Morphological Evolution: Epigenetic Mechanisms

Abstract

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).

close

References

Abedin M and King N (2008) The premetazoan ancestry of cadherins. Science 319: 946–948.

Adell T, Thakur AN and Müller WE (2007) Isolation and characterization of Wnt pathway‐related genes from Porifera. Cell Biology International 31: 939–949.

Angers S and Moon RT (2009) Proximal events in Wnt signal transduction. Nature Review of Molecular Cell Biology 10: 468–477.

Badyaev AV and Uller T (2009) Parental effects in ecology and evolution: mechanisms, processes and implications. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 364: 1169–1177.

Bellairs AD and Gans C (1983) A reinterpretation of the amphisbaenian orbitosphenoid. Nature 302: 243–244.

Bürger R (1986) Constraints for the evolution of functionally coupled characters: a nonlinear analysis of a phenotypic model. Evolution 40: 182–193.

Conway Morris S (2006) Darwin's dilemma: the realities of the Cambrian ‘explosion’. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 361: 1069–1083.

Crick FHC (1970) Diffusion in embryogenesis. Nature 225: 420–422.

Davidson EH (2006) The Regulatory Genome: Gene Regulatory Networks in Development and Evolution. Amsterdam, London: Elsevier/Academic Press.

Dequéant ML and Pourquié O (2008) Segmental patterning of the vertebrate embryonic axis. Nature Review. Genetics 9: 370–382.

Ehebauer M, Hayward P and Arias AM (2006) Notch, a universal arbiter of cell fate decisions. Science 314: 1414–1415.

Eldredge N and Gould SJ (1997) On punctuated equilibria. Science 276: 338–341.

Gilbert SF and Epel D (2009) Ecological Developmental Biology: Integrating Epigenetics, Medicine, and Evolution. Sunderland, MA: Sinauer.

Giudicelli F, Özbudak EM, Wright GJ and Lewis J (2007) Setting the tempo in development: an investigation of the zebrafish somite clock mechanism. PLoS Biology 5: e150.

Goldbeter A (1996) Biochemical Oscillations and Cellular Rhythms: The Molecular Bases of Periodic and Chaotic Behaviour. Cambridge, UK: Cambridge University Press.

Hall BK (1983) Epigenetic control in development and evolution. In: Goodwin BC, Holder N and Wylie CG (eds) Development and Evolution, pp. 353–379. Cambridge, UK: Cambridge University Press.

Jablonka E and Lamb MJ (2005) Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral, and Symbolic Variation in the History of Life. Cambridge, MA: MIT Press.

Jablonski D (2005) Evolutionary innovations in the fossil record: the intersection of ecology, development, and macroevolution. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution 304: 504–519.

Keller R, Davidson L, Edlund A et al. (2000) Mechanisms of convergence and extension by cell intercalation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355: 897–922.

King N, Westbrook MJ, Young SL et al. (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451: 783–788.

Kiontke K, Barriere A, Kolotuev I et al. (2007) Trends, stasis, and drift in the evolution of nematode vulva development. Current Biology 17: 1925–1937.

Krieg M, Arboleda‐Estudillo Y, Puech PH et al. (2008) Tensile forces govern germ‐layer organization in zebrafish. Nature Cell Biology 10: 429–436.

Lang BF, O'Kelly C, Nerad T, Gray MW and Burger G (2002) The closest unicellular relatives of animals. Current Biology 12: 1773–1778.

Larsen E (1992) Tissue strategies as developmental constraints: implications for animal evolution. Trends in Ecology and Evolution 7: 414–417.

Meinhardt H (2008) Models of biological pattern formation: from elementary steps to the organization of embryonic axes. Current Topics in Developmental Biology 81: 1–63.

Meinhardt H and Gierer A (2000) Pattern formation by local self‐activation and lateral inhibition. BioEssays 22: 753–760.

Müller GB (2003a) Embryonic motility: environmental influences and evolutionary innovation. Evolution & Development 5: 56–60.

Müller GB (2003b) Homology: the evolution of morphological organization. In: Müller GB and Newman SA (eds) Origination of Organismal Form: Beyond the Gene in Developmental and Evolutionary Biology, pp. 51–69. Cambridge, MA: MIT Press.

