Abstract
Although classical evolutionary theory, i.e., population genetics and the Modern Synthesis, was already implicitly ‘gene-centred’, the organism was, in practice, still generally regarded as the individual unit of which a population is composed. The gene-centred approach to evolution only reached a logical conclusion with the advent of the gene-selectionist or gene’s eye view in the 1960s and 1970s. Whereas classical evolutionary theory can only work with (genotypically represented) fitness differences between individual organisms, gene-selectionism is capable of working with fitness differences among genes within the same organism and genome. Here, we explore the explanatory potential of ‘intra-organismic’ and ‘intra-genomic’ gene-selectionism, i.e., of a behavioural-ecological ‘gene’s eye view’ on genetic, genomic and organismal evolution. First, we give a general outline of the framework and how it complements the—to some extent—still ‘organism-centred’ approach of classical evolutionary theory. Secondly, we give a more in-depth assessment of its explanatory potential for biological evolution, i.e., for Darwin’s ‘common descent with modification’ or, more specifically, for ‘historical continuity or homology with modular evolutionary change’ as it has been studied by evolutionary developmental biology (evo-devo) during the last few decades. In contrast with classical evolutionary theory, evo-devo focuses on ‘within-organism’ developmental processes. Given the capacity of gene-selectionism to adopt an intra-organismal gene’s eye view, we outline the relevance of the latter model for evo-devo. Overall, we aim for the conceptual integration between the gene’s eye view on the one hand, and more organism-centred evolutionary models (both classical evolutionary theory and evo-devo) on the other.
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Notes
We return to the relevance of intra-organismic and intra-genomic conflict for evo-devo in Sect. 3.4.
References
Agren, J. A. (2013). Selfish genes and plant speciation. Evolutionary Biology, 40, 439–449.
Agren, J. A. (2016). Selfish genetic elements and the gene’s eye view of evolution. Current Zoology, 62, 659–665.
Alberch, P. (1982). The generative and regulatory roles of development in evolution. In D. Mossakowski & G. Roth (Eds.), Environmental adaptations and evolution (pp. 19–35). Stuttgart: Gustav Fisher.
Alberch, P. (1991). From genes to phenotype: Dynamical systems and evolvability. Genetica, 84, 5–11.
Andersson, J. O. (2005). Lateral gene transfer in eukaryotes. CMLS Cellular and Molecular Life Sciences, 62, 1182–1197.
Avise, J. C. (2001). Evolving genomic metaphors: A new look at the language of DNA. Science, 294, 86–87.
Badyaev, A. V. (2009). Evolutionary significance of phenotypic accommodation in novel environments: An empirical test of the Baldwin effect. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364, 1125–1141.
Bateson, P. (2014). New thinking about biological evolution. Biological Journal of the Linnean Society, 112, 268–275.
Bohl, K., Hummert, S., Werner, S., Basanta, D., Deutsch, A., et al. (2014). Evolutionary game theory: Molecules as players. Molecular BioSystems, 10, 3066–3074.
Bourke, A. F. G. (2014). The gene’s-eye view, major transitions and the formal Darwinism project. Biology and Philosophy, 29, 241–248.
Braendle, C., & Flatt, T. (2006). A role for genetic accommodation in evolution? BioEssays, 28, 868–873.
Brigandt, I. (2007). Typology now: Homology and developmental constraints explain evolvability. Biology and Philosophy, 22, 709–725.
Brigandt, I., & Griffiths, P. E. (2007). The importance of homology for biology and philosophy. Biology and Philosophy, 22, 633–641.
Broom, M., & Rychtár, J. (2013). Game-theoretical models in biology. Boca Raton: CRC Press.
Broom, M., & Rychtár, J. (2016). Nonlinear and multiplayer evolutionary games. In F. Thuijsman & F. Wagener (Eds.), Advances in dynamic and evolutionary games: Theory, applications, and numerical methods. Volume 14 of the series Annals of the International Society of Dynamic Games (pp. 95–115). Birkhäuser: Springer.
Burt, A., & Trivers, R. (2006). Genes in conflict: The biology of selfish genetic elements. Cambridge, MA: Belknap Harvard.
Cairns, J. (1975). The cancer problem. Scientific American, 233, 64–78.
Calcott, B., & Sterelny, K. (2011). The major transitions in evolution revisited. Cambridge: MIT Press.
