Evolution by means of natural selection without reproduction: revamping Lewontin’s account

Abstract

This paper analyzes recent attempts to reject reproduction with lineage formation as a necessary condition for evolution by means of natural selection (Bouchard in Philos Sci 75(5):560–570, 2008; Stud Hist Philos Sci Part C Stud Hist Philos Biol Biomed Sci 42(1):106–114, 2011; Bourrat in Biol Philos 29(4):517–538, 2014; Br J Philos Sci 66(4):883–903, 2015; Charbonneau in Philos Sci 81(5):727–740, 2014; Doolittle and Inkpen in Proc Natl Acad Sci 115(16):4006–4014, 2018). Building on the strengths of these attempts and avoiding their pitfalls, it is argued that a robust formulation of evolution by natural selection without reproduction can be established. The main contribution of this paper is a reformulation of Lewontin’s three principles (Lewontin in Annu Rev Ecol Syst 1:1–18, 1970) stating that minimal evolution by natural selection occurs when two conditions are met in a population: fitness-related variation and memory (population-level inheritance). Paradigmatic evolution by natural selection, which can generate adaptations, takes place when an additional condition is present, namely regeneration.

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

Fig. 1

Notes

  1. 1.

    I provide only a superficial analysis of Godfrey-Smith’s very rich and insightful treatment of the concept of reproduction. This overview should suffice to fulfill the aim of this section, that is, to highlight the consensus according to which reproduction is necessary for ENS to obtain and to identify an abstract definition of reproduction that can apply despite the variety of ways in which it has been defined.

  2. 2.

    While the expression “origin explanation” has indeed been coined by Godfrey-Smith, it should be noted that Neander (1995a, b) similarly highlighted the creative power of natural selection, in cases of cumulative (rather than single-step) selection. Her claim sparked a debate with Sober (1995), who famously emphasized the negative power of selection (Sober 1984).

  3. 3.

    As it is shown shortly, I reject Bouchard’s claim that the notion of population needs to be replaced by the concept of ensemble. I keep using the concept of population even when discussing his work in order to simplify the analysis.

  4. 4.

    In a recent paper (Bourrat 2019), Bourrat further theorizes heritability by developing a causation (interventionist) account of it. While the paper is extremely interesting and has great practical value, the issue tackled therein is orthogonal to the more abstract and conceptual debate broached in this paper.

  5. 5.

    Charbonneau explicitly acknowledges that the resulting analysis is not a comprehensive in regard to the complexity of reproduction and the role it plays in the biological world. However, he claims that focusing on those two aspects allows for sufficient precision relative to its role as a necessary condition for ENS. This nuance is completely endorsed and reiterated in the context of this paper.

  6. 6.

    Given the aim of the paper, one might think I am suggesting that the evolutionary success of an entity should only be calculated in regard to its persisting capacities. It is not the case. Calculating fitness in regard to reproduction and survivability is an extremely powerful way to make evolutionary predictions. This is true even if reproduction is but one evolutionary strategy among others that generate success. In the thought experiment now being discussed, reproduction could be taken into account in the evolutionary success as calculated by the machine before a new event of creation. Hence, there will sometimes be causal input by parent on the offspring, and sometimes not. This is coherent with the claim that reproduction is neither a defining trait of units of selection nor necessary for ENS to occur.

  7. 7.

    As this paper is focused on the notion of reproduction and hence on those of memory and regeneration, it leaves the notion of fitness somewhat unspecified. Nonetheless, building on the work of Bouchard and Bourrat, the abstract definition provided here fulfills the needs of a general account of ENS. Further specifications of parameters can be added to fulfill the needs of specific empirical inquiries, when required (e.g. Roughgarden et al. 2018).

References

  1. Ariew, A. (2008). Population thinking. In M. Ruse (Ed.), The Oxford handbook of philosophy of biology (pp. 64–86). Oxford: Oxford University Press.

