Biology & Philosophy

, Volume 24, Issue 5, pp 623–644 | Cite as

The theory of increasing autonomy in evolution: a proposal for understanding macroevolutionary innovations

Article

Abstract

Attempts to explain the origin of macroevolutionary innovations have been only partially successful. Here it is proposed that the patterns of major evolutionary transitions have to be understood first, before it is possible to further analyse the forces behind the process. The hypothesis is that major evolutionary innovations are characterized by an increase in organismal autonomy, in the sense of emancipation from the environment. After a brief overview of the literature on this subject, increasing autonomy is defined as the evolutionary shift in the individual system–environment relationship, such that the direct influences of the environment are gradually reduced and a stabilization of self-referential, intrinsic functions within the system is generated. This is described as relative autonomy because numerous interconnections with the environment and dependencies upon it are retained. Features of increasing autonomy are spatial separations, an increase in homeostatic functions and in body size, internalizations and an increase in physiological and behavioral flexibility. It is described how these features are present in different combinations in the major evolutionary transitions of metazoans and, consequently, how they should be taken into consideration when evolutionary innovations are studied. The hypothesis contributes to a reconsideration of the relationship between organisms and their environment.

Keywords

Trends Biological autonomy Macroevolution Evolutionary innovations Major transitions Robustness Organismic biology 