Müller GB (2007) Evo‐devo: extending the evolutionary synthesis. Nature Review. Genetics 8: 943–949.

Müller GB and Newman SA (1999) Generation, integration, autonomy: three steps in the evolution of homology. Novartis Foundation Symposium 222: 65–73.

Müller GB and Newman SA (2005) The innovation triad: an EvoDevo agenda. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution 304: 487–503.

Müller GB and Streicher J (1989) Ontogeny of the syndesmosis tibiofibularis and the evolution of the bird hindlimb: a caenogenetic feature triggers phenotypic novelty. Anatomy and Embryology 179: 327–339.

Newman SA (2006) The developmental‐genetic toolkit and the molecular homology‐analogy paradox. Biological Theory 1: 12–16.

Newman SA and Bhat R (2009) Dynamical patterning modules: a “pattern language” for development and evolution of multicellular form. International Journal of Developmental Biology 53: 693–705.

Newman SA and Müller GB (2000) Epigenetic mechanisms of character origination. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution 288: 304–317.

Newman SA, Christley S, Glimm T et al. (2008) Multiscale models for vertebrate limb development. Current Topics in Developmental Biology 81: 311–340.

Newman SA, Forgacs G and Müller GB (2006) Before programs: the physical origination of multicellular forms. International Journal of Developmental Biology 50: 289–299.

Pigliucci M and Müller GB (eds) (2010) Evolution – The Extended Synthesis. Cambridge, MA: MIT Press.

Salazar‐Ciudad I (2006) On the origins of morphological disparity and its diverse developmental bases. BioEssays 28: 1112–1122.

Salazar‐Ciudad I, Jernvall J and Newman SA (2003) Mechanisms of pattern formation in development and evolution. Development 130: 2027–2037.

Shalchian‐Tabrizi K, Minge MA, Espelund M et al. (2008) Multigene phylogeny of choanozoa and the origin of animals. PLoS ONE 3: e2098.

Srivastava M, Begovic E, Chapman J et al. (2008) The Trichoplax genome and the nature of placozoans. Nature 454: 955–960.

Steinberg MS (2003) Cell adhesive interactions and tissue self‐organization. In: Müller GB and Newman SA (eds) Origination of Organismal Form: Beyond the Gene in Developmental and Evolutionary Biology, pp. 137–163. Cambridge, MA: MIT Press.

True JR and Haag ES (2001) Developmental system drift and flexibility in evolutionary trajectories. Evolution & Development 3: 109–119.

Tsarfaty I, Rong S, Resau JH et al. (1994) The Met proto‐oncogene: mesenchymal to epithelial cell conversion. Science 263: 98–101.

Turing AM (1952) The chemical basis of morphogenesis. Philosophical Transactions of the Royal Society B 237: 37–72.

West‐Eberhard MJ (2003) Developmental Plasticity and Evolution. Oxford, NY: Oxford University Press.

Wilkins AS (2002) The Evolution of Developmental Pathways. Sunderland, MA: Sinauer Associates.

Wray GA and Raff RA (1989) Evolutionary modification of cell lineage in the direct‐developing sea urchin Heliocidaris erythrogramma. Developmental Biology 132: 458–470.

Yin L, Zhu M, Knoll AH et al. (2007) Doushantuo embryos preserved inside diapause egg cysts. Nature 446: 661–663.

Further Reading

Bonner JT (1996) Sixty Years of Biology: Essays on Evolution and Development. Princeton, NJ: Princeton University Press.

Forgacs G and Newman SA (2005) Biological Physics of the Developing Embryo. Cambridge: Cambridge University Press.

Kirschner M and Gerhart J (2005) The Plausibility of Life: Resolving Darwin's Dilemma. New Haven: Yale University Press.

Minelli A (2003) The Development of Animal Form: Ontogeny, Morphology, and Evolution. Cambridge, NY: Cambridge University Press.

Müller GB and Newman SA (eds) (2003) Origination of Organismal Form: Beyond the Gene in Developmental and Evolutionary Biology. Cambridge, MA: MIT Press.

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.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

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