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Evolutionary Biology

, Volume 45, Issue 4, pp 374–394 | Cite as

A Virtue Made of Necessity: Is the Increasing Hierarchical Complexity of Sexual Clades an Inevitable Outcome of Their Declining (Macro)evolutionary Potential?

  • Jan Toman
  • Jaroslav Flegr
Synthesis Paper
  • 75 Downloads

Abstract

The increasing maximal hierarchical complexity of organisms is one of the best-supported macroevolutionary trends. The nature and causes of this trend, as well as several accompanying macroevolutionary phenomena are, however, still unclear. In this theoretical article, we propose that the cause of this trend could be the increasing pressure of species selection, which results from the gradual decrease of (macro)evolutionary potential (i.e. the probability of producing major evolutionary innovations). As follows from the Theory of Frozen Evolution, this process is an inevitable consequence of the sorting of genes, traits, and their integrated groups (modules) based on their contextually dependent stability. In turn, this causes effectively unchangeable elements of genetic architecture to accumulate during the existence of evolutionary lineages. Although (macro)evolutionary potential can be partially restored by several processes, a profound restoration of (macro)evolutionary potential is probably possible only by means of a transition to a higher level of hierarchical complexity. However, the accumulation of contextually more stable elements continues even on this higher level. This leads to the integration of the modular character of composite organisms and a repeated pressure to increase the level of hierarchical complexity. Our model explains all components of McShea’s “Evolutionary Syndrome,” i.e. the trend of increasing the hierarchical complexity of organisms, the growth of variability among elements on the immediately lower level, and their gradual machinification. This pattern should be characteristic of sexual eukaryotes and especially their complex representatives. Our model also sheds new light on several related macroevolutionary phenomena, such as the gradual acceleration of the trend or the striking difference between pre-Neoproterozoic and Phanerozoic evolution.

Keywords

Evolvability (Macro)evolutionary potential Evolutionary trends Hierarchical complexity Frozen evolution theory Frozen plasticity theory Stability-based sorting 

Notes

Acknowledgements

We thank Lincoln Cline and Charlie Lotterman for the final revisions of our text.

Funding

This work was supported by the Grant Agency of the Charles University in Prague (project no: 578416); and the Charles University Research Centre (UNCE 204004). The funding sources had no role in study design, collection, analysis and interpretation of data, the writing of the report or in the decision to submit the article for publication.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Adami, C., Ofria, C., & Collier, T. (2000). Evolution of biological complexity. Proceedings of the National Academy of Sciences of the United States of America, 97(9), 4463–4468.  https://doi.org/10.1073/pnas.97.9.4463.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Arthur, W. (1982). A developmental approach to the problem of variation in evolutionary rates. Biological Journal of the Linnean Society, 18(3), 243–261.  https://doi.org/10.1111/j.1095-8312.1982.tb02038.x.CrossRefGoogle Scholar
  3. Auman, T., & Chipman, A. D. (2017). The evolution of gene regulatory networks that define arthropod body plans. Integrative and Comparative Biology, 57(3), 523–532.  https://doi.org/10.1093/icb/icx035.CrossRefPubMedGoogle Scholar
  4. Bedau, M. (2009). The evolution of complexity. In A. Barberousse, M. Morange & T. Pradeu (Eds.), Mapping the Future of biology: Evolving concepts and theories (pp. 111–130). Dodrecht: Springer.CrossRefGoogle Scholar
  5. Bedau, M., McCaskill, J., Packard, N., Rasmussen, S., Adami, C., Green, D., et al. (2000). Open problems in artificial life. Artificial Life, 6(4), 363–376.  https://doi.org/10.1162/106454600300103683.CrossRefPubMedGoogle Scholar
  6. Bedau, M., Snyder, E., Brown, C. T., & Packard, N. H. (1997). A comparison of evolutionary activity in artificial evolving systems and in the biosphere. In P. Husbands, & I. Harvey (Eds.), Proceedings of the fourth European conference on artificial life (pp. 125–134). Cambridge: MIT Press.Google Scholar
  7. Blount, Z., Borland, C., & Lenski, R. (2008). Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 105(23), 7899–7906.  https://doi.org/10.1073/pnas.0803151105.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bonner, J. (1988). The evolution of complexity by means of natural selection. Princeton: Princeton University Press.Google Scholar
