Abstract
According to the Modern Synthesis (MS), population genetics, as the science of the dynamics of changing allele frequencies in a population, is the core of evolutionary biology since it explains the arising of adaptations by cumulative selection. Its scale is microevolution, namely, evolution of the population of one species within a timescale not too large, defined by a small window of variations and environmental changes. Microevolution constrats with macroevolution, that is, evolution above the level of speciation – such as the extinction or emergence of species and clades – which involves a longer timescale and therefore may assume large environmental changes. MS claimed that macroevolution is not different from macroevolution. This “extrapolationist” thesis formulated by Simpson has been challenged for three decades: by the “punctuated equilibrium” thesis, and recently by Evo-Devo. Here I question the reasons why the extrapolationist thesis is threatened by advances in paleobiology and evolutionary developmental theory. The paper essentially distinguishes between biological and mathematical reasons why there could be principled differences between microevolution and macroevolution. The former concern the nature of variation, which fuels natural selection: whether it’s only made up by mutations and sexual recombination, or whether other developmental features should account for phenotypic variation; it ultimately relies on topological features of the genotype-phenotype maps. Mathematical reasons concern the modeling of chance events in microevolution: at larger timescales, models of chance (such as Gaussian distribution of fluctuations) may not be any more justified, and other models would be required, though at microevolutionary timescales all models would be in practice equivalent. This argument will be applied to recent evolutionary research on extinction time. It appeals to the distinction made by mathematician Mandelbrot between “wild randomness” and “mild randomness” as two distinct structures of randomness. I conclude by showing that the mathematical differences between micro and macroevolution are more general, and therefore may challenge the extrapolation thesis even if empirical facts do not support the biological differences.
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- 1.
For example Ernst Mayr is one of the founders of the Synthesis, and one of his major achievements is arguably the elaboration of a model of speciation focusing on the mechanisms of “reproductive isolation” (Mayr 1963).
- 2.
- 3.
An allele is the variable form of a given gene . A genotype is the whole or a given part of the genetic information of an individual.
- 4.
The phenotype is the set of observable characters of an individual.
- 5.
Proximity in adaptive terms – technically, it means analogies rather than homologies. The quotation below by Dobzhansky provides examples.
- 6.
See comments in Amundson (2005).
- 7.
Dobzhansky (1951) writes: “Experience shows, however, that there is no way toward understanding of the mechanisms of macroevolutionary changes, which require time on geological scales, other than through understanding of microevolutionary processes observable within the span of a human lifetime, often controlled by man’s will, and sometimes reproducible in laboratory experiments.”
- 8.
Eldredge (1971) anticipated some of the radical claims made in Eldredge and Gould (1972), especially by studying an allopatric -speciation based model accounting for phylogenetic patterns that would yield non-gradual evolution . I thank Alexandre Peluffo for having brought this paper to my attention.
- 9.
Notice also that discontinuous change was already acknowledged by Simpson (1944) who named it “quantum evolution ”. The point was that according to him, even if in principle plausible, quantum evolution was not the rule in nature and only concerned rare and rapid diversification and abrupt transition to different “adaptive zones”. Simpson reacted very harshly to the punctuated equilibria thesis, as it is documented by his private correspondence with Gould (Cain 2009), since he objected strongly to the claim of novelty from the authors.
- 10.
As he wrote in retrospect: “punctuated equilibria, which at first sight, seem to support saltationism and discontinuity, are in fact strictly populational phenomena, and therefore gradual (Mayr 1963). They are in no respect whatsoever in conflict with the conclusions of the evolutionary synthesis” (Mayr 2001, p. 298).
- 11.
My emphasis; notice how this contradicts what Dobzhansky says about the only way to address macroevolution .
- 12.
“Regulatory changes in the timing of complex ontogenetic programs seem far more promising and potentially rapid, in conformity with our punctuational predilections. (…) We are pleased that some recent molecular evidence, based on regulatory rather than structural gene changes, supports our model” (Gould and Eldredge 1977, p. 138)
- 13.
The class of bilaterian animals includes all animals showing some symmetry, which encompasses both deuterostomes and protostomes.
- 14.
