Tempos and modes of collectivity in the history of life

  • Douglas H. ErwinEmail author
Original Article


Collective integration and processing of information have increased through the history of life, through both the formation of aggregates in which the entities may have very different properties and which jointly coarse-grained environmental variables (ranging from widely varying metabolism in microbial consortia to the ecological diversity of species on reefs) and through collectives of similar entities (such as cells within an organism or social groups). Such increases have been implicated in significant transitions in the history of life, including aspects of the origin of life, the generation of pangenomes among microbes and microbial communities such as stromatolites, multicellularity and social insects. This contribution provides a preliminary overview of the dominant modes of collective information processing in the history of life, their phylogenetic distribution and extent of convergence, and the effects of new modes for integrating and acting upon information on the tempo of evolutionary change.


Evolutionary novelty Major evolutionary transitions Pangenome Convergence 



I appreciate the opportunity extended by the organizers to participate in the Santa Fe Institute working group meeting on collective computation (B. Daniels, J. Flack and M. Laubichler) and to contribute to this special issue. The discussions among the participants in the meeting also greatly influenced the resulting paper. I was supported by NASA through National Astrobiology Institute (Grant No. NNA13AA90A) to the MIT node.


  1. Allwood AC, Walter MR, Kamber BS, Marshall CP, Burch IW (2006) Stromatolite reef from the Early Archaean era of Australia. Nature 441:714–718CrossRefPubMedGoogle Scholar
  2. Arendt D (2008) The evolution of cell types in animals: emerging principles from molecular studies. Nat Rev Genet 8:868–882CrossRefGoogle Scholar
  3. Arendt D, Tosches MA, Marlow H (2016) From nerve net to nerve ring, nerve cord and brain: evolution of the nervous system. Nat Rev Neurosci 17:61–72. CrossRefPubMedGoogle Scholar
  4. Berezikov E (2011) Evolution of microRNA diversity and regulation in animals. Nat Rev Genet 12:846–860CrossRefPubMedGoogle Scholar
  5. Bergstrom CT, Rosvall M (2011) The transmission sense of information. Biol Philos 26:159–176. CrossRefGoogle Scholar
  6. Bolouri H, Davidson EH (2002) Modeling transcriptional regulatory networks. BioEssays 24:1118–1129CrossRefPubMedGoogle Scholar
  7. Boyd R (2018) A different kind of animal. Princeton University Press, PrincetonCrossRefGoogle Scholar
  8. Calcott B, Sterelny K (eds) (2011) The major transitions in evolution revisited. MIT Press, CambridgeGoogle Scholar
  9. Conway Morris S (2010) Evolution: like any other science it is predictable. Philos Trans R Soc Lond B Biol Sci 365:133–145. CrossRefPubMedCentralGoogle Scholar
  10. Cornforth DM et al (2014) Combinatorial quorum sensing allows bacteria to resolve their social and physical environment. Proc Natl Acad Sci USA 111:4280–4284. CrossRefPubMedGoogle Scholar
  11. Couzin ID (2009) Collective cognition in animal groups. Trends Cog Sci 13:36–43. CrossRefGoogle Scholar
  12. Daniels BC, Ellison CJ, Krakauer DC, Flack JC (2016) Quantifying collectivity. Curr Opin Neurobiol 37:106–113. CrossRefPubMedGoogle Scholar
  13. Darwin C (1881) The formation of vegetable mould, through the action of worMS. John Murray, LondonGoogle Scholar
  14. Davidson EH, Erwin DH (2010) Evolutionary innovation and stability in animal gene networks. J Exp Zool (Mol Dev Evol) 314B:182–186Google Scholar
  15. de Muizon C (1993) Walrus-like feeding adaptation in a new cetacean from the Pliocene of Peru. Nature 365:745–748CrossRefGoogle Scholar