  9. Bonner, J. (1998). The origins of multicellularity. Integrative Biology Issues News and Reviews, 1(1), 27–36.CrossRefGoogle Scholar
  10. Bonner, J. (2003). On the origin of differentiation. Journal of Biosciences, 28(4), 523–528.  https://doi.org/10.1007/BF02705126.CrossRefPubMedGoogle Scholar
  11. Bouchard, F. (2011). Darwinism without populations: A more inclusive understanding of the “survival of the fittest”. Studies in History and Philosophy of Science Part C: Studies in History and Philosophy of Biological and Biomedical Sciences, 42(1), 106–114.  https://doi.org/10.1016/j.shpsc.2010.11.002.CrossRefGoogle Scholar
  12. Bouchard, F., & Huneman, P. (2013). From groups to individuals: Evolution and emerging individuality. Cambridge: MIT Press.Google Scholar
  13. Bourrat, P. (2014). From survivors to replicators: Evolution by natural selection revisited. Biology & Philosophy, 29(4), 517–538.  https://doi.org/10.1007/s10539-013-9383-1.CrossRefGoogle Scholar
  14. Brigandt, I. (2015). From developmental constraint to evolvability: How concepts figure in explanation and disciplinary identity. In A. Love (Ed.), Conceptual change in biology (pp. 305–352). Dordrecht: Springer.Google Scholar
  15. Budd, G. (2006). On the origin and evolution of major morphological characters. Biological Reviews, 81(4), 609–628.  https://doi.org/10.1017/S1464793106007135.CrossRefPubMedGoogle Scholar
  16. Buss, L. (2014). The evolution of individuality. Princeton: Princetom University Press.Google Scholar
  17. Butterfield, N. (2007). Macroevolution and macroecology through deep time. Palaeontology, 50(1), 41–55.  https://doi.org/10.1111/j.1475-4983.2006.00613.x.CrossRefGoogle Scholar
  18. Calcott, B. (2008). The other cooperation problem: Generating benefit. Biology & Philosophy, 23(2), 179–203.  https://doi.org/10.1007/s10539-007-9095-5.CrossRefGoogle Scholar
  19. Calcott, B., & Sterelny, K. (2001). The major transitions in evolution revisited. Cambridge: MIT Press.Google Scholar
  20. Callebaut, W., & Rasskin-Gutman, D. (2005). Modularity: Understanding the development and evolution of natural complex systems. Cambridge: MIT Press.Google Scholar
  21. Canning, E., Okamura, B., Baker, J., Muller, R., & Rollinson, D. (2004). Biodiversity and evolution of the myxozoa. Advances in Parasitology, 56(56), 43–131.  https://doi.org/10.1016/S0065-308X(03)56002-X.CrossRefPubMedGoogle Scholar
  22. Carroll, S. (2001). Chance and necessity: The evolution of morphological complexity and diversity. Nature, 409(6823), 1102–1109.  https://doi.org/10.1038/35059227.CrossRefPubMedGoogle Scholar
  23. Channon, A. (2001). Passing the A life test: Activity statistics classify evolution in Geb as unbounded. In J. Kelemen, & P. Sosik (Eds.), Advances in artificial life: 6th European conference (pp. 417–426). Prague: ECALCrossRefGoogle Scholar
  24. Channon, A., & Damper, R. (2000). Towards the evolutionary emergence of increasingly complex advantageous behaviours. International Journal of Systems Science, 31(7), 843–860.  https://doi.org/10.1080/002077200406570.CrossRefGoogle Scholar
  25. Chao, L. (1990). Fitness of RNA virus decreased by Muller’s ratchet. Nature, 348(6300), 454–455.  https://doi.org/10.1038/348454a0.CrossRefPubMedGoogle Scholar
  26. Claessen, D., Rozen, D., Kuipers, O., Sogaard-Andersen, L., & van Wezel, G. (2014). Bacterial solutions to multicellularity: A tale of biofilms, filaments and fruiting bodies. Nature Reviews Microbiology, 12(2), 115–124.  https://doi.org/10.1038/nrmicro3178.CrossRefPubMedGoogle Scholar
  27. Corning, P., & Szathmary, E. (2015). “Synergistic selection”: A Darwinian frame for the evolution of complexity. Journal of Theoretical Biology, 371, 45–58.  https://doi.org/10.1016/j.jtbi.2015.02.002.CrossRefPubMedGoogle Scholar
  28. Crombach, A., & Hogeweg, P. (2008). Evolution of evolvability in gene regulatory networks. PLoS Computational Biology, 4(7), 1–13.  https://doi.org/10.1371/journal.pcbi.1000112.CrossRefGoogle Scholar
  29. Davidson, E., & Erwin, D. (2006). Gene regulatory networks and the evolution of animal body plans. Science, 311(5762), 796–800.  https://doi.org/10.1126/science.1113832.CrossRefPubMedGoogle Scholar
  30. Davison, J. (1998). Evolution as a self-limiting process. Rivista Di Biologia-Biology Forum, 91(2), 199–220.Google Scholar
  31. de Vladar, H., Santos, M., & Szathmáry, E. (2017). Grand views of evolution. Trends in Ecology & Evolution.  https://doi.org/10.1016/j.tree.2017.01.008.CrossRefGoogle Scholar
  32. Dececchi, T., & Larsson, H. (2013). Body and limb size dissociation at the origin of birds: Uncoupling allometric constraints across a macroevolutionary transition. Evolution, 67(9), 2741–2752.  https://doi.org/10.1111/evo.12150.CrossRefPubMedGoogle Scholar