Callebaut, W., Müller, G. B., & Newman, S. A. (2007). The organismic systems approach: EvoDevo and the streamlining of the naturalistic agenda. In R. Sansom & R. Brandon (Eds.), Integrating evolution and development: From theory to practice (pp. 25–92). Cambridge: MIT Press.
Callebaut, W., & Rasskin-Gutman, D. (Eds.). (2005). Modularity: Understanding the development and evolution of natural complex systems. Cambridge: MIT Press.
Carroll, S. B., Grenier, J. K., & Weatherbee, S. D. (2005). From DNA to diversity: Molecular genetics and the evolution of animal design. Malden, MA: Blackwell Publishing.
Clune, J., Mouret, J.-P., & Lipson, H. (2013). The evolutionary origins of modularity. Proceedings of the Royal Society B, 280, 20122863.
Cosmides, L. M., & Tooby, J. (1981). Cytoplasmic inheritance and intragenomic conflict. Journal of Theoretical Biology, 89, 83–129.
Cronin, H. (1991). The ant and the peacock: Altruism and sexual selection from Darwin to today. Cambridge: Cambridge University Press.
Cronin, H. (2005). Adaptation: “A critique of some current evolutionary thought”. The Quarterly Review of Biology, 80, 19–26.
Darwin, C. (1859). On the origin of species by means of natural selection. London: John Murray.
Dawkins, R. (1976). The selfish gene. Oxford: Oxford University Press.
Dawkins, R. (1982). The extended phenotype. Oxford: Oxford University Press.
Dawkins, R. (1986). The blind watchmaker. London: Longman.
Dawkins, R. (1994). Burying the vehicle. Behavioral and Brain Sciences, 17, 616–617.
Dawkins, R. (2004). Extended phenotype—But not too extended. A reply to Laland, Turner and Jablonka. Biology and Philosophy, 19, 377–396.
De Tiège, A., Tanghe, K., Braeckman, J., & Van de Peer, Y. (2014). From DNA- to NA-centrism and the conditions for gene-centrism revisited. Biology and Philosophy, 29, 55–69.
Dobzhansky, T. (1937). Genetics and the origin of species. New York: Columbia University Press.
Dobzhansky, T. (1964). Biology, molecular and organismic. American Zoologist, 4, 443–452.
Doolittle, W. F. (1989). Hierarchical approaches to genome evolution. Canadian Journal of Philosophy, 102, 101–133.
Doolittle, W. F. (1999). Lateral genomics. Trends in Biochemical Sciences, 24, M5–M8.
Doolittle, W. F. (2013). Is junk DNA bunk? A critique of ENCODE. Proceedings of National Academy of Sciences, 110, 5294–5300.
Doolittle, W. F., & Sapienza, C. (1980). Selfish genes, the phenotypic paradigm and genome evolution. Nature, 284, 601–603.
Eberhard, W. G. (1980). Evolutionary consequences of intracellular organelle competition. The Quarterly Review of Biology, 55, 231–249.
Edwards, A. W. F. (2014). R.A. Fisher’s gene-centred view of evolution and the fundamental theorem of natural selection. Biological Reviews, 89, 135–147.
Fedoroff, N. V. (2012). Transposable elements, epigenetics, and genome evolution. Science, 338, 758–767.
Fisher, R. A. (1918). The correlation between relatives on the supposition of Mendelian inheritance. Transactions of the Royal Society of Edinburgh, 52, 399–433.
Fisher, R. A. (1930). The genetical theory of natural selection. Oxford: Oxford University Press.
Gardner, A., & Grafen, A. (2009). Capturing the superorganism: A formal theory of group adaptation. Journal of Evolutionary Biology, 22, 659–671.
Gardner, A., & Welch, J. J. (2011). A formal theory of the selfish gene. Journal of Evolutionary Biology, 24, 1801–1813.
Gilbert, S. F., Opitz, J. M., & Raff, R. A. (1996). Resynthesizing evolutionary and developmental biology. Developmental Biology, 173, 357–372.
Gilbert, S. F., & Sarkar, S. (2000). Embracing complexity: Organicism for the 21st century. Developmental Dynamics, 219, 1–9.
Godfrey-Smith, P. (2009). Darwinian populations and natural selection. NY: Oxford University Press.
Gogarten, J. P., & Townsend, J. P. (2005). Horizontal gene transfer, genome innovation and evolution. Nature Reviews Microbiology, 3, 679–687.