  16. Degnan BM, Vervoort M, Larroux C, Richards GS (2009) Early evolution of metazoan transcription factors. Curr Opin Genet Dev 19:591–599. CrossRefPubMedGoogle Scholar
  17. Delwiche CF (1999) Tracing the thread of plastid diversity through the tapestry of life. Am Nat 154(Suppl):S164–S177CrossRefPubMedGoogle Scholar
  18. Douglas AE (2014) Symbiosis as a general principle in eukaryotic evolution. Cold Spring Harbor Perspect Biol 6:a016113CrossRefGoogle Scholar
  19. Eme L, Spang A, Lombard J, Stairs CW, Ettema TJG (2017) Archaea and the origin of eukaryotes. Nat Rev Microbiol 15:711–723. CrossRefPubMedGoogle Scholar
  20. Erkenbrack EM, Davidson EH (2015) Evolutionary rewiring of gene regulatory network linkages at divergence of the echinoid subclasses. Proc Natl Acad Sci USA 112:E4075–E4084. CrossRefPubMedGoogle Scholar
  21. Erwin DH (2006) Dates and rates: temporal resolution in the deep time stratigraphic record. Ann Rev Earth Planet Sci 34:569–589CrossRefGoogle Scholar
  22. Erwin DH (2008) Macroevolution of ecosystem engineering, niche construction and diversity. Trends Ecol Evol 23:304–310CrossRefPubMedGoogle Scholar
  23. Erwin DH (2015) Early metazoan life: divergence, environment and ecology. Philos Trans R Soc B. CrossRefGoogle Scholar
  24. Erwin DH (2016) Wonderful life revisited: chance and contingency in the Ediacaran-Cambrian radiation. In: Ramsay G, Pence CH (eds) Chance in evolution. University of Chicago Press, Chicago, pp 277–298Google Scholar
  25. Erwin DH, Davidson EH (2009) The evolution of hierarchical gene regulatory networks. Nat Rev Genet 10:141–148. CrossRefPubMedGoogle Scholar
  26. Erwin DH, Tweedt SM (2011) Ecosystem engineering and the Ediacaran-Ordovician diversification of Metazoa. Evol Ecol 26:417–433CrossRefGoogle Scholar
  27. Feinerman O, Korman A (2017) Individual versus collective cognition in social insects. J Exp Biol 220:73–82. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Flack JC (2012) Multiple time-scales and the developmental dynamics of social systems. Philos Trans R Soc B 367:1802–1810. CrossRefGoogle Scholar
  29. Flack JC (2017a) Life’s information hierarchy. In: Walker SI, Davies PCW, Ellis GFR (eds) From matter to life. Cambridge University Press, Cambridge, pp 283–302CrossRefGoogle Scholar
  30. Flack JC (2017b) Coarse-graining as downward causation. Philos Trans R Soc A 375(2109):20160338CrossRefGoogle Scholar
  31. Gompel N, Prud’homme B, Wittkopp PJ, Kassner VA, Carroll SB (2005) Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433:481–487CrossRefPubMedGoogle Scholar
  32. Grotzinger JP, Knoll AH (1999) Stromatolites in Precambrian carbonates: evolutionary mileposts or environmental dipsticks? Ann Rev Earth Planet Sci 27:313–358CrossRefGoogle Scholar
  33. Hallgrimsson B et al (2019) The developmental-genetics of canalization. Sem Cell Dev Biol 88:69–79. CrossRefGoogle Scholar
  34. Hein AM, Rosenthal SB, Hagstrom GI, Berdahl A, Torney CJ, Couzin ID (2015) The evolution of distributed sensing and collective computation in animal populations. eLife. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Hopfield JJ, Tank DW (1986) Computing with neural circuits: a model. Science 233:625–633. CrossRefPubMedGoogle Scholar
  36. Jekely G, Keijzer F, Godfrey-Smith P (2015) An option space for early neural evolution. Philos Trans R Soc Lond B. CrossRefGoogle Scholar
  37. Jensen S, Droser ML, Gehling JG (2005) Trace fossil preservation and the early evolution of animals. Palaeogeogr Palaeoclimatol Palaeoecol 220:19–29CrossRefGoogle Scholar
  38. Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957CrossRefGoogle Scholar
  39. Kiessling W, Simpson C, Foote M (2010) Reefs as cradles of evolution and sources of biodiversity in the Phanerozoic. Science 327:196–198. CrossRefPubMedGoogle Scholar