    Google Scholar 

  2. Bapteste, E., & Huneman, P. (2018). Towards a Dynamic Interaction Network of Life to unify and expand the evolutionary theory. BMC Biology,16, 56.

    Article  Google Scholar 

  3. Bapteste, E., O’Malley, M. A., Beiko, R. G., Ereshefsky, M., Gogarten, J. P., Franklin-Hall, L., et al. (2009). Prokaryotic evolution and the tree of life are two different things. Biology Direct,4(1), 34.

    Article  Google Scholar 

  4. Booth, A. (2014a). Symbiosis, selection, and individuality. Biology and Philosophy,29(5), 657–673.

    Article  Google Scholar 

  5. Booth, A. (2014b). Populations and individuals in heterokaryotic fungi: A multilevel perspective. Philosophy of Science,81(4), 612–632.

    Article  Google Scholar 

  6. Bouchard, F. (2004). Evolution, fitness and the struggle for persistence. ProQuest Dissertations Publishing. Retrieved from http://search.proquest.com/docview/305180238/.

  7. Bouchard, F. (2008). Causal processes, fitness, and the differential persistence of lineages. Philosophy of Science,75(5), 560–570.

    Article  Google Scholar 

  8. Bouchard, F. (2010). Symbiosis, lateral function transfer and the (many) saplings of life. Biology and Philosophy,25(4), 623–641.

    Article  Google Scholar 

  9. 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.

    Article  Google Scholar 

  10. Bouchard, F., & Rosenberg, A. (2004). Fitness, probability and the principles of natural selection. The British Journal for the Philosophy of Science,55(4), 693–712.

    Article  Google Scholar 

  11. Bourrat, P. (2014). From survivors to replicators: Evolution by natural selection revisited. Biology and Philosophy,29(4), 517–538.

    Article  Google Scholar 

  12. Bourrat, P. (2015). How to read ‘heritability’in the recipe approach to natural selection. The British Journal for the Philosophy of Science,66(4), 883–903.

    Article  Google Scholar 

  13. Bourrat, P. (2019). Heritability, causal influence and locality. Synthese. https://doi.org/10.1007/s11229-019-02484-3.

    Article  Google Scholar 

  14. Charbonneau, M. (2014). Populations without reproduction. Philosophy of Science,81(5), 727–740.

    Article  Google Scholar 

  15. 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.

    Article  Google Scholar 

  16. Corel, E., Meheust, R., Watson, A. K., McInerney, J. O., Lopez, P., & Bapteste, E. (2018). Bipartite network analysis of gene sharings in the microbial world. Molecular Biology and Evolution,35(4), 899–913.

    Article  Google Scholar 

  17. Dawkins, R. (1976). The selfish gene. Oxford: Oxford University Press.

    Google Scholar 

  18. Dobzhansky, T. (1970). Genetics of the evolutionary process (Vol. 139). New York: Columbia University Press.

    Google Scholar 

  19. Doolittle, W. F. (2000). Uprooting the tree of life. Scientific American,282(2), 90–95.

    Article  Google Scholar 

  20. Doolittle, W. F. (2019). Making evolutionary sense of Gaia. Trends in Ecology & Evolution. https://doi.org/10.1016/j.tree.2019.05.001.

    Article  Google Scholar 

  21. Doolittle, W. F., & Booth, A. (2017). It’s the song, not the singer: an exploration of holobiosis and evolutionary theory. Biology and Philosophy,32(1), 5–24.

    Article  Google Scholar 

  22. Doolittle, W. F., & Inkpen, S. A. (2018). Processes and patterns of interaction as units of selection: An introduction to ITSNTS thinking. Proceedings of the National Academy of Sciences,115(16), 4006–4014.

    Article  Google Scholar 

  23. Douglas, A. E., & Werren, J. H. (2016). Holes in the hologenome: Why host-microbe symbioses are not holobionts. mBio,7(2), e02099-15.