References

  1. Ahlberg PE, Clark JA (2006) A firm step from water to land. Nature 440:747–749. doi:10.1038/440747a CrossRefGoogle Scholar
  2. Ahlberg PE, Clack JA, Blom H (2005) The axial skeleton of the Devonian tetrapod Ichthyostega. Nature 437:137. doi:10.1038/nature03893 CrossRefGoogle Scholar
  3. Barandiaran X, Ruiz-Mirazo K (2008) Modelling autonomy: simulating the essence of life and cognition. Biosystems 91:295–304. doi:10.1016/j.biosystems.2007.07.001 CrossRefGoogle Scholar
  4. Barker G (2008) Biological levers and extended adapationism. Biol Philos 23:1–25. doi:10.1007/s10539-007-9061-2 CrossRefGoogle Scholar
  5. Bechtel W (2007) Biological mechanisms: organized to maintain autonomy. In: Boogerd F, Bruggeman FJ, Hofmeyr JHS, Westerhoff HV (eds) Systems biology: philosophical foundations. Elsevier, Amsterdam, pp 269–302Google Scholar
  6. Bekoff M, Byers JA (eds) (1998) Animal play. Evolutionary, comparative and ecological perspectives. Cambridge University Press, CambridgeGoogle Scholar
  7. Bennett AF (1991) The evolution of aerobic capacity. J Exp Biol 160:1–23Google Scholar
  8. Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) (1984) Biology of the integument. Springer, BerlinGoogle Scholar
  9. Bernard C (1859) Lecons sur les Propriétés Physiologiques et les Altérations Pathologiques des Liquides de l’Organisme, ParisGoogle Scholar
  10. Bertschinger N, Olbrich E, Ay N, Jost J (2008) Autonomy: an information theoretic perspective. Biosystems 91:331–345. doi:10.1016/j.biosystems.2007.05.018 CrossRefGoogle Scholar
  11. Bonner JT (1988) The evolution of complexity. Princeton University Press, PrincetonGoogle Scholar
  12. Bonner JT (1998) The origins of multicellularity. Integr Biol 1:27–36. doi:10.1002/(SICI)1520-6602(1998)1:1<27::AID-INBI4>3.0.CO;2-6 CrossRefGoogle Scholar
  13. Brooks DL, Collier J, Maurer BA, Smith J, Wiley EO (1989) Entropy and information in evolving biological systems. Biol Philos 4:407–432. doi:10.1007/BF00162588 CrossRefGoogle Scholar
  14. Bullock TH (1993) How are more complex brains different? Brain Behav Evol 41:88–96. doi:10.1159/000113826 CrossRefGoogle Scholar
  15. Bullock TH (1995) Are the main grades of brains different principally in numbers of connections or also in quality? In: Breidbach O, Kutsch W (eds) The nervous systems of invertebrates: an evolutionary and comparative approach. Birkhäuser, Basel, pp 439–448Google Scholar
  16. Butler AB, Hodos W (1996) Comparative vertebrate neuroanatomy. Wiley-Liss, New YorkGoogle Scholar
  17. Byrne RW (1995) The thinking ape. Evolutionary origins of intelligence. Oxford University Press, OxfordGoogle Scholar
  18. Cannon WB (1932) The wisdom of the body. Norton, New YorkGoogle Scholar
  19. Carroll RL (1988) Vertebrate paleontology and evolution. Freeman, New YorkGoogle Scholar
  20. Carroll SB, Grenier JK, Weatherbee SD (2005) From DNA to diversity. Molecular genetics and the evolution of animal design. Blackwell, MaldenGoogle Scholar
  21. Cavalier-Smith T (2006) Cell evolution and earth history: stasis and revolution. Philos Trans R Soc B 361:969–1006. doi:10.1098/rstb.2006.1842 CrossRefGoogle Scholar
  22. Conway Morris S (2003) Life’s solution. Inevitable humans in a lonely universe. Cambridge University Press, CambridgeGoogle Scholar
  23. De Duve C (2007) The origin of eukaryotes: a reappraisal. Nat Rev Genet 8(5):395–403CrossRefGoogle Scholar
  24. Di Paolo EA (2004) Unbinding biological autonomy: Francisco varela’s contributions to artificial life. Artif Life 10:231–233. doi:10.1162/1064546041255566 CrossRefGoogle Scholar
  25. Dobzhansky T, Ayala FJ, Stebbins GL, Valentine JW (1977) Evolution. Freeman, San FranciscoGoogle Scholar
  26. Doolittle WF (1999) Phylogenetic classification and the universal tree. Science 284(5423):2124. doi:10.1126/science.284.5423.2124 CrossRefGoogle Scholar
  27. Dubbeldam JL (2001) Evolution of playlike behaviour and the uncoupling of neural locomotor mechanisms. Neth J Zool 51:335–345. doi:10.1163/156854201753247587 Google Scholar
  28. Eibl-Eibesfeldt I (1999) Grundriß der vergleichenden Verhaltensforschung. Piper, MünchenGoogle Scholar
  29. Gerhart J, Kirschner M (1997) Cells, embryos, and evolution. Toward a cellular and developmental understanding of phenotypic variation and evolutionary adaptability. Blackwell, MaldenGoogle Scholar