  40. Knoll AH (2011) The multiple origins of complex multicellularity. Ann Rev Earth Planet Sci 39:217–239CrossRefGoogle Scholar
  41. Lapierrel P, Gogarten JP (2009) Estimating the size of the bacterial pan-genome. Trends Genet 25:107–110. CrossRefGoogle Scholar
  42. Lopez-Garcia P, Moreira D (2015) Open questions on the origin of eukaryotes. Trends Ecol Evol 30:697–708. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Maynard Smith J, Szathmary E (1995) The major transitions in evolution. W. H. Freeman, New YorkGoogle Scholar
  44. McGhee GR Jr (2011) Convergent evolution. MIT Press, CambridgeCrossRefGoogle Scholar
  45. McGhee GR Jr (2016) Can evolution be directional without being teleological? Stud Hist Philos Biol Biomed Sci 58:93–99. CrossRefPubMedGoogle Scholar
  46. McInerney J, Cummins C, Haggerty L (2011) Goods-thinking vs. tree-thinking: finding a place for mobile genetic elements. Mob Genet Elem 1:304–308. CrossRefGoogle Scholar
  47. McInerney JO, O’Connell MJ, Pisani D (2014) The hybrid nature of the Eukaryota and a consilient view of life on Earth. Nat Rev Microbiol 12:449–455. CrossRefPubMedGoogle Scholar
  48. McInerney JO, McNally A, O’Connell MJ (2017) Why prokaryotes have pangenomes. Nat Microbiol. CrossRefPubMedGoogle Scholar
  49. McShea DW (1991) Complexity and evolution: what everybody knows. Biol Philos 6:303–324CrossRefGoogle Scholar
  50. Melo D, Porto A, Cheverud JM, Marroig G (2016) Modularity: genes, development, and evolution. Ann Rev Ecol Evol Syst 47:463–486. CrossRefGoogle Scholar
  51. Michod RE (1999) Darwinian dynamics. Princeton University Press, PrincetonGoogle Scholar
  52. Morris KV, Mattick JS (2014) The rise of regulatory RNA. Nat Rev Genet 15:423–437. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Nandell CD, Bucci V, Drescher K, Levin SL, Bassler BL, Xavier JB (2014) Cutting through the complexity of cell collectives. Proc R Soc Lond B. CrossRefGoogle Scholar
  54. Nordbotten JM, Levin SA, Szathmary E, Stenseth NC (2018) Ecological and evolutionary dynamics of interconnectedness and modularity. Proc Natl Acad Sci USA 115:750–755. CrossRefPubMedGoogle Scholar
  55. Odling-Smee FJ, Laland KN, Feldman MW (2003) Niche construction: the neglected process in evolution. Princeton University Press, PrincetonGoogle Scholar
  56. Peak D, West JD, Messinger SM, Mott KA (2004) Evidence for complex, collective dynamics and emergent, distributed computation in plants. Proc Natl Acad Sci USA 101:918–922. CrossRefPubMedGoogle Scholar
  57. Peter IS, Davidson EH (2011) A gene regulatory network controlling the embryonic specification of endoderm. Nature 474:635–639CrossRefPubMedPubMedCentralGoogle Scholar
  58. Peter IS, Davidson EH (2015) Genomic control processes. Development and evolution. Academic Press, LondonGoogle Scholar
  59. Peter IS, Davidson EH (2017) Assessing regulatory information in developmental gene regulatory networks. Proc Natl Acad Sci USA 114:5862–5869. CrossRefPubMedGoogle Scholar
  60. Peter IS, Faure E, Davidson EH (2012) Predictive computation of genomic logic processing functions in embryonic development. Proc Natl Acad Sci USA 109:16434–16442. CrossRefPubMedGoogle Scholar
  61. Pigliucci M (2008) Is evolvability evolvable? Nat Rev Genet 9:75–82CrossRefPubMedGoogle Scholar
  62. Plotnick RE (2003) Ecological and L-system based simulations of trace fossils. Palaeogeogr Palaeoclimatol Palaeoecol 192:45–58. CrossRefGoogle Scholar
  63. Queller DC (1997) Cooperators since life began. Quart Rev Biol 72:184–188CrossRefGoogle Scholar
  64. Rebeiz M, Patel NH, Hinman VF (2015) Unraveling the tangled skein: the evolution of transcriptional regulatory networks in development. Ann Rev Genom Human Genet 16:103–131. CrossRefGoogle Scholar