  33. DiMichele, W., & Bateman, R. (1996). Plant paleoecology and evolutionary inference: Two examples from the Paleozoic. Review of Palaeobotany and Palynology, 90(3–4), 223–247.  https://doi.org/10.1016/0034-6667(95)00085-2.CrossRefGoogle Scholar
  34. Doolittle, W. (2014). Natural selection through survival alone, and the possibility of Gaia. Biology & Philosophy, 29(3), 415–423.  https://doi.org/10.1007/s10539-013-9384-0.CrossRefGoogle Scholar
  35. Eble, G. (1998). The role of development in evolutionary radiations. In M. McKinney & J. Drake (Eds.), Biodiversity dynamics: Turnover of populations, taxa, and communities (pp. 132–161). New York: Columbia University Press.Google Scholar
  36. Eble, G. (1999). Originations: Land and sea compared. Geobios, 32(2), 223–234.  https://doi.org/10.1016/S0016-6995(99)80036-9.CrossRefGoogle Scholar
  37. Eble, G. (2005). Morphological modularity and macroevolution: Conceptual and empirical aspects. In W. Callebaut & R.-G. D (Eds.), Modularity: Understanding the development and evolution of natural complex systems (pp. 221–238). Cambridge: MIT Press.Google Scholar
  38. Erwin, D. (2007). Disparity: Morphological pattern and developmental context. Palaeontology, 50(1), 57–73.  https://doi.org/10.1111/j.1475-4983.2006.00614.x.CrossRefGoogle Scholar
  39. Erwin, D., Valentine, J., & Sepkoski, J. (1987). A comparative study of diversification events: The early Paleozoic versus the Mesozoic. Evolution, 41(6), 1177–1186.  https://doi.org/10.2307/2409086.CrossRefPubMedGoogle Scholar
  40. Flegr, J. (1998). On the “origin” of natural selection by means of speciation. Rivista Di Biologia-Biology Forum, 91(2), 291–304.  https://doi.org/10.1400/22749.CrossRefGoogle Scholar
  41. Flegr, J. (2008). Frozen evolution: Or, that’s not the way it is, Mr. Darwin—farewell to selfish gene. Scotts Valley: Createspace Independent Pub.Google Scholar
  42. Flegr, J. (2010). Elastic, not plastic species: Frozen plasticity theory and the origin of adaptive evolution in sexually reproducing organisms. Biology Direct.  https://doi.org/10.1186/1745-6150-5-2.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Flegr, J. (2013). Microevolutionary, macroevolutionary, ecological and taxonomical implications of punctuational theories of adaptive evolution. Biology Direct.  https://doi.org/10.1186/1745-6150-8-1.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Flegr, J. (2015). Evolutionary meltdown: Or on the origin of Genera (Evoluční tání aneb O původu rodů). Praha: Academia.Google Scholar
  45. Flegr, J., & Ponížil, P. (2018). On the importance of being stable: Evolutionarily frozen species can win in fluctuating environments. Biological Journal of the Linnean Society.  https://doi.org/10.1093/biolinnean/bly110.CrossRefGoogle Scholar
  46. Foote, M. (1997). The evolution of morphological diversity. Annual Review of Ecology and Systematics, 28, 129–152.  https://doi.org/10.1146/annurev.ecolsys.28.1.129.CrossRefGoogle Scholar
  47. Galis, F., & Metz, J. (2001). Testing the vulnerability of the phylotypic stage: On modularity and evolutionary conservation. Journal of Experimental Zoology, 291(2), 195–204.  https://doi.org/10.1002/jez.1069.CrossRefPubMedGoogle Scholar
  48. Glenner, H., & Hebsgaard, M. B. (2006). Phylogeny and evolution of life history strategies of the parasitic barnacles (Crustacea, Cirripedia, Rhizocephala). Molecular Phylogenetics and Evolution, 41(3), 528–538.  https://doi.org/10.1016/j.ympev.2006.06.004.CrossRefPubMedGoogle Scholar
  49. Godfrey-Smith, B. (2009). Darwinian populations and natural selection. Oxford: Oxford University Press.CrossRefGoogle Scholar
  50. Gould, S. (1989). Wonderful life: The burgess shale and the nature of history. New York: W. W. Norton & Company.Google Scholar
  51. Gould, S. (2002). The structure of evolutionary theory. Cambridge: The Belknap Press of Harvard University Press.Google Scholar
  52. Gregory, T. (2008). Evolutionary trends. Evolution: Education and Outreach, 1(3), 259–273.  https://doi.org/10.1007/s12052-008-0055-6.CrossRefGoogle Scholar
  53. Gregory, W., Roigneau, M., Burr, E., Evans, G., Hellman, E., Jackson, F., et al. (1935). Williston’s law relating to the evolution of skull bones in the vertebrates. American Journal of Physical Anthropology, 20(2), 123–152.  https://doi.org/10.1002/ajpa.1330200202.CrossRefGoogle Scholar
  54. Hu, H., Uesaka, M., Guo, S., Shimai, K., Lu, T.-M., Li, F., et al. (2017). Constrained vertebrate evolution by pleiotropic genes. Nature Ecology & Evolution, 1(11), 1722–1730.  https://doi.org/10.1038/s41559-017-0318-0.CrossRefGoogle Scholar
