oxford: Oxford University Press.

    Google Scholar 

  • Dawkins R (1982) The Extended Phenotype. Oxford: Freeman.

    Google Scholar 

  • Dawkins R (2004) Extended phenotype-but not too extended. A reply to Laland, Turner and Jablonka. Biology and Philosophy 19: 377–396.

    Article  Google Scholar 

  • Deacon TW (1997) The Symbolic Species: The Co-evolution of Language and the Brain. New York: Norton.

    Google Scholar 

  • Diamond J (2005) Collapse: How Societies Choose to Fail or Survive. London: Penguin/Allen Lane.

    Google Scholar 

  • Dietrich WE, Taylor Perron J (2006) The search for a topographic signature of life. Nature 439: 411–418.

    Article  Google Scholar 

  • Donohue K (2005) Niche construction through phonological plasticity: Life history dynamics and ecological consequences. New Phytologist 166: 83–92.

    Article  Google Scholar 

  • Durham WH (1991) Coevolution: Genes, Culture and Human Diversity. Stanford, CA: Stanford University Press.

    Google Scholar 

  • Enattah NS, Sahi T, Savilhati E, Terwilliger JD, Peltonen L, Jarvela I (2002) Identification of a variant associated with adult-type hypolactasia. Nature Genetics 30: 233–237.

    Article  Google Scholar 

  • Feldman MW, Cavalli-Sforza LL (1989) On the theory of evolution under genetic and cultural transmission, with application to the lactose absorption problem. In: Mathematical Evolutionary Theory (Feldman MW, ed). Princeton: Princeton University Press.

    Chapter  Google Scholar 

  • Flack JC, Girvan M, de Waal FBM, Krakauer DC (2006) Policing stabilizes construction of social niches in primates. Nature 439: 426–429.

    Article  Google Scholar 

  • Fragaszy DM, Perry S (2003) The Biology of Traditions. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Frederickson ME, Greene MJ, Gordon DM (2005) “Devil’s gardens” bedevilled by ants. Nature 437: 495–496.

    Article  Google Scholar 

  • Fry I (2000) The Emergence of Life on Earth: A Historical and Scientific Overview. New Brunswick, NJ: Rutgers University Press.

    Google Scholar 

  • Futuyma DJ (1998) Evolutionary biology. 3rd ed. Sunderland, MA: Sinauer.

    Google Scholar 

  • Gilbert SF (2001) Ecological developmental biology: Developmental biology meets the real world. Developmental Biology 233: 1–12.

    Article  Google Scholar 

  • Gilbert SF (2004) Mechanisms for the environmental regulation of gene expression. Birth Defects Research (Part C) 72: 291–299.

    Article  Google Scholar 

  • Godfrey-Smith P (1996) Complexity and the Function of Mind in Nature. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Hansell MH (2005) Animal Architecture. Oxford Animal Biology Series. Oxford: Oxford University Press.

    Book  Google Scholar 

  • Hanski I, Singer MC (2001) Extinction-colonization and host-plant choice in butterfly metapopulations. American Naturalist 158: 341–353.

    Article  Google Scholar 

  • Holt RD (2005) On the integration of community ecology and evolutionary biology: Historical perspectives, and current prospects. In: Ecological Paradigms Lost: Routes of Theory Change (Cuddington K, Beisner B, eds), 235–271. New York: Academic Press.

    Chapter  Google Scholar 

  • Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291: 881–884.

    Article  Google Scholar 

  • Hui C, Li Z, Yu D (2004) Metapopulation dynamics and distribution and environmental heterogeneity induced by niche construction. Ecological Modelling 177: 107–118.

    Article  Google Scholar 

  • Ihara Y, Feldman MW (2004) Cultural niche construction and the evolution of small family size. Theoretical Population Biology 65: 105–111.

    Article  Google Scholar 

  • Jablonka E, Lamb MJ (1995) Epigenetic Inheritance and Evolution. Oxford: Oxford University Press.

    Google Scholar 

  • Jablonka E, Lamb MJ (2005) Evolution in Four Dimensions. Cambridge, MA: MIT Press.

    Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69: 373–386.

    Article  Google Scholar 

  • Jones CG, Lawton JH, eds (1995) Linking Species and Ecosystems. New York: Chapman and Hall.

    Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78: 1946–1957.

    Article  Google Scholar 

  • Kirkpatrick M, Lande R (1989) The evolution of maternal characters. Evolution 43: 485–503.

