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Limb, tooth, beak: Three modes of development and evolutionary innovation of form

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Abstract

The standard model of evolutionary change of form, deriving from Darwin’s theory via the Modern Synthesis, assumes a gradualistic reshaping of anatomical structures, with major changes only occurring by many cycles of natural selection for marginal adaptive advantage. This model, with its assertion that a single mechanism underlies both micro- and macroevolutionary change, contains an implicit notion of development which is only applicable in some cases. Here we compare the embryological processes that shape the vertebrate limb bud, the mammalian tooth and the avian beak. The implied notion of development in the standard evolutionary picture is met only in the case of the vertebrate limb, a single-primordium organ with morphostatic shaping, in which cells rearrange in response to signalling centres which are essentially unchanged by cell movement. In the case of the tooth, a single-primordium organ with morphodynamic shaping in which the strengths and relationships between signalling centres is influenced by the cell and tissue movements they induce, and the beak, in which the final form is influenced by the collision and rearrangement of multiple tissue primordia, abrupt appearance of qualitatively different forms (i.e. morphological novelties) can occur with small changes in system parameters induced by a genetic change, or by an environmental factor whose effects can be subsequently canalized genetically. Bringing developmental mechanisms and, specifically, the material properties of tissues as excitable media into the evolutionary picture, demonstrates that gradualistic change for incremental adaptive advantage is only one of the possible modes of morphological evolution.

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Notes

  1. We emphasize that our limb example only pertains to the shaping of the bud before the skeleton differentiates, a developmental episode in every tetrapod embryo. The skeleton itself is, of course, a set of discrete elements that emerge in a partly discontinuous fashion. Subtle changes in limb bud shape, as well as in the functioning of molecules directly involved in its formation, as described above, can have sharply divergent effects on the skeletal pattern. Specifically, due to the properties of its underlying Turing-type patterning mechanism (Turing 1952; Newman and Frisch 1979), the skeleton undergoes discontinuous jumps between numbers and sizes of elements in response to continuous changes in the shape and other parameters of the developing limb bud (Miura et al. 2006; Sheth et al. 2012).

  2. Note that the model of Mallarino et al. (2011) is based on a single primordium, the frontonasal mass, whereas the model of Wu et al. (2006) takes into account the multiprimordium nature of the bird beak. However, the latter model is exclusively based on intrinsic growth patterns of the facial primordia, with no mention of the extrinsic budding interactions in the generation of the beak form.

  3. While the early developmental events would determine the general shape of the upper beak, its adult form will also depend on processes that take place at later ontogenetic stages (patterning and growth of skeletal tissues) or during the juvenile phase (by the active use of the jaw muscles) (Genbrugge et al. 2011). The growth of the rhamphotheca, the sheet of cornified epithelium covering the beak, also influences the adult beak shape (Genbrugge et al. 2012).

  4. There have been exceptions. The late John Maynard Smith, for instance, described himself as ‘open-minded about the possibility that development may impose discontinuous constraints on the pattern of phenotypic variation’, concluding that ‘[i]f so, mutations of large phenotypic effect may sometimes initiate new evolutionary departures’ (Maynard Smith 1983 p 19). Although advanced three decades ago by one of the most highly regarded theorists of the Modern Synthesis, this notion, which may have even greater relevance to the less canalized forms of earlier periods of evolution than to present-day organisms (Newman 2012), has remained marginal to mainstream evolutionary theory.

  5. A recent study of the formation of head crests in pigeons shows this unequivocally to have occurred (Shapiro et al. 2013). Darwin was familiar with such abrupt morphological changes in populations of domesticated pigeons, but considered them ‘sports’ that, by his theory, could not have contributed to the evolution of this trait in the wild (Darwin 1859).

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Acknowledgements

We thank Vidyanand Nanjundiah for organizing the Almora workshop on ‘Individuals and Groups’, where one of us (M L-M) presented a preliminary version of this paper. We also thank V Nanjundiah and three reviewers for incisive criticism of an earlier draft. We acknowledge support from the European Commission (Marie Curie Fellowship PIOF-GA-2008-219676) (M L-M) and the National Science Foundation (SAN).

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  1. University of Manchester, Manchester, UK

    Marta Linde-Medina

  2. New York Medical College, Valhalla, NY, USA

    Marta Linde-Medina & Stuart A Newman

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  1. Marta Linde-Medina
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Correspondence to Marta Linde-Medina or Stuart A Newman.

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[Linde-Medina M and Newman SA 2014 Limb, tooth, beak: Three modes of development and evolutionary innovation of form. J. Biosci. 39 1–13] DOI 10.1007/s12038-013-9355-2

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Linde-Medina, M., Newman, S.A. Limb, tooth, beak: Three modes of development and evolutionary innovation of form. J Biosci 39, 211–223 (2014). https://doi.org/10.1007/s12038-013-9355-2

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