Gokhale, C. S., & Traulsen, A. (2014). Evolutionary multiplayer games. Dynamic Games and Applications, 4, 468–488.
Goldenfeld, N., & Woese, C. (2011). Life is physics: Evolution as a collective phenomenon far from equilibrium. Annual Review of Condensed Matter Physics, 2, 375–399.
Goodwin, B. C. (1982). Development and evolution. Journal of Theoretical Biology, 97, 43–55.
Goodwin, B. C. (1994). How the leopard changed its spots: The evolution of complexity. London: Weidenfeld and Nicolson.
Goodwin, B. C., Kauffman, S., & Murray, J. D. (1993). Is morphogenesis an intrinsically robust process? Journal of Theoretical Biology, 163, 135–144.
Gould, S. J. (1983). What happens to bodies if genes act for themselves? In S. J. Gould (Ed.), Hen’s teeth and horse’s toes (pp. 166–176). New York: Norton.
Gould, S. J. (2002). The structure of evolutionary theory. Cambridge, MA: Harvard University Press.
Gould, S. J., & Lewontin, R. C. (1979). The spandrels of San Marco and the Panglossian paradigm: A critique of the adaptationist programme. Proceedings of the Royal Society of London, Series B: Biological Sciences, 205, 581–598.
Goymer, P. (2008). Natural selection: The evolution of cancer. Nature, 454, 1046–1048.
Gregory, T. R. (2004). Macroevolution, hierarchy theory, and the C-value enigma. Paleobiology, 30, 179–202.
Gregory, T. R., Elliott, T. A., & Linquist, S. (2016). Why genomics needs multilevel evolutionary theory. In N. Eldredge, T. Pievani, E. Serrelli, & I. Tëmkin (Eds.), Evolutionary theory: A hierarchical perspective (pp. 137–150). Chicago: University of Chicago Press.
Griffiths, P. E. (2002). Lost: One gene concept, reward to finder. Biology and Philosophy, 17, 271–283.
Griffiths, P., & Stotz, K. (2013). Genetics and philosophy: An introduction. Cambridge: Cambridge University Press.
Haig, D. (1997). The social gene. In J. R. Krebs & N. B. Davies (Eds.), Behavioural ecology: An evolutionary approach (pp. 284–304). Oxford: Blackwell Publisher.
Haig, D. (2006). Intragenomic politics. Cytogenetic and Genome Research, 113, 68–74.
Haig, D. (2007). Weismann rules! OK? Epigenetics and the Lamarckian temptation. Biology and Philosophy, 22, 415–428.
Haig, D. (2012). The strategic gene. Biology and Philosophy, 27, 461–479.
Haig, D. (2014). Genetic dissent and individual compromise. Biology and Philosophy, 29, 233–239.
Haldane, J. B. S. (1932). The causes of evolution. Princeton: Princeton University Press.
Hall, B. K. (Ed.). (1994). Homology: The hierarchical basis of comparative biology. San Diego: Academic Press.
Hall, B. K. (1998). Evolutionary developmental biology (2nd ed.). Dordrecht: Kluwer.
Hamilton, W. D. (1963). The evolution of altruistic behavior. American Naturalist, 97, 354–356.
Hamilton, W. D. (1964). The genetical evolution of social behaviour. Journal of Theoretical Biology, 7, 1–52.
Higgs, P. G., & Lehman, N. (2014). The RNA world: Molecular cooperation at the origins of life. Nature Reviews Genetics, 16, 7–17.
Hull, D. L. (1980). Individuality and selection. Annual Reviews of Ecology and Systematics, 11, 311–332.
Hurst, G. D. D., & Werren, J. H. (2001). The role of selfish genetic elements in eukaryotic evolution. Nature Reviews Genetics, 2, 597–606.
Huxley, J. S. (1942). Evolution: The modern synthesis. London: Allen and Unwin.
Jablonka, E., & Lamb, M. (2005). Evolution in four dimensions: Genetic, epigenetic, behavioral, and symbolic variation in the history of life. Cambridge, MA: MIT Press.
Jablonka, E., & Raz, G. (2009). Transgenerational epigenetic inheritance: Prevalence, mechanisms, and implications for the study of heredity and evolution. The Quarterly Review of Biology, 84, 131–176.
Jo, B.-S., & Choi, S. S. (2015). Introns: The functional benefits of introns in genomes. Genomics Informatics, 13, 112–118.