    Article  Google Scholar 

  24. Dupré, J. (2017). The metaphysics of evolution. Interface Focus,7(5), 20160148.

    Article  Google Scholar 

  25. Dupré, J., & O’Malley, M. (2009). Varieties of living things: Life at the intersection of lineage and metabolism. Philosophy et Theory in Biology,1, 1–25.

    Article  Google Scholar 

  26. Dussault, A. C., & Bouchard, F. (2017). A persistence enhancing propensity account of ecological function to explain ecosystem evolution. Synthese,194(4), 1115–1145.

    Article  Google Scholar 

  27. Earnshaw-Whyte, E. (2012). Increasingly radical claims about heredity and fitness. Philosophy of Science,79(3), 396–412.

    Article  Google Scholar 

  28. Endler, J. A. (1986). Natural selection in the wild. Princeton: Princeton University Press.

    Google Scholar 

  29. Ereshefsky, M., & Pedroso, M. (2013). Biological individuality: The case of biofilms. Biology and Philosophy,28(2), 331–349.

    Article  Google Scholar 

  30. Ereshefsky, M., & Pedroso, M. (2015). Rethinking evolutionary individuality. Proceedings of the National Academy of Sciences,112(33), 10126–10132.

    Article  Google Scholar 

  31. Ereshefsky, M., & Pedroso, M. (2016). What biofilms can teach us about individuality. In Alexandre Guay & Thomas Pradeu (Eds.), Individiuals across the sciences (pp. 103–121). New York: Oxford University Press.

    Google Scholar 

  32. Gannett, L. (2003). Making populations: Bounding genes in space and in time. Philosophy of Science,70(5), 989–1001.

    Article  Google Scholar 

  33. Godfrey-Smith, P. (2007). Conditions for evolution by natural selection. The Journal of Philosophy,104(10), 489–516.

    Article  Google Scholar 

  34. Godfrey-Smith, P. (2009). Darwinian populations and natural selection. New York: Oxford University Press.

    Google Scholar 

  35. Godfrey-Smith, P. (2011). Darwinian Populations and Transitions in Individuality. In B. Calcott & K. Sterelny (Eds.), The major transitions in evolution revisited (pp. 65–82). Cambridge: The MIT Press.

    Google Scholar 

  36. Godfrey-Smith, P. (2012). Darwinism and cultural change. Philosophical Transactions of the Royal Society B,367, 2160–2170.

    Article  Google Scholar 

  37. Godfrey-Smith, P. (2013). Darwinian Individuals. In F. Bouchard & P. Huneman (Eds.), From groups to individuals: Evolution and emerging individuality (pp. 17–36). Cambridge, MA: MIT Press.

    Google Scholar 

  38. Godfrey-Smith, P. (2015). Reproduction, symbiosis, and the eukaryotic cell. Proceedings of the National Academy of Sciences,112(33), 10120–10125.

    Article  Google Scholar 

  39. Griesemer, J. R. (2000a). Development, culture and the units of inheritance. Philosophy of Science,67, S348–S368.

    Article  Google Scholar 

  40. Griesemer, J. R. (2000b). The units of evolutionary transition. Selection,1(1–3), 67–80.

    Google Scholar 

  41. Griesemer, J. R. (2005). The informational gene and the substantial body: On the generalization of evolutionary theory by abstraction. In M. R. Jones & N. Cartwright (Eds.), Idealization XII: Correcting the model (pp. 59–115). Brill: Rodopi.

    Google Scholar 

  42. Halfon, M. S. (2017). Perspectives on gene regulatory network evolution. Trends in Genetics,33(7), 436–447.

    Article  Google Scholar 

  43. Hull, D. L. (1978). A matter of individuality. Philosophy of Science,45(3), 335–360.

    Article  Google Scholar 

  44. Hull, D. L. (1980). Individuality and selection. Annual Review of Ecology and Systematics,11, 311–332.

    Article  Google Scholar 

  45. Keller, E. F. (1987). Reproduction and the central project of evolutionary theory. Biology and Philosophy,2, 383–396.