  65. Reid P, Dupraz CD, Visscher PT, Sumner DY (2003) Microbial processes forming marine stromatolites. In: Krumbein WE, Paterson DM, Zavarzin GA (eds) Fossil and recent biofilms. Springer, Dordrecht, pp 103–118CrossRefGoogle Scholar
  66. Schmitz JF, Zimmer F, Bornberg-Bauer E (2016) Mechanisms of transcription factor evolution in Metazoa. Nucl Acids Res 44:6287–6297. CrossRefPubMedGoogle Scholar
  67. Sebe-Pedros A, de Mendoza A (2016) Transcription factors and the origin of animal multicellularity. In: Ruiz-Trillo I, Nedelcu AM (eds) Evolutionary transitions to multicellular life, vol 2. Springer, Dordrecht, pp 379–394Google Scholar
  68. Sebe-Pedros A, Ruiz-Trillo I, de Mendoza A, Lang BF, Degnan BM (2011) Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol Biol Evol 28:1241–1254. CrossRefPubMedGoogle Scholar
  69. Sebe-Pedros A et al (2016) The dynamic regulatory genome of Capsaspora and the origin of animal multicellularity. Cell 165:1224–1237. CrossRefPubMedPubMedCentralGoogle Scholar
  70. Seilacher A (1986) Evolution of behavior as expressed in marine trace fossils. In: Nitecki MH, Kitchel JA (eds) Evolution of animal behavior. Oxford University Press, Oxford, pp 62–87Google Scholar
  71. Shapiro JA (1988) Thinking about bacterial populations as multicellular organisms. Ann Rev Microbiol 52:81–104CrossRefGoogle Scholar
  72. Smaldino PE, Richerson PJ (2013) Human cumulative cultural evolution as a form of distributed computation. In: Mechelucci P (ed) Handbook of human computation. Springer, New York, pp 979–992CrossRefGoogle Scholar
  73. Szabo A, Mayor R (2016) Modelling collective cell migration of neural crest. Curr Opin Cell Biol 42:22–28. CrossRefPubMedPubMedCentralGoogle Scholar
  74. Takahashi KH (2018) Multiple modes of canalization: links between genetic, environmental canalizations and developmental stability, and their trait-specificity. Sem Cell Dev Biol. CrossRefGoogle Scholar
  75. Tosches MA (2017) Developmental and genetic mechanisms of neural circuit evolution. Dev Biol 431:16–25. CrossRefPubMedGoogle Scholar
  76. Tweedt SM, Erwin DH (2015) Origin of metazoan developmental toolkits and their expression in the fossil record. In: Ruiz-Trillo I, Nedelcu AM (eds) Evolution of multicellularity. Academic Press, London, pp 47–77Google Scholar
  77. Valiant L (2013) Probably approximately correct. Basic Books, New YorkGoogle Scholar
  78. Van Belleghem SM et al (2017) Complex modular architecture around a simple toolkit of wing pattern genes. Nat Ecol Evol 1:52. CrossRefPubMedGoogle Scholar
  79. Wagner GP, Altenberg L (1996) Complex adaptations and the evolution of evolvability. Evolution 50:967–976CrossRefPubMedGoogle Scholar
  80. Wagner PJ, Kosnik MA, Lidgard S (2006) Abundance distributions imply elevated complexity of post-Paleozoic marine ecosystems. Science 314:1289–1292CrossRefPubMedGoogle Scholar
  81. Wagner GP, Pavlicev M, Cheverud JM (2007) The road to modularity. Nat Rev Genet 8:921–931CrossRefPubMedGoogle Scholar
  82. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Ann Rev Cell Dev Biol 21:319–346. CrossRefGoogle Scholar
  83. Watson RA, Szathmary E (2016) How can evolution learn? Trends Ecol Evol 31:147–157. CrossRefPubMedGoogle Scholar
  84. Watson RA et al (2016) Evolutionary connectionism: algorithmic principles underlying the evolution of biological organisation in evo-devo, evo-eco and evolutionary transitions. Evol Biol 43:553–581. CrossRefPubMedGoogle Scholar
  85. Webster M (2018) Morphological homeostasis in the fossil record. Semin Cell Dev Biol. CrossRefPubMedGoogle Scholar
  86. Wood R (1999) Reef evolution. Oxford University Press, OxfordGoogle Scholar

Copyright information

© This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2019

Authors and Affiliations

  1. 1.Department of Paleobiology, MRC-121National Museum of Natural HistoryWashingtonUSA
  2. 2.Santa Fe InstituteSanta FeUSA

Personalised recommendations