Jurka, J., Bao, W., & Kojima, K. K. (2011). Families of transposable elements, population structure and the origin of species. Biology Direct, 6, 44.
Kauffman, S. A. (1983). Developmental constraints: Internal factors in evolution. In B. C. Goodwin, N. Holder, & C. C. Wylie (Eds.), Development and evolution (pp. 195–225). Cambridge: Cambridge University Press.
Kauffman, S. A. (1993). The origins of order: Self-organization and selection in evolution. Oxford: Oxford University Press.
Keeling, P. J., & Palmer, J. D. (2008). Horizontal gene transfer in eukaryotic evolution. Nature Reviews Genetics, 9, 605–618.
Kimura, M. (1983). The neutral theory of molecular evolution. Cambridge: Cambridge University Press.
Kirschner, M., & Gerhart, J. (1998). Evolvability. PNAS, 95, 8420–8427.
Koonin, E. V. (2016). Viruses and mobile elements as drivers of evolutionary transitions. Philosophical Transactions of the Royal Society B, 371, 20150442.
Koonin, E. V., Senkevich, T. G., & Dolja, V. V. (2006). The ancient virus world and evolution of cells. Biology Direct, 1, 29.
Laland, K., Uller, T., Feldman, M., et al. (2014). Does evolutionary theory need a rethink? Nature, 514, 161–164.
Leigh, E. G. (1971). Adaptation and diversity: Natural history and the mathematics of evolution. San Francisco: Freeman.
Lewontin, R. C. (1970). The units of selection. Annual Review of Ecology and Systematics, 1, 1–18.
Lisch, D. (2013). How important are transposons for plant evolution? Nature Reviews Genetics, 14, 49–61.
Lynch, M. (2002). Intron evolution as a population-genetic process. PNAS USA, 99, 6118–6123.
Lynch, M. (2007a). The origins of genome architecture. Sunderland (MA): Sinauer Associates.
Lynch, M. (2007b). The frailty of adaptive hypotheses for the origins of organismal complexity. PNAS, 104, 8597–8604.
Maynard Smith, J. M. (1976). Evolution and the theory of games. American Scientist, 64, 41–45.
Maynard Smith, J. (1982). Evolution and the theory of games. Cambridge: Cambridge University Press.
Maynard Smith, J., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Goodwin, B., et al. (1985). Developmental constraints and evolution. The Quarterly Review of Biology, 60, 265–287.
Maynard Smith, J., & Szathmáry, E. (1995). The major transitions in evolution. Oxford: Oxford University Press.
Mayr, E., & Provine, W. B. (Eds.). (1980). The evolutionary synthesis: Perspectives on the unification of biology. London, MA: Harvard University Press.
Merlo, L. M. F., Pepper, J. W., Reid, B. J., & Maley, C. C. (2006). Cancer as an evolutionary and ecological process. Nature Reviews Cancer, 6, 924–935.
Michod, R. E. (1999). Darwinian dynamics: Evolutionary Transitions in fitness and individuality. Princeton: Princeton University Press.
Moczek, A. P., Sultan, S., Foster, S., Ledón-Rettig, C., Dworkin, I., Nijhout, H. F., et al. (2011). The role of developmental plasticity in evolutionary innovation. Proceedings of the Royal Society of London B: Biological Sciences, 278, 2705–2713.
Newman, S. A., Forgacs, G., & Müller, G. B. (2006). Before programs: The physical origination of multicellular forms. International Journal of Developmental Biology, 50, 289–299.
Newman, S. A., & Müller, G. B. (2010). Morphological evolution: Epigenetic mechanisms. In J. Wiley (Ed.), Encyclopedia of life sciences (ELS). Chichester. New York: Wiley. https://doi.org/10.1002/9780470015902.a0002100.pub2.
Noble, D., Jablonka, E., Joyner, M. J., Müller, G. B., & Omholt, S. W. (2014). Evolution evolves: Physiology returns to centre stage. The Journal of Physiology, 592, 2237–2244.
Nowell, P. C. (1976). The clonal evolution of tumor cell populations. Science, 194, 23–28.
Okasha, S. (2006). Evolution and the levels of selection. Oxford: Oxford University Press.
Okasha, S. (2008). Fisher’s fundamental theorem of natural selection: A philosophical analysis. The British Journal for the Philosophy of Science, 59, 319–351.