  55. Hughes, C. L., & Kaufman, T. C. (2002). Hox genes and the evolution of the arthropod body plan. Evolution & Development, 4(6), 459–499.  https://doi.org/10.1046/j.1525-142X.2002.02034.x.CrossRefGoogle Scholar
  56. Hughes, M., Gerber, S., & Wills, M. (2013). Clades reach highest morphological disparity early in their evolution. Proceedings of the National Academy of Sciences of the United States of America, 110(34), 13875–13879.  https://doi.org/10.1073/pnas.1302642110.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Human, K., & Gordon, D. (1996). Exploitation and interference competition between the invasive Argentine ant, Linepithema humile, and native ant species. Oecologia, 105(3), 405–412.  https://doi.org/10.1007/BF00328744.CrossRefPubMedGoogle Scholar
  58. Jablonka, E., & Lamb, M. (2006). The evolution of information in the major transitions. Journal of Theoretical Biology, 239(2), 236–246.  https://doi.org/10.1016/j.jtbi.2005.08.038.CrossRefPubMedGoogle Scholar
  59. Kirschner, M., & Gerhart, J. (1998). Evolvability. Proceedings of the National Academy of Sciences of the United States of America, 95(15), 8420–8427.  https://doi.org/10.1073/pnas.95.15.8420.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Knoll, A., & Bambach, R. (2000). Directionality in the history of life: Diffusion from the left wall or repeated scaling of the right? Paleobiology, 26(4), 1–14.  https://doi.org/10.1666/0094-8373(2000)26%5B1:DITHOL%5D2.0.CO;2.CrossRefGoogle Scholar
  61. Langton, C. (1984). Self-reproduction in cellular automata. Physica D: Nonlinear Phenomena, 10(1–2), 135–144.  https://doi.org/10.1016/0167-2789(84)90256-2.CrossRefGoogle Scholar
  62. Lee, M., Soubrier, J., & Edgecombe, G. (2013). Rates of phenotypic and genomic evolution during the cambrian explosion. Current Biology, 23(19), 1889–1895.  https://doi.org/10.1016/j.cub.2013.07.055.CrossRefPubMedGoogle Scholar
  63. Lenski, R. (2004). Phenotypic and genomic evolution during a 20,000-generation experiment with the bacterium Escherichia coli. Plant Breeding Reviews, 24(2), 225–266.Google Scholar
  64. Lewontin, R. (1978). Adaptation. Scientific American, 239(3), 212–231.CrossRefGoogle Scholar
  65. Lloyd, G., Wang, S., & Brusatte, S. (2012). Identifying heterogeneity in rates of morphological evolution: Discrete character change in the evolution of lungfish (Sarcopterygii; Dipnoi). Evolution: International Journal of Organic Evolution, 66(2), 330–348.  https://doi.org/10.1111/j.1558-5646.2011.01460.x.CrossRefGoogle Scholar
  66. Marcot, J., & McShea, D. (2007). Increasing hierarchical complexity throughout the history of life: Phylogenetic tests of trend mechanisms. Paleobiology, 33(2), 182–200.  https://doi.org/10.1666/06028.1.CrossRefGoogle Scholar
  67. Maynard Smith, J., & Szathmáry, E. (2010). The major transitions in evolution. Oxford: Oxford University Press.Google Scholar
  68. McInerney, J., Martin, W., Koonin, E., Allen, J., Galperin, M., Lane, N., et al. (2011). Planctomycetes and eukaryotes: A case of analogy not homology. Bioessays, 33(11), 810–817.  https://doi.org/10.1002/bies.201100045.CrossRefPubMedPubMedCentralGoogle Scholar
  69. McMullin, B. (2000). John von Neumann and the evolutionary growth of complexity: Looking backward, looking forward. Artificial Life, 6(4), 347–361.  https://doi.org/10.1162/106454600300103674.CrossRefPubMedGoogle Scholar
  70. McNamara, K. (1990). Evolutionary trends. Tucson: University of Arizona Press.Google Scholar
  71. McNamara, K. (2006). Evolutionary trends. eLS.  https://doi.org/10.1038/npg.els.0004136.CrossRefGoogle Scholar
  72. McShea, D. (1991). Complexity and evolution: What everybody knows. Biology and Philosophy, 6(3), 303–324.  https://doi.org/10.1007/BF00132234.CrossRefGoogle Scholar
  73. McShea, D. (1993). Evolutionary change in the morphological complexity of the mammalian vertebral column. Evolution, 47(3), 730–740.  https://doi.org/10.2307/2410179.CrossRefPubMedGoogle Scholar
  74. McShea, D. (1994). Mechanisms of large-scale evolutionary trends. Evolution, 48(6), 1747–1763.  https://doi.org/10.2307/2410505.CrossRefPubMedGoogle Scholar
  75. McShea, D. (1996). Metazoan complexity and evolution: Is there a trend? Perspective. Evolution, 50(2), 477–492.  https://doi.org/10.2307/2410824.CrossRefPubMedGoogle Scholar
  76. McShea, D. (1998). Possible largest-scale trends in organismal evolution: Eight “live hypotheses”. Annual Review of Ecology and Systematics, 29, 293–318.  https://doi.org/10.1146/annurev.ecolsys.29.1.293.CrossRefGoogle Scholar
  77. McShea, D. (2000). Functional complexity in organisms: Parts as proxies. Biology & Philosophy, 15(5), 641–668.  https://doi.org/10.1023/A:1006695908715.CrossRefGoogle Scholar
