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.
Similar content being viewed by others
Notes
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.
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.
‘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.
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.
“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).
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).
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.
References
Abouheif E (1997) Developmental genetics and homology: a hierarchical approach, Trends Ecol Evol 12:405–408
Abouheif E, Akam M, Dickinson WJ, Holland PWH, Meyer A, Patel NH, Raff RA, Roth VL, Wray GA (1997) Homology and developmental genes. Trends Genet 13:432–433
Amundson R (1994) Two concepts of constraint: adaptationism and the challenge from developmental biology. Philos Sci 61:556–578
Amundson R (2005) The changing role of the embryo in evolutionary thought: roots of evo-devo. Cambridge University Press, Cambridge
Amundson R, Lauder G (1994) Function without purpose: the uses of causal role functions in evolutionary biology. Biol Philos 9:443–469
Bolker JA (2000) Modularity in development and why it matters to evo-devo. Am Zool 40:770–776
Bolker JA, Raff RA (1996) Developmental genetics and traditional homology. Bioessays 18:489–494
Brigandt I (2003) Homology in comparative, molecular, and evolutionary developmental biology: the radiation of a concept. J Exp Zool (Mol Dev Evol) 299B:9–17
Brigandt I (2006) Homology and heterochrony: the evolutionary embryologist Gavin Rylands de Beer (1899–1972). J Exp Zool (Mol Dev Evol) 306B:317–328
Brigandt I (in press) Natural kinds in evolution and systematics: metaphysical and epistemological considerations. Acta Biotheoretica
Cracraft J (2005) Phylogeny and evo-devo: characters, homology, and the historical analysis of the evolution of development. Zoology 108:345–356
de Beer GR (1971) Homology, an unsolved problem. Oxford University Press, Glasgow
Dickinson WJ (1995) Molecules and morphology: where’s the homology? Trends Genet 11:119–121
Donoghue MJ (1992) Homology. In: Keller EF, Lloyd EA (eds) Keywords in evolutionary biology, Harvard University Press, Cambridge, MA, pp 170–179
Gerhart J, Kirschner M (1998) Evolvability. Proc Natl Acad Sci USA 95:8420–8427
Gilbert SF, Bolker JA (2001) Homologies of process and modular elements of embryonic construction. J Exp Zool (Mol Dev Evol) 291:1–12
Gilbert SF, Opitz JM, Raff RA (1996) Resynthesizing evolutionary and developmental biology. Dev Biol 173:357–372
Gilbert SF, Sarkar S (2000) Embracing complexity: organicism for the 21st century. Dev Dyn 219:1–9
Gould SJ, Lewontin RC (1979) The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B 205:581–598
Griffiths PE (1996) The historical turn in the study of adaptation. Br J Philos Sci 47:511–532
Griffiths PE (2006) Function, homology, and character individuation. Philos Sci 73:1–25
Hall BK (1995) Homology and embryonic development. In: Hecht MK, MacIntyre RJ, Clegg MT (eds) Evolutionary biology, vol 28. Plenum Press, New York, pp 1–37
Kirschner M, Gerhart J (2005) The plausibility of life: resolving Darwin’s dilemma. Yale University Press, New Haven
Laubichler M (2000) Homology in development and the development of the homology concept. Am Zool 40:777–788
Lauder GV (1986) Homology, analogy, and the evolution of behavior. In: Nitecki MH, Kitchell JA (eds) Evolution of animal behavior: paleontological and field approaches. Oxford University Press, New York, pp 9–40
Lauder GV (1994) Homology, form, and function. In: Hall BK (eds) Homology: the hierarchical basis of comparative biology. Academic Press, San Diego, pp 151–196
Love AC (2006) Evolutionary morphology and evo-devo: hierarchy and novelty. Theory Biosci 124:317–333
Love AC, Raff RA (2006) Larval ectoderm, organizational homology, and the origins of evolutionary novelty. J Exp Zool (Mol Dev Evol) 306B:18–34
Maynard Smith J, Burian R, Kauffman S, Alberch P, Campbell J, Goodwin B, Lande R, Raup D, Wolpert L (1985) Developmental constraints and evolution. Q Rev Biol 60:265–287
Mayr E (1959) Where are we? In: Wooldridge C (ed) Genetics and twentieth century Darwinism (Cold Spring Harbor symposia on quantitative biology, vol 24). The Biological Laboratory, New York, pp 1–14
Mayr E (1982) The growth of biological thought. Belknap Press, Cambridge, MA