Even though some biologists designed powerful models that still ascribe stabilizing selection a major role in this, e.g. Eldredge et al. (2005).
- 15.
Except purely physical constraints like gravity, but here we talk of genetic constraints, or developmental constraints bearing on genetic systems (e.g. Wake 1991).
- 16.
Tempo and modes are the concepts Simpson (1944) introduced to address evolutionary change. The tempo is the rate of evolution of something, for instance the amount of change per million years in a given character . The mode is, more generally, the way evolution occurs in changing populations, and it’s not only quantitative (unlike tempo): for instance, “quantum evolution” and “gradual evolution” are modes of evolution.
- 17.
As in the above Valentine and Jablonski (2003) quote about developmental processes impinging on macroevolution .
- 18.
Remember, the genotypes are dots in the space; the whole reasoning assumes that we deal with discrete sets.
- 19.
See also Wilkins and Godfrey-Smith (2009) on zooming in and out landscapes.
- 20.
On this program see Ruse and Sepkoski (2011), Huss (2004).
- 21.
There is a large controversy over whether natural selection maximizes population fitness, initiated by Fisher (1930) and his “fundamental theorem of natural selection”, and still going on now, but this is not the place to develop it. See Grafen (2007), Huneman (2014a) for a contemporary defense of the view, and Lehmann and Rousset (2014) for a critique. In the current context it’s enough to indicate a link between selection and directionality: if selection drives microevolution , then in many cases we can expect a maximal (inclusive) fitness phenotype , and in even more cases we can predict the outcome, even if it’s not a fitness maximizing outcome (for instance because the genetic structure prevents this maximization, even if the genotypic frequencies under selection are predictable).
- 22.
This extinction was indeed massively studied, especially because of the controversy about the causes of the disparition of the dinosaurs, which was revivified by the hypothesis of an asteroid impact, elaborated by Luis Alvarez in the 80s - an asteroid often later identified with the meteor responsible of the Chicxulub crater in Yucatan. We know that in no sense were the dinosaurs groups’ diversity declining just before the extinction.
- 23.
In practice, things are not always like this, and the effects of taxes, in particular, may hugely impinge on this distribution (happily).
References
Amundson, R. 2005. The changing role of the embryo in evolutionary thought. Cambridge: Cambridge University Press.
Bateson, P. 2017. Evolutionary theory evolving. In Challenging the modern synthesis: Development, adaptation and inheritance, ed. P. Huneman and D. Walsh. New-York: Oxford University Press.
Beatty, J. 1994. Chance and natural selection. Philosophy of Science 51 (2): 183–211.
———. 1995. The evolutionary contingency thesis. In Concepts, theories, and rationality in the biological sciences, ed. G. Wolters and J.G. Lennox. Pittsburgh: University of Pittsburgh Press.
———. 2006. Replaying life’s tape. Journal of Philosophy 103: 336–362.
———. 2016. The creativity of natural selection? Part I: Darwin, Darwinism, and the mutationists. Journal of the History of Biology. doi:10.1007/s10739-016-9456-5.
Bell, G., and S. Collins. 2008. Adaptation, extinction and global change. Evolutionary Applications 1: 3–16.
Box, G.E.P., W.G. Hunter, and J.S. Hunter. 1978. Statistics for experimenters. New York: Wiley.
Burger, R., and M. Lynch. 1995. Evolution and extinction in a changing environment: A quantitative-genetic analysis. Evolution 49: 151–163.
Burian, R.M. 1994. Dobzhansky on evolutionary dynamics: Some questions about his Russian background. In The evolution of Theodosius Dobzhansky, ed. M.B. Adams. Princeton University Press: Princeton.
Cain, J. 2009. Ritual Patricide: Why Stephen Jay Gould assassinated George Gaylord Simpson. In The paleobiological revolution, ed. M. Ruse and D. Sepkoski, 345–363. Chicago: University of Chicago Press.
Cheetham, A.H. 1986. Tempo of evolution in a Neogene bryozoan: Rates of morphologic change within and across species boundaries. Paleobiology 12 (2): 190–202.
