Robustness: The Explanatory Picture

  • Philippe Huneman
Part of the History, Philosophy and Theory of the Life Sciences book series (HPTL, volume 23)


Robustness is a pervasive property of living systems, instantiated at all levels of the biological hierarchies (including ecology). As several other usual concepts in evolutionary biology, such as plasticity or dominance, it has been questioned from the viewpoint of its consequences upon evolution as well as from the side of its causes, on an ultimate or proximate viewpoint. It is therefore equally the explanandum for some enquiries in evolution in ecology, and the explanans for some interesting evolutionary phenomena such as evolvability. This epistemological fact instantiates general property of biological evolution that I call “explanatory reversibility”. In this chapter, I attempt to systematize the explanatory projects regarding robustness by distinguishing a set of epistemological questions. Are they the various expressions of one general project with specific key concepts and methods, or very disparate epistemic projects, unified by the mere homonymy of the term “robustness”? More precisely, are there specific kinds of explanations suited to explain robustness? Finally, how does robustness as an explanandum connect with other explananda in which evolutionists have been massively interested recently such as complexity, modularity or evolvability? After having initially explored various meanings of the concept of robustness and surveyed its instances in biology, I will propose a distinction between mechanical and structural explanations of robustness in evolutionary and functional biology. Then, among the latter, I will highlight the class of “topological explanations,” and the subclass of explanations based on networks, as a major explanatory tool to address robustness. Focusing on evolutionary issues, I will eventually address the “explanatory reversibility” of robustness and consider its relation to key evolutionary concepts that are also explanatorily revertible such as modularity, evolvability and complexity.



The author thanks Anya Plutynski, Nick Jones, Carl Craver and Matteo Mossio for helpful comments and discussions on the arguments presented in this paper. Many thanks to the editors of the volume, whose careful reading improved the manuscript. I also thank Andrew McFarland for his thorough language-check. I am finally grateful to an anonymous reviewer for constructive criticism. This work was possible thanks to the grant ANR--13-BSH3-0007 Explabio and the LIA CNRS Paris “Montreal ECIEB.”