  78. McShea, D. (2001a). The hierarchical structure of organisms: A scale and documentation of a trend in the maximum. Paleobiology. 27(2), 405–423.  https://doi.org/10.1666/0094-8373(2001)027%3C0405:THSOOA%3E2.0.CO;2.CrossRefGoogle Scholar
  79. McShea, D. (2001b). The minor transitions in hierarchical evolution and the question of a directional bias. Journal of Evolutionary Biology, 14(3), 502–518.  https://doi.org/10.1046/j.1420-9101.2001.00283.x.CrossRefGoogle Scholar
  80. McShea, D. (2002). A complexity drain on cells in the evolution of multicellularity. Evolution, 56(3), 441–452.  https://doi.org/10.1111/j.0014-3820.2002.tb01357.x.CrossRefPubMedGoogle Scholar
  81. McShea, D. (2005). The evolution of complexity without natural selection, a possible large-scale trend of the fourth kind. Paleobiology, 31(2), 146–156.CrossRefGoogle Scholar
  82. McShea, D. (2015). Three trends in the history of life: An evolutionary syndrome. Evolutionary Biology, 43(4), 531–542.  https://doi.org/10.1007/s11692-015-9323-x.CrossRefGoogle Scholar
  83. McShea, D., & Anderson, C. (2005). The remodularization of the organism. In W. Callebaut & R.-G. D (Eds.), Modularity: Understanding the development and evolution of natural complex systems (pp. 185–205). Cambridge: MIT Press.Google Scholar
  84. McShea, D., & Brandon, R. (2010). Biology’s First Law. Chicago: University of Chicago Press.CrossRefGoogle Scholar
  85. McShea, D., & Changizi, M. (2003). Three puzzles in hierarchical evolution. Integrative and Comparative Biology, 43(1), 74–81.  https://doi.org/10.1093/icb/43.1.74.CrossRefPubMedGoogle Scholar
  86. McShea, D., & Simpson, C. (2001). The miscellaneous transitions in evolution. In B. Calcott & K. Sterelny (Eds.), The major transitions in evolution revisited (pp. 19–33). Cambridge: MIT Press.Google Scholar
  87. Melo, D., Porto, A., Cheverud, J., Marroig, G., & Futuyma, D. (2016). Modularity: Genes, development, and evolution. Annual Review of Ecology, Evolution, and Systematics, 47, 463–486.  https://doi.org/10.1146/annurev-ecolsys-121415-032409.CrossRefPubMedPubMedCentralGoogle Scholar
  88. Meyer, A., & Van de Peer, Y. (2005). From 2R to 3R: Evidence for a fish-specific genome duplication (FSGD). Bioessays, 27(9), 937–945.  https://doi.org/10.1002/bies.20293.CrossRefPubMedGoogle Scholar
  89. Michod, R. (2000). Darwinian dynamics: Evolutionary transitions in fitness and individuality. Princeton: Princeton University Press.Google Scholar
  90. Michod, R. (2007). Evolution of individuality during the transition from unicellular to multicellular life. Proceedings of the National Academy of Sciences of the United States of America, 104(suppl1), 8613–8618.  https://doi.org/10.1073/pnas.0701489104.CrossRefPubMedPubMedCentralGoogle Scholar
  91. Michod, R., & Herron, M. (2006). Cooperation and conflict during evolutionary transitions in individuality. Journal of Evolutionary Biology, 19(5), 1406–1409.  https://doi.org/10.1111/j.1420-9101.2006.01142.x.CrossRefPubMedGoogle Scholar
  92. Michod, R., & Nedelcu, A. (2003). On the reorganization of fitness during evolutionary transitions in individuality. Integrative and Comparative Biology, 43(1), 64–73.  https://doi.org/10.1093/icb/43.1.64.CrossRefPubMedGoogle Scholar
  93. Mills, D., Peterson, R., & Spiegelman, S. (1967). An extracellular Darwinian experiment with a self-duplicating nucleic acid molecule. Proceedings of the National Academy of Sciences of the United States of America, 58(1), 217–224.  https://doi.org/10.1073/pnas.58.1.217.CrossRefPubMedPubMedCentralGoogle Scholar
  94. Mitchell, M. (2009). Complexity: A guided tour. Oxford: Oxford University Press.Google Scholar
  95. Monteiro, A. (2012). Gene regulatory networks reused to build novel traits: Co-option of an eye-related gene regulatory network in eye-like organs and red wing patches on insect wings is suggested by optix expression. BioEssays, 34(3), 181–186.  https://doi.org/10.1002/bies.201100160.CrossRefPubMedGoogle Scholar
  96. Morlon, H., Potts, M., & Plotkin, J. (2010). Inferring the dynamics of diversification: A coalescent approach. PLoS Biology, 8(9), 1–13.  https://doi.org/10.1371/journal.pbio.1000493.CrossRefGoogle Scholar
  97. Muller, H. (1964). The relation of recombination to mutational advance. Mutation Research, 1(1), 2–9.  https://doi.org/10.1016/0027-5107(64)90047-8.CrossRefGoogle Scholar
  98. Murchison, E. (2008). Clonally transmissible cancers in dogs and Tasmanian devils. Oncogene, 27, 19–30.  https://doi.org/10.1038/onc.2009.350.CrossRefGoogle Scholar
  99. Nedelcu, A., & Michod, R. (2004). Evolvability, modularity, and individuality during the transition to multicellularity in volvocalean green algae. In G. Schlosser & G. Wagner (Eds.), Modularity in development and evolution (pp. 466–489). Chicago: The University of Chicago Press.Google Scholar