Chevin, L.M., and R. Lande. 2010. When do adaptive plasticity and genetic evolution prevent extinction of a density-regulated population? Evolution 64: 1143–1150.
Chevin, L.-M., R. Lande, and G.M. Mace. 2010. Adaptation, plasticity, and extinction in a changing environment: Towards a predictive theory. PLoS Biol 8 (4): e1000357.
Conway-Morris, S. 1998. The crucible of creation: The Burgess shale and the rise of animals. Oxford: Oxford University Press.
———. 2010. Evolution: Like other science it is predictable. Philosophical Transactions of the Royal Society, B: Biological Sciences 365 (1537): 133–145.
Coyne, R., N.H. Barton, and M. Turelli. 1997. Perspective: A critique of Sewall Wright’s shifting balance theory of evolution. Evolution 51: 643–671.
Darwin, C. 1859. The origin of species. London: John Murray.
Davidson, E.H. 1986. Gene activity in early development. Orlando: Academic Press.
Davidson, E., and D. Erwin. 2006. Gene regulatory networks and the evolution of animal body plans. Science 311 (5762): 796–800.
Dawkins, R. 1982. The extended phenotype. Oxford: Oxford University Press.
Dennett, D. 1995. Darwin’s dangerous idea. New York: Simons & Shuster.
Depew, D. 2017. Natural selection, adaptation, and the recovery of development. In Challenging the modern synthesis: Development, adaptation and inheritance, ed. P. Huneman and D. Walsh. New York: Oxford University Press.
Devictor, V., C. van Swaay, T. Brereton, L. Brotons, D. Chamberlain, J. Heliölä, S. Herrando, R. Julliard, M. Kuussaari, Å. Lindström, J. Reif, D.B. Roy, O. Schweiger, J. Settele, C. Stefanescu, A. Van Strien, C. Van Turnhout, Z. Vermouzek, M. WallisDeVries, I. Wynhoff, and F. Jiguet. 2012. Differences in the climatic debts of birds and butterflies at a continental scale. Nature Climate Change 2: 121–124.
Dobzhansky, T. 1951. Genetics and the origin of species, Columbia University Biological Series. 3rd revised ed. New York: Columbia University Press.
Eldredge, N. 1971. The allopatric model and phylogeny in Paleozoic invertebrates. Evolution 25 (1): 156–167.
———. 1989. Macroevolutionary dynamics: Species, niches and adaptive peaks. New York: McGraw-Hill.
Eldredge, N., and S.J. Gould. 1972. Punctuated equilibria: An alternative to phyletic gradualism. In Models of paleobiology, ed. T.J. Schopf. San Francisco: Freeman Cooper.
Eldredge, N., J. Thompson, P. Brakefield, S. Gavrilets, D. Jablonski, J. Jackson, R. Lenski, B. Lieberman, M. McPeek, and W. Miller. 2005. The dynamics of evolutionary stasis. Paleobiology 31 (S2): 133–145.
Erwin, D. 2000. Macroevolution is more than repeated rounds of microevolution. Evolution & Development 2 (2): 78–84.
Estes, S., and S. Arnold. 2007. Resolving the paradox of stasis: Models with stabilizing selection explain evolutionary divergence on all timescales. American Naturalist 169: 227–244.
Fisher, R. 1930. The genetical theory of natural selection. London: Oxford University Press.
Foote, M. 2003. Origination and extinction through the Phanerozoic: A new approach. Journal of Geology 111: 125–148.
Ford, E.B. 1975. Ecological genetics. London: Chapman and Hall.
Frank, S.A., and M. Slatkin. 1992. Fisher's fundamental theorem of natural selection. Trends in Ecology and Evolution 7:92–95.
Gavrilets, S. 1999. A dynamical theory of speciation on holey adaptive landscapes. American Naturalist 154: 1–22.
Gayon, J. 1998. Darwinism’s struggle for survival: Heredity and the hypothesis of natural selection. Trans. M. Cobb. Cambridge, MA: Cambridge University Press.
Gillespie, J. 2004. Population genetics. New York: Oxford University Press.
Gould, S.J. 1977. Ontogeny and phylogeny. Cambridge, MA: Harvard University Press.