  1. Alon, U. (2007). Network motifs: Theory and experimental approaches. Nature Reviews Genetics, 8, 450–461.CrossRefGoogle Scholar
  2. Baker, A. (2009). Mathematical explanation in science. British Journal for the Philosophy of Science, 60, 611–633.CrossRefGoogle Scholar
  3. Barton, N. (2010). Mutation and the evolution of recombination. Philosophical Transactions of the Royal Society B, 365, 1281–1294.CrossRefGoogle Scholar
  4. Bassett, D., & Muldoon, S. (2016). Network and multilayer network approaches to understanding human brain dynamics. Philosophy of Science, 83(5), 710–720.CrossRefGoogle Scholar
  5. Batterman, R. (2010). On the explanatory role of mathematics in empirical science. British Journal for the Philosophy of Science, 61, 1–25.CrossRefGoogle Scholar
  6. Bernard, C. (1858). Leçons sur la physiologie et la pathologie du système nerveux. Paris: Baillière.Google Scholar
  7. Brandon, R., & McShea, D. (2011). Biology’s first law. Chicago: University of Chicago Press.Google Scholar
  8. Canguilhem, G. (1977). La formation du concept de régulation biologique aux XVIII et XIXe siècles. In Idéologie et rationalité dans l’histoire des sciences de la vie. Paris: Vrin.Google Scholar
  9. Cannon, W. B. (1932). The wisdom of the body. London: Norton.CrossRefGoogle Scholar
  10. Cooper, G. J. (2004). The science of the struggle for existence: On the foundations of ecology. New York: Cambridge University Press.Google Scholar
  11. Craver, C. (2007). Explaining the brain. New York: Oxford University Press.CrossRefGoogle Scholar
  12. Craver, C., & Darden, L. (2013). In search for mechanisms: Discovery across the life sciences. Chicago: University of Chicago Press.CrossRefGoogle Scholar
  13. Cupal, J., Stadler, P., & Schuster, P. (1999). Topology in phenotype space. In J. Giegerich (Ed.), Computer science in biology (pp. 9–15). Dordrecht: Springer.Google Scholar
  14. Darden, L. (2006). Reasoning in biological discoveries: Essays on mechanisms, interfield relations, and anomaly resolution. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  15. Davidson, E. H. (1986). Gene activity in early development. Orlando: Academic.Google Scholar
  16. de Visser, J. A. G. M., Hermisson, J., Wagner, G. P., Ancel Meyers, L., Bagheri-Chaichian, H., Blanchard, J. L., & Chao, L. (2003). Evolution and detection of genetic robustness. Evolution, 57, 1959–1972.Google Scholar
  17. Denamur, E., & Matic, I. (2006). Evolution of mutation rates in bacteria. Molecular Microbiology, 60, 820–827.CrossRefGoogle Scholar
  18. Dunne, J. (2006). The network structure of food webs. In M. Pascual & J. Dunne (Eds.), Ecological networks: Linking structure to dynamics in food webs. Oxford: Oxford University Press.Google Scholar
  19. Dunne, J. A., Williams, R. J., & Martinez, N. D. (2002a). Network structure and biodiversity loss in food webs: Robustness increases with connectance. Ecology Letters, 5, 558–567.CrossRefGoogle Scholar
  20. Dunne, J. E., Williams, R. J., & Martinez, N. D. (2002b). Food web structure and network theory: The role of connectance and size. PNAS, 99, 12917–12922.CrossRefGoogle Scholar
  21. Edwards, A. W. F. (1994). The fundamental theorem of natural selection. Biological Reviews of the Cambridge Philosophical Society, 69(4), 443–474.CrossRefGoogle Scholar
  22. Eldredge, N. (1985). Unfinished synthesis: Biological hierarchies and modern evolutionary thought. New York: Oxford University Press.Google Scholar
  23. Elowitz, M. B., Levine, A. J., Siggia, E. D., et al. (2002). Stochastic gene expression in a single cell. Science, 297, 1183–1186.CrossRefGoogle Scholar
  24. Fisher, R. (1930). The genetical theory of natural selection. London: Methuen.CrossRefGoogle Scholar
  25. Fisher, R. (1932). The evolutionary modification of genetic phenomena. Proceedings of the 6th International Congress of Genetics, 1, 165–172.Google Scholar
  26. Fontana, W., Stadler, P. F., Bornberg-Bauer, E., Griesmacher, T., Hofacker, I. L., Tacker, M., et al. (1999). RNA folding and combinatory landscapes. Physics Review E, 47, 2083–2099.CrossRefGoogle Scholar
  27. Frank, S. A. (2009). The common patterns of nature. Journal of Evolutionary Biology, 22, 1563–1585.CrossRefGoogle Scholar
  28. Glennan, S. (1996). Mechanisms and the nature of causation. Erkenntnis, 44, 49–71.CrossRefGoogle Scholar
  29. Gouyon, P. H., Vienne, D., & Giraud, T. (2015). Sex and evolution. In T. Heams, P. Huneman, G. Lecointre, & M. Silberstein (Eds.), Handbook of evolutionary thinking in the sciences (pp. 499–502). Dordecht: Springer.Google Scholar
  30. Gross, J. L., & Tucker, T. W. (1987). Topological graph theory. Reading: Wiley Interscience.Google Scholar