  30. Gould SJ (1983) The hardening of the modern synthesis. In: Grene M (ed) Dimensions of Darwinism. Cambridge University Press, New York, pp 71–93Google Scholar
  31. Gould SJ (2002) The structure of evolutionary theory. The Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  32. Gutmann WF (1981) Relationships between invertebrate phyla based on functional-mechanical analysis of the hydrostatic skeleton. Am Zool 21:63–81Google Scholar
  33. Hassenstein B (1969) Aspekte der “Freiheit” im Verhalten von Tieren. Universitas (Stuttg) 24:1325–1330Google Scholar
  34. Heinrich B (2004) Corvids: the crow family. In: Bekoff M (ed) Encyclopedia of animal behavior, vol 1. Greenwood, Westport, pp 445–447Google Scholar
  35. Huxley J (1948) Evolution, the modern synthesis, 3rd edn. Allen & Unwin, London 1974Google Scholar
  36. Huxley J (1957) The three types of evolutionary process. Nature 180:454–455. doi:10.1038/180454a0 CrossRefGoogle Scholar
  37. Jablonka E, Lamb MJ (2006) Evolution in four dimensions. Genetic, epigenetic, behavioral, and symbolic variation in the history of life. MIT Press, CambridgeGoogle Scholar
  38. Jonas H (1966) The phenomenon of life: toward a philosophical biology. Harper and Row, New YorkGoogle Scholar
  39. Kauffman S (2003) Molecular autonomous agents. Philos Trans R Soc Lond A 361:1089–1099. doi:10.1098/rsta.2003.1186 CrossRefGoogle Scholar
  40. Kirk DL (2005) A twelve-step program for evolving multicellularity and a division of labor. Bioessays 27:299–310. doi:10.1002/bies.20197 CrossRefGoogle Scholar
  41. Kirschner MW, Gerhart JC (2005) The plausibility of life. Resolving Darwins’s dilemma. Yale University Press, New HavenGoogle Scholar
  42. Kitano H (2007) Towards a theory of biological robustness. Mol Syst Biol 3:137. doi:10.1038/msb4100179 CrossRefGoogle Scholar
  43. Koteja P (2000) Energy assimilation, parental care and the evolution of endothermy. Proc R Soc Lond B Biol Sci 267:479–484. doi:10.1098/rspb.2000.1025 CrossRefGoogle Scholar
  44. Laland KN, Odling-Smee J, Feldman MW (2005) On the breadth and significance of niche construction: a reply to Griffiths, Okasha and Sterelny. Biol Philos 20:37–55CrossRefGoogle Scholar
  45. Lewontin R (2000) The triple helix. Gene, organism and environment. Harvard University Press, CambridgeGoogle Scholar
  46. Lillywhite HB, Maderson PFA (1988) The structure and permeability of integument. Am Zool 28:945–962Google Scholar
  47. López-García P, Moreira D (2004) The synthrophy hypothesis for the origin of eukaryotes. In: Seckbach J (ed) Symbiosis: mechanisms and model systems. Kluwer Academic Publisher, Dordrecht, pp 133–147Google Scholar
  48. Luisi PL (2003) Autopoiesis: a review and a reappraisal. Naturwissenschaften 90:49–59Google Scholar
  49. Mahner M, Bunge M (1997) Foundations of biophilosophy. Springer, BerlinGoogle Scholar
  50. Margulis L, Sagan D (2002) Acquiring genomes. A theory of the origins of species. Basic Books, New YorkGoogle Scholar
  51. McNamara KJ (ed) (1990) Evolutionary trends. Belhaven, LondonGoogle Scholar
  52. McShea D (1998) Possible largest-scale trends in organismal evolution: eight ‘live hypotheses’. Annu Rev Ecol Syst 29:293–318. doi:10.1146/annurev.ecolsys.29.1.293 CrossRefGoogle Scholar
  53. Moreno A, Etxeberria A, Umerez J (2008) The autonomy of biological individuals and artificial models. Biosystems 91:309–319. doi:10.1016/j.biosystems.2007.05.009 CrossRefGoogle Scholar
  54. Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution. Princeton University Press, PrincetonGoogle Scholar
  55. Pough FH (1980) The advantages of ectothermy for tetrapods. Am Nat 115:92–112. doi:10.1086/283547 CrossRefGoogle Scholar
  56. Rieger RM (1984) Evolution of the Cuticle in the lower eumeatzoa. In: Bereiter-Hahn J, Matoltsy AG, Sylvia Richards K (eds) Biology of the integument. Springer, Berlin, pp 389–399Google Scholar
  57. Rieger RM (1994) Evolution of the “lower” metazoa. In: Bengtson S (ed) Early life on earth. Columbia University Press, NY, pp 475–488Google Scholar
  58. Rosslenbroich B (2006) The notion of progress in evolutionary biology—the unresolved problem and an empirical suggestion. Biol Philos 21:41–70. doi:10.1007/s10539-005-0957-4 CrossRefGoogle Scholar