  100. Novák, V. (1982). The principle of sociogenesis. Praha: Academia.Google Scholar
  101. Oehlenschläger, F., & Eigen, M. (1997). 30 years later: A new approach to Sol Spiegelman’s and Leslie Orgel’s in vitro evolutionary studies—dedicated to Leslie Orgel on the occasion of his 70th birthday. Origins of Life and Evolution of the Biosphere, 27(5–6), 437–457.  https://doi.org/10.1023/A:1006501326129.CrossRefPubMedGoogle Scholar
  102. Okasha, S. (2006). Evolution and the levels of selection. Oxford: Oxford University Press.CrossRefGoogle Scholar
  103. Pavlicev, M., & Wagner, G. (2012). Coming to grips with evolvability. Evolution: Education and Outreach, 5(2), 231–244.  https://doi.org/10.1007/s12052-012-0430-1.CrossRefGoogle Scholar
  104. Pettersson, M. (1996). Complexity and evolution. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  105. Pigliucci, M. (2008). Opinion: Is evolvability evolvable? Nature Reviews Genetics, 9(1), 75–82.  https://doi.org/10.1038/nrg2278.CrossRefPubMedGoogle Scholar
  106. Pross, A. (2012). What is life? How chemistry becomes biology. Oxford: Oxford University Press.Google Scholar
  107. Queller, D. (1997). Cooperators since life began. The Quarterly Review of Biology, 72(2), 184–188.  https://doi.org/10.1086/419766.CrossRefGoogle Scholar
  108. Queller, D. (2000). Relatedness and the fraternal major transitions. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 355(1403), 1647–1655.  https://doi.org/10.1098/rstb.2000.0727.CrossRefGoogle Scholar
  109. Queller, D., & Strassmann, J. (2009). Beyond society: The evolution of organismality. Philosophical Transactions of the Royal Society B-Biological Sciences, 364(1533), 3143–3155.  https://doi.org/10.1098/rstb.2009.0095.CrossRefPubMedCentralGoogle Scholar
  110. Raff, R. A., & Wray, G. A. (1989). Heterochrony: Developmental mechanisms and evolutionary results. Journal of Evolutionary Biology, 2(6), 409–434.  https://doi.org/10.1046/j.1420-9101.1989.2060409.x.CrossRefGoogle Scholar
  111. Rasnicyn, A. (2005). Collected works in evolutionary biology (Izbrannye trudy po evolucionnoj biologii). Moscow: Tovarisevstvo naucnych izdanii KMK.Google Scholar
  112. Rasskin-Gutman, D., & Esteve-Altava, B. (2008). The multiple directions of evolutionary change. Bioessays, 30(6), 521–525.  https://doi.org/10.1002/bies.20766.CrossRefPubMedGoogle Scholar
  113. Ray, T. (1993). An evolutionary approach to synthetic biology: Zen and the art of creating life. Artificial Life, 1(1_2), 179–209.CrossRefGoogle Scholar
  114. Ray, T. (1997). Evolving complexity. Artificial Life and Robotics, 1(1), 21–26.CrossRefGoogle Scholar
  115. Ray, T., & Hart, J. (1998). Evolution of differentiated multi-threaded digital organisms. In C. Adami, R. Belew, H. Kitano, & C. Taylor (Eds.), Artificial life VI: Proceedings of the sixth international conference on artificial life (pp. 295–306). Cambridge: MIT Press.Google Scholar
  116. Ridley, M. (1994). The red queen: Sex and the evolution of human nature. Westminster: Penguin.Google Scholar
  117. Riedl, R. (1977). A systems-analytical approach to macro-evolutionary phenomena. Quarterly Review of Biology, 52(4), 351–370.  https://doi.org/10.1086/410123.CrossRefPubMedGoogle Scholar
  118. Riedl, R. (1978). Order in living organisms: A systems analysis of evolution. New York: Wiley.Google Scholar
  119. Rosa, D. (1899). La Riduzione progressiva della variabilità e i suoi rapporti coll’estinzione e coll’origine delle specie. Torino: Clausen.Google Scholar
  120. Sayama, H. (1999). A new structurally dissolvable self-reproducing loop evolving in a simple cellular automata space. Artificial Life, 5(4), 343–365.  https://doi.org/10.1162/106454699568818.CrossRefPubMedGoogle Scholar
  121. Schank, J., & Wimsatt, W. (1986). Generative entrenchment and evolution. In PSA: Proceedings of the biennial meeting of the philosophy of science association, number two: Symposia and invited papers (pp. 33–60). Baltimore: Philosophy of Science Association.Google Scholar
  122. Schlosser, G. (2002). Modularity and the units of evolution. Theory in Biosciences, 121(1), 1–80.  https://doi.org/10.1078/1431-7613-00049.CrossRefGoogle Scholar
  123. Schlosser, G. (2004). The role of modules in development and evolution. In G. Schlosser & G. Wagner (Eds.), Modularity in development and evolution (pp. 519–582). Chicago: The University of Chicago Press.Google Scholar
  124. Schlosser, G., & Wagner, G. (2004). Modularity in development and evolution. Chicago: University of Chicago Press.Google Scholar