    Article  Google Scholar 

  • Laland KN, Brown GR (2002) Sense and Nonsense: Evolutionary Perspectives on Human Behaviour. Oxford: Oxford University Press.

    Google Scholar 

  • Laland KN, Odling-Smee FJ, Feldman MW (1996) On the evolutionary consequences of niche construction. Journal of Evolutionary Biology 9: 293–316.

    Article  Google Scholar 

  • Laland KN, Odling-Smee FJ, Feldman MW (1999) Evolutionary consequences of niche construction and their implications for ecology. Proceedings of the National Academy of Sciences USA 96: 10242–10247.

    Article  Google Scholar 

  • Laland KN, Odling-Smee FJ, Feldman MW (2000) Niche construction, biological evolution, and cultural change. Behavioral and Brain Sciences 23: 131–175.

    Article  Google Scholar 

  • Laland KN, Odling-Smee FJ, Feldman MW (2001) Cultural niche construction and human evolution. Evolutionary Biology 14: 22–23.

    Article  Google Scholar 

  • Laland KN, Sterelny K (2006) Seven reasons (not) to neglect niche construction. Evolution 60: 1751–1762.

    Article  Google Scholar 

  • Lewontin, RC (1982) Organism and environment. In: Learning, Development and Culture (Plotkin HC, ed), 151–170. New York: Wiley.

    Google Scholar 

  • Lewontin RC (1983) Gene, organism, and environment. In: Evolution from Molecules to Men (Bendall DS, ed), 273–285. Cambridge: Cambridge University Press.

    Google Scholar 

  • Lewontin R (2000) The Triple Helix: Gene, Organism, and Environment. Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124: 837–848.

    Article  Google Scholar 

  • Mameli M (2004) Nongenetic selection and nongenetic inheritance. British Journal for the Philosophy of Science 55: 35–71.

    Article  Google Scholar 

  • Maynard Smith J (2000) The concept of information in biology. Philosophy of Science 67: 177–194.

    Article  Google Scholar 

  • Maynard Smith J, Harper D (2003) Animal Signals. Oxford Series in Ecology and Evolution. Oxford: Oxford University Press.

    Google Scholar 

  • Meysman FJR, Middleburg JJ, Heip CHR (2006) Bioturbation: A fresh look at Darwin’s last idea. Trends in Ecology abd Evolution 21: 688–695.

    Article  Google Scholar 

  • Morgan TH (1919) The Physical Basis of Heredity. Philadelphia: Lippincott.

    Book  Google Scholar 

  • Mousseau TA (2006) Maternal effects. In: Evolutionary Genetics: Concepts and Case Studies (Fox W, Wolf JB, eds), 19–21. Oxford: Oxford University Press.

    Google Scholar 

  • Mousseau TA, Fox CW, eds (1998a) Maternal Effects as Adaptations. Oxford University Press.

  • Mousseau TA, Fox CW (1998b) The adaptive significance of maternal effects: Moms do more than make babies. Trends in Ecology and Evolution 13: 403–406.

    Article  Google Scholar 

  • Odling-Smee FJ (1983) Multiple levels in evolution: An approach to the nature-nurture issue via applied epistemology. In: Animal Models of Human Behaviour (Davey G, ed), 135–158. Chichester: Wiley.

    Google Scholar 

  • Odling-Smee FJ (1988) Niche constructing phenotypes. In: The Role of Behavior in Evolution (Plotkin HC, ed), 73–132. Cambridge, MA: MIT Press.

    Google Scholar 

  • Odling-Smee FJ (2006) How niche construction contributes to human gene-culture coevolution. In: Social Information Transmission and Human Biology (Wells JCK, Strickland S, Laland K, eds), 39–57. Boca Raton, FL: Taylor and Francis.

    Chapter  Google Scholar 

  • Odling-Smee FJ, Laland KN, Feldman MW (1996) Niche construction. American Naturalist 147: 641–648.

    Article  Google Scholar 

  • Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche Construction: The Neglected Process in Evolution. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • O’Neill RV, DeAngelis DL, Waide JB, Allen TFH (1986) A Hierarchical Concept of Ecosystems. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Oyama S, Griffiths PE, Gray RD, eds (2001) Cycles of Contingency: Developmental Systems and Evolution. Cambridge, MA: MIT Press.