  59. Rosslenbroich B (2007) Autonomiezunahme als Modus der Makroevolution. Galunder, NümbrechtGoogle Scholar
  60. Roth G (1981) Biological systems theory and the problem of reductionism. In: Roth G, Schwegler H (eds) Self-organizing systems. An interdisciplinary approach. Campus, Frankfurt, pp 106–120Google Scholar
  61. Roth G, Wullimann MF (2001) Brain evolution and cognition. Wiley-VCH, New York, HeidelbergGoogle Scholar
  62. Ruben J (1995) The evolution of endothermy in mammals and birds: from physiology to fossils. Annu Rev Physiol 57:69–95. doi:10.1146/annurev.ph.57.030195.000441 CrossRefGoogle Scholar
  63. Ruben JA, Jones TD, Geist NR (2003) Respiratory and reproductive paleophysiology of dinosaurs and early birds. Physiol Biochem Zool 76:141–164. doi:10.1086/375425 CrossRefGoogle Scholar
  64. Ruiz-Mirazo K, Moreno A (2004) Basic autonomy as a fundamental step in the synthesis of life. Artif Life 10:235–259. doi:10.1162/1064546041255584 CrossRefGoogle Scholar
  65. Ruiz-Mirazo K, Umerez J, Moreno A (2008) Enabling conditions for ‘open-ended evolution’. Biol Philos 23:67–85. doi:10.1007/s10539-007-9076-8 CrossRefGoogle Scholar
  66. Schad W (1993) Heterochronical patterns of evolution in the transitional stages of vertebrate classes. Acta Biotheor 41:383–389. doi:10.1007/BF00709372 CrossRefGoogle Scholar
  67. Shubin NH, Marshall CR (2000) Fossils, genes, and the origin of novelty. Paleobiology 26(Suppl. 4):324–340. doi:10.1666/0094-8373(2000)26[324:FGATOO]2.0.CO;2 CrossRefGoogle Scholar
  68. Simpson GG (1971) The meaning of evolution, 6th edn. Yale University Press, New HavenGoogle Scholar
  69. Slobodkin LB (1964) The strategy of evolution. Am Sci 52:342–357Google Scholar
  70. Smith H (1953) From fish to philosopher. Little Brown, BostonGoogle Scholar
  71. Spencer H (1864) Principles of biology. Williams Norgate, LondonGoogle Scholar
  72. Steiner R (1894) Philosophy of freedom. Rudolf Steiner Press, LondonGoogle Scholar
  73. Stelling J, Sauer U, Szallasi Z, Doyle FJIII, Doyle J (2004) Robustness of cellular functions. Cell 118:675–685. doi:10.1016/j.cell.2004.09.008 CrossRefGoogle Scholar
  74. Streffer W (2009) Klangsphären. Motive der Autonomie im Gesang der Vögel, StuttgartGoogle Scholar
  75. Sumida SS, Martin KLM (eds) (1997) Amniote origins completing the transition to land. Academic Press, LondonGoogle Scholar
  76. Turner JS (2007) The tinkerer’s accomplice. How design emerges from life itself. Harvard University Press, CambridgeGoogle Scholar
  77. Varela FJ (1979) Principles of biological autonomy. New York, North HollandGoogle Scholar
  78. Varela FJ (1981) Autonomy and autopoiesis. In: Roth G, Schwegler H (eds) Self-organizing systems. An interdisciplinary approach. Campus, Frankfurt, pp 14–23Google Scholar
  79. Waggoner B (2001) Eukaryotes and multicells: origin. Encycl life sci. www.els.net, doi: 10.1038/npg.els.0001627
  80. Wagner A (2005) Robustness, evolvability, and neutrality. FEBS Lett, Elsevier Amsterdam (www.FEBSLetters.org) 579:1772–1778. doi: 10.1016/j.febslet.2005.01.063
  81. Wagner G, Chiu CH, Laubichler M (2000) Developmental evolution as a mechanistic science: the inference from developmental mechanisms to evolutionary processes. Am Zool 40:819–831. doi:10.1668/0003-1569(2000)040[0819:DEAAMS]2.0.CO;2 CrossRefGoogle Scholar
  82. Wake DB (1986) Directions in the history of life. Group report. In: Raup DM, Jablonski D (eds) Patterns and processes in the history of life. Report of the Dahlem workshop on patterns and processes in the history of life. Springer, BerlinGoogle Scholar
  83. Weingarten M (1993) Organismen—Objekte oder Subjekte der Evolution? DarmstadtGoogle Scholar
  84. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar
  85. Willmer P (1990) Invertebrate relationships. Patterns in animal evolution. Cambridge University Press, CambridgeGoogle Scholar
  86. Willmer P, Stone G, Johnston I (2000) Environmental physiology of animals. Blackwell, LondonGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Institute of Evolutionary Biology and MorphologyUniversity of Witten-HerdeckeWittenGermany

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