Mayr E (1994) Response to John Beatty. Biol Philos 9:357–358
Minelli A (2003) The development of animal form: ontogeny, morphology, and evolution. Cambridge University Press, Cambridge
Müller GB (1991) Developmental mechanisms at the origin of morphological novelty: a side-effect hypothesis. In: Nitecki MH (ed) Evolutionary innovations. University of Chicago Press, Chicago, pp 99–130
Müller GB (2003) Homology: the evolution of morphological organization. In: Müller GB, Newman SA (eds) Origination of organismal form: beyond the gene in developmental and evolutionary biology. MIT Press, Cambridge, MA, pp 52–69
Müller GB, Newman SA (1999) Generation, integration, autonomy: three steps in the evolution of homology. In: Bock GR, Cardew G (eds) Homology. John Wiley & Sons, Chicester, pp 65–73
Müller GB, Wagner GP (1991) Novelty in evolution: restructuring the concept. Annu Rev Ecol Syst 22:229–256
Müller GB, Wagner GP (1996) Homology, hox genes, and developmental integration. Am Zool 36:4–13
Müller GB, Wagner GP (2003) Innovation. In: Hall BK, Olson WM (eds) Keywords and concepts in evolutionary developmental biology. Harvard University Press, Cambridge, MA, pp 218–227
Newman SA (2006) The developmental genetic toolkit and the molecular homology-analogy paradox. Biol Theor Integr Dev Evol Cogn 1:12–16
Nielsen C, Martinez P (2003) Patterns of gene expression: homology or homocracy? Dev Genes Evol 213:149–154
Oster G, Alberch P (1982) Evolution and bifurcation of developmental programs. Evolution 36:444–459
Owen R (1843) Lectures on the comparative anatomy and physiology of the invertebrate animals, delivered at the Royal College of Surgeons in 1843. Longman, Brown, Green, and Longmans, London
Patterson C (1982) Morphological characters and homology. In: Joysey KA, Friday AE (eds) Problems of phylogenetic reconstruction. Academic Press, London pp 21–74
Rieppel O (2006) Modules, kinds, and homology. J Exp Zool (Mol Dev Evol) 304B:18–27
Roth VL (1988) The biological basis of homology. In: Humphries CJ (ed) Ontogeny and systematics. Columbia University Press, New York, pp 1–26
Simpson GG (1961) Principles of animal taxonomy. Columbia University Press, New York
Stadler BMR, Stadler PF, Wagner GP, Fontana W (2001) The topology of the possible: formal spaces underlying pattern of evolutionary change. J Theor Biol 213:241–274
von Dassow G, Munro E (1999) Modularity in animal development and evolution: elements for a conceptual framework for EvoDevo. J Exp Zool (Mol Dev Evol) 285:307–325
Wagner GP (1989a) The biological homology concept. Annu Rev Ecol Syst 20:51–69
Wagner GP (1989b) The origin of morphological characters and the biological basis of homology. Evolution 43:1157–1171
Wagner GP (1994) Homology and the mechanisms of development. In: Hall BK (ed) Homology: the hierarchical basis of comparative biology. Academic Press, San Diego pp 273–299
Wagner GP (1996) Homologues, natural kinds and the evolution of modularity. Am Zool 36:36–43
Wagner GP (2000) What is the promise of developmental evolution? Part I: why is developmental biology necessary to explain evolutionary innovations? J Exp Zool (Mol Dev Evol) 288:95–98
Wagner GP (2007a) How wide and how deep is the divide between population genetics and developmental evolution? Biol Philos 22:145–153
Wagner GP (2007b) The developmental genetics of homology. Nat Rev Genet 8:473–479
Wagner GP, Laubichler M (2000) Character identification in evolutionary biology: the role of the organism. Theory Biosci 119:20–40
Wagner GP, Misof BY (1993) How can a character be developmentally constrained despite variation in developmental pathways? J Evol Biol 6:449–455
Wagner GP, Stadler PF (2003) Quasi-independence, homology and the unity of type: a topological theory of characters. J Theor Biol 220:505–527
Wallace B (1986) Can embryologists contribute to an understanding of evolutionary mechanisms? In: Bechtel W (ed) Integrating scientific disciplines. M. Nijhoff, Dordrecht, pp 149–163
Winther RG (2001) Varieties of modules: kinds, levels, origins and behaviors. J Exp Zool (Mol Dev Evol) 291:116–129
Wouters A (2003) Four notions of biological function. Stud Hist Philos Biol Biomed Sci 34:633–668
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
Corresponding author
Rights and permissions
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10539-007-9089-3