Morphological Evolution: Epigenetic Mechanisms


Organismal forms have not always been generated by the highly integrated developmental programmes characteristic of modern multicellular species. Physical forces and other conditional processes played a more prominent role at the earlier stages of evolution, establishing morphological templates that were consolidated by later genetic change. In particular, with the appearance of multicellular aggregates, physical effects relevant to parcels of matter larger than single cells were newly mobilized by gene products (e.g. the ‘developmental‐genetic toolkit’ of the animals) that had originally evolved to serve unicellular functions. These mechanisms are responsible for continued generation of morphological novelty, and are ultimately involved in the establishment of the individualized and heritable construction units of morphological evolution known as homologues.

Key Concepts:

  • Evolution of multicellular organisms began with clusters of individual cells that themselves were products of several billion years of prior evolution.

  • The genes and gene products that eventually came to coordinate multicellular development originally evolved to serve different, unicellular, functions.

  • With the emergence of multicellularity, physical effects and processes relevant to viscoelastic, chemically and mechanically active materials came into play, mobilized by the products of ancient genes.

  • The morphological motifs generated from cell clusters by such ‘mesoscale’ processes are at once predictable and plastic, since the outcomes of physical effects are constrained by the inherent properties of materials and influenced by variable external parameters.

  • Predictable morphological motifs in aggregates of ancestral animal‐type cells include multilayered, hollow, elongated, segmented, appendage‐bearing forms, i.e. embryo‐like entities.

  • Morphological phenotypes arising by such epigenetic means will, through processes of stabilizing and canalizing selection, come to depend on programmes of spatiotemporal gene expression.

  • Since little change in the genomes of single‐celled predecessors was needed to generate the panoply of primitive animal forms, radiations of organismal types could have arisen in relatively short periods of time (e.g. the Cambrian explosion).

  • Even at advanced stages of evolution the conditional nature of epigenetic mechanisms, which include not only the physics of tissue masses but also inductive tissue interactions and influences of the external environment on developmental processes, is retained.

  • The nonlinear and plastic responses of developmental systems to natural selection and environmental induction will occasionally lead to the crossing of a dynamical threshold, producing morphological novelties: unprecedented constructional elements of the body plan.

  • Once generated by epigenetic processes, new morphological characters can evolve to become interdependent with other characters (integration), and finally to acquire the status of a homologues of comparative anatomy by becoming organizational elements of the body plan that persist despite changes in the underlying mechanisms that generate them (autonomization).

Keywords: morphogenesis; pattern formation; genetic co‐optation; homology; novelty; EvoDevo

Figure 1.

Schematic representation of evolutionary partitioning of a morphologically plastic ancestral organism into distinct morphotypes associated with unique genotypes. (a) A hypothetical primitive metazoan is shown with a schematic representation of its genome in the box below it. Developmental‐genetic toolkit genes, specifying both transcription factors and molecules involved in form‐and‐pattern‐determining dynamical patterning modules are shown as coloured geometric objects; interactions between them by lines. Determinants of the organism's form include the products of expression of its genes (blue arrows extending from genomes to forms) and the physico‐chemical external environment (broad purple arrows pointing to forms) acting on its inherent physical properties. At this stage of evolution the organism is highly plastic, exhibiting several condition‐dependent forms that are mutually interconvertible (dark horizontal arrows). (b) Descendants of organism in (a) after some stabilizing evolution. Gene duplication, mutation, etc. have led to genetic integration and assimilation of some outcomes that were previously more dependent on the environment, as well as some subpopulations being biased towards subsets of the original morphological phenotypes. Determinants of form are still gene products inherent physical properties and the physical environment, but the effect of the latter has become attenuated (smaller, fainter purple arrows from the top) as development has become more programmatic. There is also an influence of the form on the genotype (orange arrows from forms to genomes), exerted over evolutionary time, as a well‐established morphological phenotype acts as a selective filter against those variant genotypes that are not compatible with it. Some morphotypes remain interconvertible at this stage of evolution, but others are not. (c) Modern organisms descended from those in (b). Further stabilizing evolution has now led to each morphotype being uniquely associated with its own genotype. Physical causation is even more attenuated (faint purple arrows), but influence of the form itself over acceptable genetic and gene interaction changes is increased. Note that in this idealized example the forms have remained unchanged whereas the genes and mechanisms for generating the forms have undergone extensive evolution. Adapted, with changes, from Newman et al..

Figure 2.

Schematic representation of the three steps in the establishment of homology. (a) A hypothetical evolutionarily ‘advanced’ metazoan is shown, with its genome and genetic interactions involved in its development represented schematically by coloured geometric shapes with connections in the box below. For simplicity, arrows representing the causal role of the genetic components and epigenetic effects involved in development at this stage of evolution (see Figure c) are not shown. (b) An organism like that in (a) in which a morphological novelty in the form of an appendage has arisen. This has occurred by the action of the external environment or internal embryonic microenvironment (i.e. epigenetic factors, represented collectively by the broad turquoise arrow) on the inherent physical properties of a portion of the body. The generation of the novelty also depends on a subset of the organism's genes recruited into the new epigenetic context (shown schematically in smaller box below the appendage). Note that no new genes or mutations of preexisting genes are required for the innovation, although this possibility is not excluded. In this simple example most of the interactions among this subset of gene involved in the development of the main body are also used in the novelty, but the possibility that the epigenetic effect alters gene interactions is also indicated. (c) Over the course of evolution integration of the novelty into the body plan occurs in a number of ways. For simplicity an example is shown in which new regulatory pathways are established between the genes involved in novelty generation and other genes of the organism. Epigenetic factors are indicated to play a diminished role in producing the novelty, represented by a lighter, thinner turquoise arrow. (d) With further evolution the integrated novelty becomes autonomous as a constructional element. The schematic example shown has the novelty remaining unchanged in structure as some of the genes involved in its generation are substituted by other genes in the organism's repertoire. The role of the environment in generating the novelty may be further attenuated (small turquoise arrow). During the integration and autonomization phases the increasing influence of the novelty's properties on retention of acceptable changes in gene expression and interaction are represented by the orange arrows (progressively thicker and more intense in colour) extending from the appendage to the gene boxes below (cf. Figure b and c).



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Further Reading

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Raff R (1996) The Shape of Life: Genes, Development, and the Evolution of Animal Form. Chicago: The University of Chicago Press.

Solé R and Goodwin B (2000) Signs of Life. New York: Basic Books.

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Newman, Stuart A, and Müller, Gerd B(Feb 2010) Morphological Evolution: Epigenetic Mechanisms. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0002100.pub2]