EvoDevo as a Motley Aggregation: Local Integration and Conflicting Views of Genes During the 1980s

Abstract

Although there are many historical and philosophical analyses of evolutionary developmental biology (EvoDevo), its development in the 1980s, when many individual or collective attempts to synthesize evolution and development were made, has not been examined in detail. This article focuses on some interdisciplinary studies during the 1980s and argues that they had important characteristics that previous historical and philosophical work has not recognized. First, we clarify how each set of studies from the 1980s integrated the results or approaches from different biological fields, such as paleontology, developmental genetics, comparative morphology, experimental embryology, theoretical developmental biology, and population genetics. Second, after close examination we show that the interdisciplinary studies during the 1980s adopted different and conflicting views of genes, such as developmental-genetic, epigenetic, or population-genetic ones. We conclude that EvoDevo in the 1980s was a motley aggregation of various kinds of local integration. Finally, we discuss the implications of our analysis by comparing these early EvoDevo studies with those of the Modern Synthesis and with the present state of EvoDevo.

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Notes

  1. 1.

    We cannot discuss all of the early interdisciplinary studies for lack of space. We think that the three studies addressed in the subsequent sections sufficiently show that early attempts to synthesize evolution and development were very diverse. Thus, we omitted some important work including Stephen J. Gould’s Ontogeny and Phylogeny (1977), which is thought to have played an important role in the formation of present EvoDevo (e.g., Love 2003; Gilbert and Epel 2009; Arthur 2011), and the work on functional morphology by David Wake, which was examined by some authors (e.g., Love 2003; Griesemer 2013). We also excluded workshops and conferences in the 1980s, such as the Dahlem Workshop on Evolution and Development in 1981, although we agree with authors who emphasize its importance (e.g., Love 2003; Love and Raff 2003; Müller 2007b). In the workshop, biologists from different fields together rethought the relationship between evolution and development (Bonner 1982). Wagner and Laubichler (2004, p. 96) write that it was “widely seen as the ‘official’ starting point of developmental evolution as an intellectual movement.”

  2. 2.

    Paedomorphosis is “the retention of traits characteristic of the juvenile ancestral form by the sexually mature descendant form” (Raff and Kaufman 1983, p. 37).

  3. 3.

    Kaufman’s laboratory played an important role in the discovery of homeobox genes (Scott and Weiner 1984), as did Walter Gehring’s laboratory (McGinnis et al. 1984).

  4. 4.

    This model is now a widely accepted textbook one (e.g., Carroll et al. 2001).

  5. 5.

    They argued: “Much of evolutionary theory has been colored by this prejudice, which mistakes these clock processes or the gradual substitution in a population of an allele encoding one enzyme variant for another as evolution” (Raff and Kaufman 1983, p. 338).

  6. 6.

    The word “epigenetic” here is the adjectival form of the noun “epigenesis,” which is defined as the formation of an organic germ as a new product, with the theory of epigenesis defined as the theory that the germ is brought into existence (by successive accretions), and not merely developed, in the process of reproduction (Haig 2004, p. 1). The adjective “epigenetic” today also refers to the noun “epigenetics,” which has a different meaning from “epigenesis” (Haig 2004, p. 1). For more information on the terms “epigenesis” and “epigenetics,” see Müller and Olson (2003).

  7. 7.

    Alberch, Hall, and Müller did not refer to themselves as a group, and their research has not been grouped together as a single trend. However, we categorize their studies during the 1980s together because they mutually cited one another and shared a critical stance to gene-centered research .

  8. 8.

    This argument is similar to that of Alberch and Gale (1985) on frogs and salamanders, although Hall cited research on whales with hind limbs, wingless chicks, and legless lizards.

  9. 9.

    The structure of the genetic regulatory system is now widely considered to be a network, and far more complicated than a tree structure such as Arthur’s (Davidson 2006).

  10. 10.

    Arthur (1988, p. 14) admitted that there was not necessarily a 1:1 correspondence between the number of heterogeneities and that of acting genes in each stage of development.

  11. 11.

    Although Arthur did not define the term “ill-coadapted,” it seems to refer to a property of an organism with some organs that are not mutually adapted to each other.

  12. 12.

    Arthur gave three possibilities for such simultaneous emergence: “mutations in early germ cell precursor”; “occurrence of a cluster of mutant individuals through ‘horizontal transfer of genetic material via RNA-based viruses’”; and “ordinary germ-cell mutation in ‘maternal effect’ genes” (Arthur 1988, p. 46).

  13. 13.

    This would be possible when the mutants used different resources than the preexisting species (Arthur 1988, pp. 46–47).

  14. 14.

    This final state gave this model the “French flag” name, with each type of differentiated cell represented by a different color (Wolpert 1968, 1969).

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Acknowledgments

Comments given by Rueylin Chen, Lindley Darden, Tetsuji Iseda, and Alan Love have been a great help in writing the manuscript. We are very grateful to Werner Callebaut for giving useful advice to us and so sorry to hear of his sudden passing.

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Correspondence to Yoshinari Yoshida.

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Yoshida, Y., Nakao, H. EvoDevo as a Motley Aggregation: Local Integration and Conflicting Views of Genes During the 1980s. Biol Theory 10, 156–166 (2015). https://doi.org/10.1007/s13752-014-0197-4

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Keywords

  • Biological fields
  • Evolutionary developmental biology (EvoDevo)
  • Integration
  • Synthesis