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Typology now: homology and developmental constraints explain evolvability

Abstract

By linking the concepts of homology and morphological organization to evolvability, this paper attempts to (1) bridge the gap between developmental and phylogenetic approaches to homology and to (2) show that developmental constraints and natural selection are compatible and in fact complementary. I conceive of a homologue as a unit of morphological evolvability, i.e., as a part of an organism that can exhibit heritable phenotypic variation independently of the organism’s other homologues. An account of homology therefore consists in explaining how an organism’s developmental constitution results in different homologues/characters as units that can evolve independently of each other. The explanans of an account of homology is developmental, yet the very explanandum is an evolutionary phenomenon: evolvability in a character-by-character fashion, which manifests itself in phylogenetic patterns as recognized by phylogenetic approaches to homology. While developmental constraints and selection have often been viewed as antagonistic forces, I argue that both are complementary as they concern different parts of the evolutionary process. Developmental constraints, conceived of as the presence of the same set of homologues across phenotypic change, pertain to how heritable variation can be generated in the first place (evolvability), while natural selection operates subsequently on the produced variation.

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  1. As will become clear below, I assume that homologues exist on several levels of organization (also genes and developmental processes can be homologous). Therefore my notions of ‘morphological’ organization and ‘morphological’ structure/unit have a wide scope, including homologues on several levels.

  2. My account also broadly accords with Müller’s (2003) approach to homology and morphological organization, though Müller focuses more on the developmental rather than evolutionary role of homologues.

  3. ‘Evolvability’ as commonly used includes the origin of novelties, possibly even in the strong sense of Müller and Wagner (1991), i.e. the addition of distinct homologues to a type. However, as mentioned above my account of homology as evolvability focuses on ‘evolvability’ in the sense of the possibility of the morphological change of given characters.

  4. In Brigandt (in press) I construe a homologue as a homeostatic property cluster (HPC) natural kind. The HPC view of natural kinds additionally clarifies how the two approaches to homology are related: an HPC kind consists in (1) a cluster of properties that tend to co-occur and (2) homeostatic mechanisms that are the causal basis of the properties’ clustering. Phylogenetic approaches focus on the cluster of properties that are diagnostic of a natural kind (synapomorphies shared among most instances of a homologue), while developmental approaches focus on the homeostatic mechanisms that form the causal basis of the cluster properties’ correlation.

  5. “A developmental constraint is a bias on the production of variant phenotypes or a limitation on phenotypic variability caused by the structure, character, composition, or dynamics of the developmental system” (Maynard Smith et al. 1985: 266).

  6. My focus on developmental constraints as those features that determine the type as the set of homologues aligns with the account of novelty by Müller and Wagner (1991, 2003). On their position, a morphological ‘novelty’ is a character that is not homologous to any ancestral structure; and the evolution of a novelty involves “a breaking up of developmental or functional constraints that prevailed in the ancestral lineage”, as the transitions from ancestral states to novelties “require developmental modifications that are not within the mutational reach of the ancestral character state” (2003: 220). In my terminology, their account says that the ancestral type embodies constraints determining a set of characters as the dimensions along which regular heritable phenotypic variation can occur (changes ‘within the mutational reach’ of the ancestral state), ensuring evolvability as change in given characters. The origin of a novel character consists in the ancestral type ceding to a reorganized type characterized by a different set of constraints. While a novelty emerges after rounds of mutation and selection, these notions do not carry the explanatory force when accounting for the evolution of a novelty, as in this case the regular phenotypic variation does not lead to the novel character (and the novelty may be an epigenetic side-effect of changes in overall development caused by selection; Müller 1991). Instead, any such explanation has to specify how the developmental system could be reorganized such that the new character could evolve after all. Thus, in the explanation of the evolution of novelties—as in the explanation of evolvability—features of development make up the explanans (Wagner 2000).

  7. Some proponents of the notion of developmental constraints were aware of this point (e.g. Oster and Alberch 1982), but it has often been forgotten in the ensuing debate that set up selection and constraints against each other (Amundson 1994).

  8. This does not mean that I assume that there is a fixed number of levels applying to all organisms or that for any organism there is a clear-cut number of levels into which all homologues can be neatly arranged. What an organism’s homologues are depends on what the dimensions of variability are, which may differ from taxa to taxa. While for a given organism there are cases where a certain gross-morphological structure is a distinct homologue from a particular developmental process, another structure may vary only together with its developmental basis, so that both form a single homologue that cannot be assigned to one of the standard levels. Rather than being committed to a strong notion of organismal levels, my position is that there are genuinely distinct homologues (according to my account of homology) that occupy in some cases what are intuitively considered distinct levels.

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Acknowledgements

I am indebted to Marc Ereshefsky, Paul Griffiths, and Alan Love for detailed comments on an earlier version of this paper. The work on this essay was funded with an Izaak Walton Killam Memorial Postdoctoral Fellowship by the Killam Trusts, Canada.

Author information Authors and Affiliations

  1. Department of Philosophy, University of Alberta, 4-115 Humanities Centre, Edmonton, AB, T6G 2E5, Canada

    Ingo Brigandt

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Correspondence to Ingo Brigandt.

About this article Cite this article

Brigandt, I. Typology now: homology and developmental constraints explain evolvability. Biol Philos 22, 709–725 (2007). https://doi.org/10.1007/s10539-007-9089-3

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