Okasha, S. (2012). Social justice, genomic justice and the veil of ignorance: Harsanyi meets Mendel. Economics and Philosophy, 28, 43–71.
Orgel, L. E., & Crick, F. H. C. (1980). Selfish DNA: The ultimate parasite. Nature, 284, 604–607.
Orr, H. A. (1996). Dobzhansky, Bateson, and the genetics of speciation. Genetics, 144, 1331–1335.
Oyama, S., Griffiths, P. E., & Gray, R. D. (Eds.). (2001). Cycles of contingency: Developmental systems and evolution. Cambridge, MA: MIT Press.
Pigliucci, M. (2008). Is evolvability evolvable? Nature Reviews Genetics, 9, 75–82.
Pigliucci, M., & Müller, G. B. (2010). Evolution—The extended synthesis. Cambridge, MA: The MIT Press.
Pigliucci, M., Murren, C. J., & Schlichting, C. D. (2006). Review: Phenotypic plasticity and evolution by genetic assimilation. The Journal of Experimental Biology, 209, 2362–2367.
Queller, D. C. (1997). Cooperators since life began. The Quarterly Review of Biology, 72, 184–188.
Queller, D. C. (2011). A gene’s eye view of Darwinian populations: Review of Peter Godfrey-Smith’s Darwinian populations and natural selection. Biology and Philosophy, 26, 905–913.
Queller, D. C., & Strassmann, J. E. (2009). Beyond society: The evolution of organismality. Philosophical Transactions of the Royal Society B: Biological Sciences, 364, 3143–3155.
Rice, W. R. (2013). Nothing in genetics makes sense except in the light of genomic conflict. Annual Review of Ecology Evolution and Systematics, 44, 217–237.
Sapp, J. (2009). The new foundations of evolution: On the tree of life. New York: Oxford University Press.
Schlosser, G., & Wagner, G. P. (2004). Modularity in development and evolution. Chicago: The University of Chicago Press.
Sterelny, K., & Kitcher, P. (1988). The return of the gene. The Journal of Philosophy, 85, 339–360.
Strassmann, J. E., & Queller, D. C. (2010). The social organism: Congresses, parties, and committees. Evolution, 64, 605–616.
Tanghe, K. B. (2015). Mendel at the sesquicentennial of ‘Versuche über Pflanzen-Hybriden’ (1865): The root of the biggest legend in the history of science. Endeavour, 39, 106–115.
Vrba, E. S., & Eldredge, N. (1984). Individuals, hierarchies and processes: Towards a more complete evolutionary theory. Paleobiology, 10, 146–171.
Waddington, C. H. (1957). The strategy of the genes. New York: Macmillan.
Wagner, G. P. (2007). The developmental genetics of homology. Nature Reviews Genetics, 8, 473–479.
Wagner, G. P. (2014). Homology, genes, and evolutionary innovation. Princeton: Princeton University Press.
Wagner, G. P., & Altenberg, L. (1996). Perspective: Complex adaptations and the evolution of evolvability. Evolution, 50, 967–976.
Weismann, A. (1904). The evolution theory. London: Edward Arnold.
Werren, J. H. (2011). Selfish genetic elements, genetic conflict, and evolutionary innovation. PNAS, 108, 10863–10870.
Werren, J. H., Nur, U., & Wu, C.-I. (1988). Selfish genetic elements. Trends in Ecology and Evolution, 3, 297–302.
West, S. A., Fisher, R. M., Gardner, A., & Kiers, E. T. (2015). Major evolutionary transitions in individuality. PNAS, 112, 10112–10119.
West-Eberhard, M. J. (2003). Developmental plasticity and evolution. Oxford: Oxford University Press.
Williams, G. C. (1966). Adaptation and natural selection: A critique of some current evolutionary thought. Princeton: Princeton University Press.
Wright, S. (1931). Evolution in Mendelian populations. Genetics, 16, 97–159.
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We thank two anonymous reviewers and Staffan Müller-Wille for valuable input into this paper. Preparation of this manuscript was made possible by the Fund for Scientific Research Flanders (FWO), Belgium (Project Number: G001013N).
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De Tiège, A., Van de Peer, Y., Braeckman, J. et al. The sociobiology of genes: the gene’s eye view as a unifying behavioural-ecological framework for biological evolution. HPLS 40, 6 (2018). https://doi.org/10.1007/s40656-017-0174-x
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DOI: https://doi.org/10.1007/s40656-017-0174-x