  31. Holling, G. (1973). Resilience and stability of ecological systems. Annual Review of Ecology and Systematics, 4, 1–23.CrossRefGoogle Scholar
  32. Huneman, P. (2010). Topological explanations and robustness in biological sciences. Synthese, 177(2), 213–245.CrossRefGoogle Scholar
  33. Huneman, P. (Ed.). (2013). Functions: selection and mechanisms. Dordrecht: Springer.Google Scholar
  34. Huneman, P. (2015a). Diversifying the picture of explanations in biological sciences: Ways of combining topology with mechanisms. Synthese. Scholar
  35. Huneman, P. (2015b). Redesigning the argument from design. Paradigmi, 33(2), 105–132.CrossRefGoogle Scholar
  36. Huneman, P. (2017). Outlines of a theory of structural explanations. Philosophical Studies. Scholar
  37. Ives, R., & Carpenter, J. (2007). Stability and diversity of ecosystems. Science, 317(5834), 58–62.CrossRefGoogle Scholar
  38. Jones, N. (2014). Bowtie structures, pathway diagrams, and topological explanation. Erkenntnis, 79, 1135.CrossRefGoogle Scholar
  39. Kéfi, S., Miele, V., Wieters, E. A., Navarrete, S. A., & Berlow, E. L. (2016). How structured is the Entangled Bank? The Surprisingly simple organization of multiplex ecological networks leads to increased persistence and resilience. PLoS Biology, 14(8), e1002527.CrossRefGoogle Scholar
  40. Kitano, H. (2004). Biological robustness. Nature Review Genetics, 5, 826–837.CrossRefGoogle Scholar
  41. Lange, M. (2013). Really statistical explanations and genetic drift. Philosophy of Science, 80(2), 169–188.CrossRefGoogle Scholar
  42. Lenton, T. (2016). Earth system science: A very short introduction. Oxford: Oxford University Press.CrossRefGoogle Scholar
  43. Lesne, A. (2008). Robustness: Confronting lessons from physics and biology. Biological Reviews, 83, 509–532.Google Scholar
  44. Levins, R. (1966). The strategy of model building in population biology. American Scientist, 54, 421–431.Google Scholar
  45. Lynch, M. (2010). Evolution of the mutation rate. Trends in Genetics, 26(8), 345–352.CrossRefGoogle Scholar
  46. Machamer, P., Darden, L., & Craver, C. (2000). Thinking about mechanisms. Philosophy of Science, 67(1), 1–25.CrossRefGoogle Scholar
  47. Martin, G., & Lenormand, T. (2015). The fitness effect of mutations across environments: Fisher’s geometrical model with multiple optima. Evolution, 69, 1433–1447. Scholar
  48. May, R. M. (1974). Stability and complexity in model ecosystems. Princeton: Princeton University Press.Google Scholar
  49. Maynard Smith, J. (1978). The evolution of sex. Cambridge: Cambridge University Press.Google Scholar
  50. Mayr, E. (1961). Cause and effect in biology. Science, 134, 1501–1506.CrossRefGoogle Scholar
  51. 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
  52. Minelli, A. (2017). Evolvability and its evolvability. In P. Huneman & D. Walsh (Eds.), Challenging the modern synthesis. New York: Oxford University Press.Google Scholar
  53. Montoya, J. M., & Solé, R. V. (2002). Small world patterns in food webs. Journal of Theoretical Biology, 214, 405–412.CrossRefGoogle Scholar
  54. Nicoglou, A. (2015). The evolution of phenotypic plasticity: Genealogy of a debate in genetics. Studies in History and Philosophy of Biological and Biomedical Sciences C, 50, 67.CrossRefGoogle Scholar
  55. Nicoglou, A. (ms). Plasticity in biology.Google Scholar
  56. Okasha, S. (2008). Fisher’s “fundamental theorem” of natural selection: A philosophical analysis. British Journal for the Philosophy of Science, 59(3), 319–351.CrossRefGoogle Scholar
  57. Orr, H. A. (2000). Adaptation and the cost of complexity (PDF). Evolution, 54, 13–20.CrossRefGoogle Scholar
  58. Pimm, S. L. (1984). The complexity and stability of ecosystems. Nature, 307, 321–326.CrossRefGoogle Scholar
  59. Pimm, S. (2002). Food webs (2nd ed.). Chicago: University of Chicago Press.Google Scholar
  60. Pradeu, T. (2012). The limits of the self: Immunology and biological identity. Oxford: Oxford University Press.CrossRefGoogle Scholar
  61. Revilla-i-Domingo, I., Domingo, R., & Davidson, E. (2003). Developmental gene network analysis. International Journal of Developmental Biology, 47, 695–703.Google Scholar
  62. Romano, L. A., & Gray, G. A. (2003). Conservation of endo 16 expression in sea urchins despite evolutionary divergence in both cis and trans-acting components of transcriptional regulation. Development, 130(17), 4187–4199.CrossRefGoogle Scholar
  63. Sameer, S., Bajikar, S. S., & Janes, K. A. (2012). Multiscale models of cell signaling. Annals of Biomedical Engineering, 40, 2319–2327.CrossRefGoogle Scholar
  64. Sarkar, S. (1999). From the Reaktionsnorm to the adaptive norm: The reaction norm, 1909–1960. Biology and Philosophy, 14, 235–252.CrossRefGoogle Scholar