    Google Scholar 

  • Pigliucci M, Preston K, eds (2004) Phenotypic Integration: Studying the Ecology and Evolution of Complex Phenotypes. Oxford: Oxford University Press.

    Google Scholar 

  • Reader SM, Laland KN (2003) Animal Innovation. Oxford: Oxford University Press.

    Book  Google Scholar 

  • Reik W (2007) Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447: 425–432.

    Article  Google Scholar 

  • Richerson PJ, Boyd R (2005) Not By Genes Alone: How Culture Transformed Human Evolution. Chicago: University of Chicago Press.

    Google Scholar 

  • Sapp J (1987) Beyond the Gene: Cytoplasmic Inheritance and the Struggle for Authority in Genetics. New York: Oxford University Press.

    Google Scholar 

  • Schlichting CD, Pigliucci M (1998) Phenotypic Evolution: A Reaction Norm Perspective. Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • Schwilk DW (2003) Flammability is a niche construction trait: Canopy architecture affects fire intensity. American Naturalist 162: 725–733.

    Article  Google Scholar 

  • Silver M, Di Paolo E (2006) Spatial effects favour the evolution of niche construction. Theoretical Population Biology 70: 387–400.

    Article  Google Scholar 

  • Smith BD (2007) The ultimate ecosystem engineers. Science 315: 1797–1798.

    Article  Google Scholar 

  • Stappenbeck TS, Hooper LV, Gordon JI (2002) Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proceedings of the National Academy of Sciences USA 99: 15451–15455.

    Article  Google Scholar 

  • Sterelny K (2001) Niche construction, developmental systems, and the extended replicator. In: Cycles of Contingency: Developmental Systems and Evolution (Oyama S, Griffiths PE, Gray RD, eds), 333–349. Cambridge, MA: MIT Press.

    Google Scholar 

  • Sterelny K (2003) Thought in a Hostile World: The Evolution of Human Cognition. Oxford: Blackwell.

    Google Scholar 

  • Sterelny K (2005) Made by each other: Organisms and their environment. Biology and Philosophy 20: 21–36.

    Article  Google Scholar 

  • Tomasello M, Carpenter M, Call J, Behne T, Moll H (2005) Understanding and sharing intentions: The origins of cultural cognition. Behavioral and Brain Sciences 28: 675–735.

    Google Scholar 

  • Thompson JN (1994) The Coevolutionary Process. Chicago: University of Chicago Press.

    Book  Google Scholar 

  • Turner JS (2000) The Extended Organism: The Physiology of Animal-built Structures. Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Waddington CH (1969) Paradigm for an evolutionary process. In: Towards a Theoretical Biology (Waddington CH, ed), Vol. 2: Sketches, 106–128. Edinburgh: Edinburgh University Press.

    Google Scholar 

  • Weaver CG, Cervoni N, Champagne FA, D’Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meany MJ (2004) Epigenetic programming by maternal behavior. Nature Neuroscience 7: 847–854.

    Article  Google Scholar 

  • West-Eberhard MJ (2003) Developmental Plasticity and Evolution. Oxford: Oxford University Press.

    Google Scholar 

  • Williams GC (1992) Gaia, nature worship, and biocentric fallacies. Quarterly Review of Biology 67: 479–486.

    Article  Google Scholar 

  • Wilson EO (1975) Sociobiology: The New synthesis. Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Wolf JB (2000) Indirect genetic effects and gene interactions. In: Epistasis and the Evolutionary Process (Wolf JB, Brodie III, ED, Wade MJ, eds), 158–176. Oxford: Oxford University Press.

    Google Scholar 

  • Wright JP, Jones CG (2006) The concept of organisms as ecosystem engineers ten years on: Progress, limitations and challenges. BioScience 3: 203–209.

    Article  Google Scholar 

  • Xu J, Gordon JI (2003) Honor thy symbionts. Proceedings of the National Academy of Sciences USA 100: 10452–10459.

    Article  Google Scholar 

  • Zahavi A (1975) Mate selection: A selection for handicap. Journal of Theoretical Biology 53: 205–214.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Anthropology, University of Oxford, UK

    John Odling-Smee

Authors
  1. John Odling-Smee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John Odling-Smee.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Odling-Smee, J. Niche Inheritance: A Possible Basis for Classifying Multiple Inheritance Systems in Evolution. Biol Theory 2, 276–289 (2007). https://doi.org/10.1162/biot.2007.2.3.276

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1162/biot.2007.2.3.276

Keywords

Search

Navigation