  125. Schoch, R. (2010). Riedl’s burden and the body plan: Selection, constraint, and deep time. Journal of Experimental Zoology Part B-Molecular and Developmental Evolution, 314B(1), 1–10.  https://doi.org/10.1002/jez.b.21300.CrossRefGoogle Scholar
  126. Shcherbakov, V. (2012). Stasis is an inevitable consequence of every successful evolution. Biosemiotics, 5(2), 227–245.  https://doi.org/10.1007/s12304-011-9122-4.CrossRefGoogle Scholar
  127. Shubin, N., Tabin, C., & Carroll, S. (1997). Fossils, genes and the evolution of animal limbs. Nature, 388(6643), 639.  https://doi.org/10.1038/41710.CrossRefPubMedGoogle Scholar
  128. Simon, H. (1962). The architecture of complexity. Proceedings of the American Philosophical Society, 106(6), 467–482.Google Scholar
  129. Simonin, K., & Roddy, A. (2018). Genome downsizing, physiological novelty, and the global dominance of flowering plants. PLOS Biology, 16(1), 1–15.  https://doi.org/10.1371/journal.pbio.2003706.CrossRefGoogle Scholar
  130. Simpson, C. (2012). The evolutionary history of division of labour. Proceedings of the Royal Society B-Biological Sciences, 279(1726), 116–121.  https://doi.org/10.1098/rspb.2011.0766.CrossRefGoogle Scholar
  131. Sinervo, B., & Lively, C. M. (1996). The rock–paper–scissors game and the evolution of alternative male strategies. Nature, 380(6571), 240.  https://doi.org/10.1038/380240a0.CrossRefGoogle Scholar
  132. Smith, A. (2007). Marine diversity through the Phanerozoic: Problems and prospects. Journal of the Geological Society, 164(4), 731–745.  https://doi.org/10.1144/0016/76492006-184.CrossRefGoogle Scholar
  133. Spiegelman, S., Haruna, I., Holland, I., Beaudreau, G., & Mills, D. (1965). The synthesis of a self-propagating and infectious nucleic acid with a purified enzyme. Proceedings of the National Academy of Sciences of the United States of America, 54(3), 919–927.  https://doi.org/10.1073/pnas.54.3.919.CrossRefPubMedPubMedCentralGoogle Scholar
  134. Sterelny, K. (1999). Bacteria at the high table. Biology & Philosophy, 14(3), 459–470.  https://doi.org/10.1023/A:1006542531480.CrossRefGoogle Scholar
  135. Sterelny, K. (2004). Symbiosis, evolvability, and modularity. In G. Schlosser & G. Wagner (Eds.), Modularity in development and evolution (pp. 490–516). Chicago: The University of Chicago Press.Google Scholar
  136. Suzuki, H., Ono, N., & Yuta, K. (2003). Several necessary conditions for the evolution of complex forms of life in an artificial environment. Artificial Life, 9(2), 153–174.  https://doi.org/10.1162/106454603322221504.CrossRefPubMedGoogle Scholar
  137. Szathmáry, E. (2015). Toward major evolutionary transitions theory 2.0. Proceedings of the National Academy of Sciences of the United States of America, 112(33), 10104–10111.  https://doi.org/10.1073/pnas.1421398112.CrossRefPubMedPubMedCentralGoogle Scholar
  138. Szathmáry, E., & Maynard Smith, J. (1995). The major evolutionary transitions. Nature, 374(6519), 227–232.  https://doi.org/10.1038/374227a0.CrossRefPubMedGoogle Scholar
  139. Thearling, K., & Ray, T. (1994). Evolving multi-cellular artificial life. In R. Brooks, & P. Maes (Eds.), Artificial life IV: Proceedings of the fourth international workshop on the synthesis and simulation of living systems (pp. 283–288). Cambridge: MIT Press.Google Scholar
  140. Thearling, K., & Ray, T. (1996). Evolving parallel computation. Complex Systems, 10(3), 229–237.Google Scholar
  141. Thomas, R. (2005). Hierarchical integration of modular structures in the evolution of animal skeletons. In W. Callebaut & R.-G. D (Eds.), Modularity: Understanding the development and evolution of natural complex systems (pp. 239–258). Cambridge: MIT Press.Google Scholar
  142. Toman, J., & Flegr, J. (2017a). General environmental heterogeneity as the explanation of sexuality? Comparative study shows that ancient asexual taxa are associated with both biotically and abiotically homogeneous environments. Ecology and Evolution.  https://doi.org/10.1002/ece3.3716.CrossRefPubMedPubMedCentralGoogle Scholar
  143. Toman, J., & Flegr, J. (2017b). Stability-based sorting: The forgotten process behind (not only) biological evolution. Journal of Theoretical Biology, 435, 29–41.  https://doi.org/10.1016/j.jtbi.2017.09.004.CrossRefPubMedGoogle Scholar
  144. Toman, J., & Flegr, J. (2018). Macroevolutionary freezing and the Janusian nature of evolvability: Is the evolution (of profound biological novelty) going to end? Biosemiotics, 11(2), 263–285.  https://doi.org/10.1007/s12304-018-9326-y.CrossRefGoogle Scholar
  145. Turney, P. (1999). Increasing Evolvability Considered as a Large-Scale Trend in Evolution. In Proceedings of the 1999 Genetic and Evolutionary Computation Conference (GECCO-99). Orlando: National Research Council of Canada.Google Scholar