    Article  Google Scholar 

  46. Keller, E. F. (2014). From gene action to reactive genomes. The Journal of Physiology,592(11), 2423–2429.

    Article  Google Scholar 

  47. Koonin, E. V., & Wolf, Y. I. (2009). Is evolution Darwinian or/and Lamarckian? Biology Direct,4(1), 42.

    Article  Google Scholar 

  48. Latour, B., & Lenton, T. M. (2019). extending the domain of freedom, or why Gaia is so hard to understand. Critical Inquiry,45(3), 659–680.

    Article  Google Scholar 

  49. Lewontin, R. C. (1970). The units of selection. Annual Review of Ecology and Systematics,1, 1–18.

    Article  Google Scholar 

  50. Lewontin, R. C. (1985). Adaptation. In R. Levins & R. C. Lewontin (Eds.), The dialectical biologist (pp. 65–84). Cambridge, Massachussets: Harvard University Press.

    Google Scholar 

  51. Lloyd, E. A. (2018). Holobionts as units of selection: Holobionts as interactors, reproducers, and manifestors of adaptation. In S. B. Gissis, E. Lamm, & A. Shavit (Eds.), Landscapes of collectivity in the life sciences (pp. 351–368). Cambridge, MA: MIT Press.

    Google Scholar 

  52. Margulis, L. (1991). Symbiosis as a source of evolutionary innovation: Speciation and morphogenesis. Cambridge, MA: MIT Press.

    Google Scholar 

  53. Méheust, R., Watson, A. K., Lapointe, F. J., Papke, R. T., Lopez, P., & Bapteste, E. (2018). Hundreds of novel composite genes and chimeric genes with bacterial origins contributed to haloarchaeal evolution. Genome Biology,19(1), 75.

    Article  Google Scholar 

  54. Millstein, R. L. (2006). Natural selection as a population-level causal process. The British Journal for the Philosophy of Science,57(4), 627–653.

    Article  Google Scholar 

  55. Millstein, R. L. (2009). Populations as individuals. Biological Theory,4(3), 267–273.

    Article  Google Scholar 

  56. Millstein, R. L. (2010). The concepts of population and metapopulation in evolutionary biology and ecology. In M. A. Bell, D. J. Futuyma, W. F. Eanes, & J. S. Levinton (Eds.), Evolution since Darwin: The first 150 years (pp. 61–86). Sunderland, MA: Sinauer.

    Google Scholar 

  57. Moran, N. A., & Sloan, D. B. (2015). The hologenome concept: Helpful or hollow? PLoS Biology,13(12), e1002311.

    Article  Google Scholar 

  58. Morgan, G. J., & Pitts, W. B. (2008). Evolution without species: The case of mosaic bacteriophages. The British Journal for the Philosophy of Science,59(4), 745–765.

    Article  Google Scholar 

  59. Neander, K. (1995a). Explaining complex adaptations: A reply to Sober’s ‘reply to Neander’. The British Journal for the Philosophy of Science,46(4), 583–587.

    Article  Google Scholar 

  60. Neander, K. (1995b). Pruning the tree of life. The British Journal for the Philosophy of Science,46(1), 59–80. https://doi.org/10.1093/bjps/46.1.59.

    Article  Google Scholar 

  61. O’Malley, M. A. (2014). Philosophy of microbiology. Cambridge: Cambridge University Press.

    Google Scholar 

  62. O’Malley, M. A. (2015). Reproduction expanded: Multigenerational and multilineal units of evolution. Philosophy of Science,83(5), 835–847.

    Article  Google Scholar 

  63. O’Malley, M. A., & Dupré, J. (2007). Size doesn’t matter: Towards a more inclusive philosophy of biology. Biology and Philosophy,22(2), 155–191.