———. 1989. Wonderful life. The Burgess shale and the nature of history. New York: Norton.
———. 2002. The structure of evolutionary theory. Chicago: University of Chicago Press.
Gould, S.J., and N. Eldredge. 1977. Punctuated equilibria: The tempo and mode of evolution reconsidered. Paleobiology 3: 115–151.
Gould, S.J., and E. Lloyd. 1999. Individuality and adaptation across levels of selection: How shall we name and generalize the unit of Darwinism? PNAS, Proceedings of the National Academy of Sciences 96: 11904–11909.
Grafen, A. 2007. The formal Darwinism project: A mid-term report. Journal of Evolutionary Biology 20: 1243–1254.
Grantham, T. 2007. Is macroevolution more than successive rounds of microevolution ? Palaeontology 50 (1): 75–85.
Hansen, T., and D. Houlé. 2004. Evolvability, stabilizing selection, and the problem of stasis. In Phenotypic integration: Studying the ecology and evolution of complex phenotypes, ed. M. Pigliucci and K.A. Preston, 130–150. Oxford: Oxford University Press.
Hastings, A., and J. Melbourne. 2008. Extinction risk depends strongly on factors contributing to stochasticity. Nature 454: 100–103.
Hubbell, S.P. 2001. The unified neutral theory of biodiversity and biogeography. Princeton University Press: Princeton.
———. 2009. The neutral theory of biodiversity and biogeography and Stephen Jay Gould. Paleobiology 31 (2): 122–132.
Huneman, P. 2010a. Assessing the prospects for a return of organisms in evolutionary biology. History and Philosophy of the Life Sciences 32 (2/3): 341–372.
———. 2010b. Topological explanations and robustness in biological sciences. Synthese 177: 213–245.
———. 2014a. Formal Darwinism and organisms in evolutionary biology: Answering some challenges. Biology and Philosophy 29: 271–279.
———. 2014b. Selection. In Handbook of evolutionary thinking in the sciences, ed. T. Heams, P. Huneman, G. Lecointre, and M. Silberstein. Dordrecht: Springer.
———. 2015. Inscrutability and the opacity of selection and drift: Distinguishing epistemic and metaphysical aspects. Erkenntnis 80: 491–518.
———. 2017. Why would we call for a new evolutionary synthesis? The variation issue and the explanatory alternatives. In Challenging the modern synthesis: Development, adaptation and inheritance, ed. P. Huneman and D. Walsh. New York: Oxford University Press.
Huneman, P., and D. Walsh. 2017. Challenging the modern synthesis: Development, adaptation and inheritance. New York: Oxford University Press.
Hunt, G., and M. Carrano. 2010. Models and methods for analyzing phenotypic evolution in lineages and clades. Paleontological Society Papers 16: 245–269.
Hunt, G., M. Hopkins, and S. Lidgard. 2015. Simple versus complex models of trait evolution and stasis as a response to environmental change. Proceedings of the National Academy of Sciences of the United States of America 112: 4885–4890.
Huss, J. 2004. Experimental reasoning in non-experimental science. PhD Dissertaton, The University of Chicago.
———. 2009. The shape of evolution: The MBL model and clade shape. In The paleobiological revolution, ed. M. Ruse and D. Sepkoski, 326–345. Chicago: University of Chicago Press.
Jablonka, E., and G. Raz. 2009. Transgenerational epigenetic inheritance: Prevalence, mechanisms, and implications for the study of heredity and evolution. Quarterly Review of Biology 84: 131–176.
Jablonski, D. 2000. Micro- and macroevolution: scale and hierarchy in evolutionary biology and paleobiology. Paleobiology 26(Suppl. to No. 4): 15–52.
———. 2001. Lessons from the past: Evolutionary impacts of mass extinctions. Proceedings of the National Academy of Sciences of the United States of America 98: 5393–5398.
———. 2004. Extinction: Past and present. Nature 427: 589.
———. 2005. Mass extinctions and macroevolution. Paleobiology 31(Suppl. to No. 2): 192–210.
———. 2007. Scale and hierarchy in macroevolution. Palaeontology 50: 87–109.