  65. Scheiner, S. M. (1993). Genetics and evolution of phenotypic plasticity. Annual Re- view of Ecology and Systematics, 24, 35e68.Google Scholar
  66. Schuster, P. (2002). A testable genotype-phenotype map: Modeling evolution of RNA molecules. In M. Lässig & A. Valleriani (Eds.), Lecture notes in physics, 585 (pp. 55–81). Dordrecht: Springer.Google Scholar
  67. Schuster, P., Fontana, W., Stadler, P. F., & Hofacker, I. (1994). From sequences to shapes and back: A case study in RNA secondary structures. Proceedings of the Royal Society of London Series B, 255, 279–284.CrossRefGoogle Scholar
  68. Simon, H. (1969). The sciences of the artificial. Cambridge: MIT Press.Google Scholar
  69. Sniegowski, P. D., Gerrish, P. J., Johnson, T., & Shaver, A. (2000). The evolution of mutation rates: Separating causes from consequences. Bioessays, 22, 1057–1066.CrossRefGoogle Scholar
  70. Solé, R., & Valverde, S. (2006). Are network motifs the spandrels of cellular complexity? TREE, 21(8), 419–422.Google Scholar
  71. Solé, R., & Valverde, S. (2008). Spontaneous emergence of modularity in cellular networks. Journal of the Royal Society Interface, 5, 129–133.CrossRefGoogle Scholar
  72. Stadler, B., & Stadler, P. (2004). The topology of evolutionary biology. In C. Ciobanu (Ed.), Modeling in molecular biology. Natural computing series (pp. 267–286). Dordrecht: Springer.Google Scholar
  73. Stadler, P., Stadler, P., Wagner, G., & Fontana, W. (2001). The topology of the possible: formal spaces underlying patterns of evolutionary change. Journal of Theoretical Biology, 213(2), 241–274.CrossRefGoogle Scholar
  74. Strogatz, S. (2001). Exploring complex networks. Nature, 410, 268–276.CrossRefGoogle Scholar
  75. Sultan, S. E., & Stearns, S. C. (2005). Environmentally contingent variation: Phenotypic plasticity and norms of reaction. In B. Hallgrimsson & B. Hall (Eds.), Variation. Boston: Elsevier Academic Press.Google Scholar
  76. Taddei, F., Matic, I., & Radman, M. (1995). Cyclic AMP-dependent SOS induction and mutagenesis in resting bacterial populations. Proceedings of the National Academy of Sciences of the United States of America, 92, 11736–11740.CrossRefGoogle Scholar
  77. Tilman, D. (1996). Biodiversity: Population versus ecosystem stability. Ecology, 77(2), 350–363.CrossRefGoogle Scholar
  78. Van Nimwegen, E., Crutchfield, J., & Huynen, M. (1999). Neutral evolution of mutational robustness. Proceedings of the National Academy of Sciences of the United States of America, 96(17), 9716–9720.CrossRefGoogle Scholar
  79. Via, S., & Lande, R. (1985). Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution, 39, 505–522.CrossRefGoogle Scholar
  80. Waddington, C. (1940). Organisers and genes. Cambridge: Cambridge University Press.Google Scholar
  81. Wagner, A. (2005a). Robustness and evolvability in living systems. Princeton: Princeton University Press.Google Scholar
  82. Wagner, A. (2005b). Distributed robustness versus redundancy as causes of mutational robustness. Bioessays, 27, 176–188.CrossRefGoogle Scholar
  83. Wagner, G., & Altenberg, L. (1996). Complex adaptations and the evolution of evolvability. Evolution, 50(3), 967–976.CrossRefGoogle Scholar
  84. Walsh, D. (2015). Variance, invariance and statistical explanation. Erkenntnis, 80(3), 469–489.CrossRefGoogle Scholar
  85. Watts, D. (2003). Six degrees of separation. New York: Norton.Google Scholar
  86. Watts, D. J., & Strogatz, S. H. (1998). Collective dynamics in “small-world” networks. Nature, 393, 440–442.CrossRefGoogle Scholar
  87. West-Eberhard, M. J. (2003). Developmental plasticity and evolution. Oxford: Oxford University Press.Google Scholar
  88. Williams, G. C. (1975). Sex and evolution. Princeton: Princeton University Press.Google Scholar
  89. Winther, R. (2011). Part-whole science. Synthese, 178, 397–427.CrossRefGoogle Scholar
  90. Woodward, J. (2013). II–Mechanistic explanation: Its scope and limits. Aristotelian Society Supplementary, 87(1), 39–65.CrossRefGoogle Scholar
  91. Wright, L. (1973). Functions. Philosophical Review, 85, 70–86.Google Scholar
  92. Wright, S. (1932). « The roles of mutation, inbreeding, crossbreeding, and selection in evolution » Proceedings of the sixth international congress on genetics (pp. 355–366).Google Scholar
  93. Yodzis, P. (1989). Introduction to theoretical ecology. New York: Harper & Row.Google Scholar

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Authors and Affiliations

  • Philippe Huneman
    • 1
  1. 1.Institut d’Histoire et de Philosophie des Sciences et des TechniquesCNRS/Université Paris I SorbonneParisFrance

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