  146. Valentine, J. (1995). Why no new phyla after the cambrian? Genome and ecospace hypotheses revisited. Palaios, 10(2), 190–194.  https://doi.org/10.2307/3515182.CrossRefGoogle Scholar
  147. Valentine, J., Collins, A., & Meyer, C. (1994). Morphological complexity increase in metazoans. Paleobiology, 20(2), 131–142.  https://doi.org/10.1017/S0094837300012641.CrossRefGoogle Scholar
  148. Von Dassow, G., & Meir, E. (2004). Exploring modularity with dynamical models of gene networks. In G. Schlosser & G. Wagner (Eds.), Modularity in development and evolution (pp. 244–287). Chicago: The University of Chicago Press.Google Scholar
  149. Vrsansky, P. (2000). Decreasing variability—from the Carboniferous to the present! (Validated on independent lineages of Blattaria). Paleontological Journal, 34(S3), S374–S379.Google Scholar
  150. Vrsansky, P., Oruzinsky, R., Aristov, D., Wei, D., Vidlicka, L., & Ren, D. (2017). Temporary deleterious mass mutations relate to originations of cockroach families. Biologia, 72(8), 886–912.  https://doi.org/10.1515/biolog-2017-0096.CrossRefGoogle Scholar
  151. Wagner, G. (1989a). The biological homology concept. Annual Review of Ecology and Systematics, 20(1), 51–69.  https://doi.org/10.1146/annurev.es.20.110189.000411.CrossRefGoogle Scholar
  152. Wagner, G. (1989b). The origin of morphological characters and the biological basis of homology. Evolution, 43(6), 1157–1171.  https://doi.org/10.2307/2409354.CrossRefPubMedGoogle Scholar
  153. Wagner, G., & Altenberg, L. (1996). Perspective: Complex adaptations and the evolution of evolvability. Evolution, 50(3), 967–976.  https://doi.org/10.2307/2410639.CrossRefPubMedGoogle Scholar
  154. Wagner, G., & Laubichler, M. (2004). Rupert Riedl and the re-synthesis of evolutionary and developmental biology: Body plans and evolvability. Journal of Experimental Zoology Part B-Molecular and Developmental Evolution, 302B(1), 92–102.  https://doi.org/10.1002/jez.b.20005.CrossRefGoogle Scholar
  155. Wagner, P. (1996). Contrasting the underlying patterns of active trends in morphological evolution. Evolution, 50(3), 990–1007.  https://doi.org/10.1111/j.1558-5646.1996.tb02341.x.CrossRefPubMedGoogle Scholar
  156. Watson, R. (2006). Compositional evolution: The impact of sex, symbiosis, and modularity on the gradualist framework of evolution. Vienna: MIT Press.Google Scholar
  157. Watson, R., & Szathmary, E. (2016). How can evolution learn? Trends in Ecology & Evolution, 31(2), 147–157.  https://doi.org/10.1016/j.tree.2015.11.009.CrossRefGoogle Scholar
  158. Webster, M. (2007). A Cambrian peak in morphological variation within trilobite species. Science, 317(5837), 499–502.  https://doi.org/10.1126/science.1142964.CrossRefPubMedGoogle Scholar
  159. Westheide, W. (1987). Progenesis as a principle in meiofauna evolution. Journal of Natural History, 21(4), 843–854.  https://doi.org/10.1080/00222938700770501.CrossRefGoogle Scholar
  160. Williams, G. (1966). Adaptation and natural selection: A critique of some current evolutionary thought. Princeton: Princeton University Press.Google Scholar
  161. Wimsatt, W. (2013). The role of generative entrenchment and robustness in the evolution of complexity. In C. Lineweaver, P. Davies & M. Ruse (Eds.), Complexity and the arrow of time (pp. 308–331). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  162. Wimsatt, W. (2015). Entrenchment as a theoretical tool in evolutionary developmental biology. In A. Love (Ed.), Conceptual change in biology: Scientific and philosophical perspectives on evolution and development. Dordrecht: Springer.Google Scholar
  163. Wimsatt, W., & Schank, J. (2004). Generative entrenchment, modularity, and evolvability: When genic selection meets the whole organism. In G. Schlosser & G. Wagner (Eds.), Modularity in development and evolution (pp. 359–394). Chicago: The University of Chicago Press.Google Scholar
  164. Yaeger, L. (1994). Computational genetics, physiology, metabolism, neural systems, learning, vision, and behavior or polyworld: Life in a new context. In C. Langton (Ed.), Artificial Life 3: Proceedings of the third international conference on the synthesis and simulation of living systems (pp. 263–298). Reading: Addison-Wesley.Google Scholar
  165. Zuckerkandl, E. (1997). Neutral and nonneutral mutations: The creative mix—evolution of complexity in gene interaction systems. Journal of Molecular Evolution, 44(suppl1), S2–S8.  https://doi.org/10.1007/PL00000048.CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Laboratory of Evolutionary Biology, Department of Philosophy and History of Sciences, Faculty of ScienceCharles UniversityPrague 2Czech Republic

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