———. 2008a. Species selection: Theory and data. Annual Review of Ecology, Evolution, and Systematics 39: 501–524.
———. 2008b. Biotic interactions and macroevolution: Extensions and mismatches across scales and levels. Evolution 62: 715–739.
———. 2009. Paleontology in the twenty-first century. In The paleobiological revolution, ed. M. Ruse and D. Sepkoski, 471–517. Chicago: University of Chicago Press.
Jablonski, D., and J.J. Sepkoski. 1996. Paleobiology, community ecology, and scales of ecological pattern. Ecology 77: 1367–1378.
Kaplan, J. 2008. The end of the adaptive landscape metaphor? Biology and Philosophy 23: 625–638.
———. 2009 The paradox of stasis and the nature of explanations in evolutionary biology. Philosophy of Science 76 (5): 797–808.
Kauffman, S. 1993. The origins of order: Self-organization and selection in evolution. New York: Oxford University Press.
Kettlewell, H.D.B. 1955. Selection experiments on industrial melanism in the Lepidoptera. Heredity 9: 323–342.
Kimura, M. 1983. The neutral theory of molecular evolution. Cambridge: Cambridge University Press.
Kirschner, M., and J. Gerhart. 2005. The plausibility of life: Resolving Darwin’s Dilemma. New Haven: Yale University Press.
Laland, K., T. Uller, M. Feldman, L. Sterelny, G.B. Müller, A. Moczek, E. Jablonka, and J. Odling-Smee. 2014. Does evolutionary theory need a rethink? Yes: Urgently. Nature 514: 161–164.
Lande, R. 1988. Genetics and demography in biological conservation. Science 241: 1455–1460.
Lande, R., and S.H. Orzack. 1988. Extinction dynamics of age-structured populations in a fluctuating environment. PNAS 85: 7418–7421.
Lehmann, L., and F. Rousset. 2014. Fitness, inclusive fitness and optimization. Biology and Philosophy 29: 181–195.
Lenski, R., and M. Travisano. 1994. Dynamics of adaptation and diversification: A 10,000-generation experiment with bacterial populations. PNAS 91: 6808–6814.
Lynch, M., and R. Lande. 1993. Evolution and extinction in response to environmental change. In Biotic interactions and global change, ed. P. Kareiva, J. Kingsolver, and R. Huey, 234–250. Sunderland: Sinauer.
Mandelbrot, B. 1997. Fractals and scaling in finance: Discontinuity, concentration, risk. New York: Springer.
Matthen, M. 2009. Drift and “Statistically abstractive explanations”. Philosophy of Science 76: 464–487.
Maynard Smith, J., R. Burian, S. Kauffman, P. Alberch, J. Campbell, B. Goodwin, R. Lande, D. Raup, and L. Wolpert. 1985. Developmental constraints and evolution. Quarterly Review of Biology 60: 265–287.
Mayr, E. 1963. Animal, species and evolution. Cambridge, MA: The Belknap Press at Harvard University Press.
———. 2001. What evolution is. New-York: Basic Books.
Mc Shea, D. 1994. Mechanisms of large-scale evolutionary trends. Evolution 48 (6): 1747–1763.
———. 2005. The evolution of complexity without natural selection: A possible large-scale trend of the fourth kind. Paleobiology 31 (2): 146–156.
Millstein, R.L. 2002. Are random drift and natural selection conceptually distinct? Biology and Philosophy 17 (1): 33–53.
———. 2009. Concepts of drift and selection in ‘The Great Snail Debate’ of the 1950s and early 1960s. In Descended from Darwin: Insights into the history of evolutionary studies, 1900–1970, ed. J. Cain and M. Ruse, 271–298. Philadelphia: American Philosophical Society.
Müller, G., and S. Newman 2005. The innovation triad: An evo-devo agenda. Journal of Experimental Zoology 304(B6): 487–503
Nitecki, M., and A. Hoffman. 1987. Neutral models in biology. Oxford: Oxford University Press.
Pagel, M., C. Venditti, and A. Meade. 2006. Large punctuational contribution of speciation to evolutionary divergence at the molecular level. Science 314: 119–121.