    Article  Google Scholar 

  64. Odling-Smee, J., Laland, K., & Feldman, M. (2003). Niche construction: The neglected process in evolution. Princeton, NJ: Princeton University Press.

    Google Scholar 

  65. Okasha, S. (2006). Evolution and the levels of selection. Oxford: Oxford University Press.

    Google Scholar 

  66. Papale, F., Saget, J., & Bapteste, É. (2019). Networks consolidate the core concepts of evolution. Trends in Microbiology. https://doi.org/10.1016/j.tim.2019.11.006.

    Article  Google Scholar 

  67. Pigliucci, M., & Müller, G. B. (Eds.). (2010). Evolution—The extended synthesis. Cambridge, MA: MIT Press.

    Google Scholar 

  68. Reydon, T. A. C., & Scholz, M. (2015). Searching for Darwinism in generalized Darwinism. The British Journal for the Philosophy of Science,66(3), 561–589.

    Article  Google Scholar 

  69. Ridley, M. (1996). Evolution (2nd ed.). Oxford: Blackwell.

    Google Scholar 

  70. Rosenberg, E., Sharon, G., & Zilber-Rosenberg, I. (2009). The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework. Environmental Microbiology,11(12), 2959–2962.

    Article  Google Scholar 

  71. Roughgarden, J. (2019). Holobiont evolution: Model with vertical vs. horizontal microbiome transmission. bioRxiv. https://doi.org/10.1101/465310.

  72. Roughgarden, J., Gilbert, S. F., Rosenberg, E., Zilber-Rosenberg, I., & Lloyd, E. A. (2018). Holobionts as units of selection and a model of their population dynamics and evolution. Biological Theory,13(1), 44–65.

    Article  Google Scholar 

  73. Skillings, D. (2016). Holobionts and the ecology of organisms: Multi-species communities or integrated individuals? Biology and Philosophy,31(6), 875–892.

    Article  Google Scholar 

  74. Sober, E. (1984). The nature of selection. Cambridge, MA: The MIT Press/A Bradford Book.

    Google Scholar 

  75. Sober, E. (1995). Natural selection and distributive explanation: A reply to Neander. The British Journal for the Philosophy of Science,46(3), 384–397. https://doi.org/10.1093/bjps/46.3.384.

    Article  Google Scholar 

  76. Williams, H. T. P., & Lenton, T. J. (2008). Environmental regulation in a network of simulated microbial ecosystems. Proceedings of the National Academy of Sciences of the United States of America,105(30), 10432–10435.

    Article  Google Scholar 

  77. Wilson, D. S., & Sober, E. (1989). Reviving the superorganism. Journal of Theoretical Biology,136(3), 337–356.

    Article  Google Scholar 

  78. Woese, C. (1998). The universal ancestor. Proceedings of the National Academy of Sciences,95(12), 6854–6859.

    Article  Google Scholar 

  79. Xavier, J. B., & Foster, K. R. (2007). Cooperation and conflict in microbial biofilms. Proceedings of the National Academy of Sciences,104(3), 876–881.

    Article  Google Scholar 

  80. Zilber-Rosenberg, I., & Rosenberg, E. (2008). Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiology Reviews,32(5), 723–735.

    Article  Google Scholar 

Download references

Acknowledgements

I wish to thank Mathieu Charbonneau, Pierrick Bourrat, Frédéric Bouchard, Éric Bapteste and Cassandre Ville for their unwavering support and for their help with the paper. I am also grateful to a few anonymous referees for their great insights and comments.

Funding

The Social Sciences and Humanities Research Council of Canada provided financial support for this research (file number: 767-2018-1113).

Author information

Affiliations

Authors

Corresponding author

Correspondence to François Papale.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Papale, F. Evolution by means of natural selection without reproduction: revamping Lewontin’s account. Synthese (2020). https://doi.org/10.1007/s11229-020-02729-6

Download citation

Keywords

  • Biology
  • Evolution
  • Natural selection
  • Reproduction
  • Inheritance
  • Unit of selection