Pigliucci, M., and G. Müller. 2011. Evolution: The extended synthesis. Cambridge, MA: MIT Press.
Plutynski, A. 2007. Drift: A historical and conceptual overview. Biological Theory 2 (2): 156–167.
Raup, D. 1994. The role of extinction in evolution. Proceedings of the National Academy of Sciences of the United States of America 91 (15): 6758–6763.
Raup, D., and J. Sepkoski. 1984. Periodicity of extinctions in the geologic past. Proceedings of the National Academy of Sciences of the United States of America 81 (3): 801–805.
Raup, D.M., S.J. Gould, T.J.M. Schopf, and D. Simberloff. 1973. Stochastic models of phylogeny and the evolution of diversity. Journal of Geology 81: 525–542.
Ridley, M. 2004. Evolution. Cambridge: Blackwell.
Simpson, G.G. 1944. Tempo and mode in evolution. Columbia classics in evolution. Reprint ed. New York: Columbia University Press.
Solé, R. 2002. Modelling macroevolutionary patterns: An ecological perspective. In Lecture notes in physics 585, ed. M. Lassig and A. Valleriani, 312–337. Berlin: Springer.
Stanley, S.M., and X. Yang. 1987. Approximate evolutionary stasis for bivalve morphology over millions of years: A multivariate, multilineage study. Paleobiology 13 (2): 113–139.
Sterelny, K. 2007. Dawkins Vs Gould: Survival of the fittest. Cambridge: Icon Books.
Turner, D. 2015. Historical contingency and the explanation of evolutionary trends. In Biological explanation: An enquiry into the diversity of explanatory patterns in the life sciences, ed. C. Malaterre and P.A. Braillard, 73–90. Dordrecht: Springer.
Valentine, J.W., and D. Jablonski. 2003. Morphological and developmental macroevolution: A paleontological perspective. International Journal of Developmental Biology 47: 517–522.
Valentine, J.W., D. Jablonski, and D.H. Erwin. 1999. Fossils, molecules and embryos: New perspectives on the Cambrian explosion. Development 126: 851–859.
Wake, D.B. 1991. Homoplasy: The result of natural selection, or evidence of design limitations? The American Naturalist 138: 543–567.
Walsh, D.M. 2015. Organisms, agency, and evolution. Cambridge: Cambridge University Press.
Wilkins, J., and P. Godfrey-Smith. 2009. Adaptationism and the adaptive landscape. Biology and Philosophy 24: 199–214.
Williams, G.C. 1992. Natural selection: Domains, levels and challenges. Oxford: Oxford University Press.
Williamson, P.G. 1981. Palaeontological documentation of speciation in Cenozoic molluscs from Turkana Basin. Nature 293: 437–443.
Winther, R.G. 2006. Fisherian and Wrightian perspectives in evolutionary genetics and model-mediated imposition of theoretical assumptions. Journal of Theoretical Biology 240: 218–232.
Wray, G.A., H.E. Hoekstra, D.J. Futuyma, R.E. Lenski, T.F.C. Mackay, D. Schluter, and J.E. Strassmann. 2014. Does evolutionary theory need a rethink? No, all is well. Nature 514: 161–164.
Wright, S. 1932. The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proceedings of the sixth annual congress of genetics 1: 356–366.
Acknowledgements
The author warmly thanks Jean Gayon, Annick Lesne, Scott Lidgard and Mael Montevil, for helpful discussions, as well as audiences at the ISHPSSB 2015 meeting in Montréal. He is also grateful to Andrew Mc Farland for a thorough language check of the manuscript, and to Sébastien Dutreuil and Christophe Bouton for criticisms and suggestions on a first draft. This work has been done with the support of the grant ANR 13 BSH3 0007 “Explabio”.
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Huneman, P. (2017). Macroevolution and Microevolution: Issues of Time Scale in Evolutionary Biology. In: Bouton, C., Huneman, P. (eds) Time of Nature and the Nature of Time. Boston Studies in the Philosophy and History of Science, vol 326. Springer, Cham. https://doi.org/10.1007/978-3-319-53725-2_14
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