Morphological Evolution:

Epigenetic Mechanisms
Stuart A Newman, New York Medical College, Valhalla, New York, USA
Gerd B Muller, University of Vienna, Vienna, Austria

Keynote article
Article Contents
. Introduction
. Physics of Multicellularity and the Origin of Body Plans
. Interplay of Generic and Programmatic Mechanisms of
Development
. Epigenetics of Advanced Development
. Origin of Morphological Homology

Online posting date: 15th February 2010

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 developmentalgenetic 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.

Introduction
Materials of the nonliving world take on forms dictated by
external forces to which they are susceptible by virtue of
their inherent physical properties. Water, for example,
forms waves and vortices if it is mechanically agitated,
whereas clay bears the record of its most recent physical
impressions long after they have been exerted. Living
metazoa multicellular animals seem to obey dierent
rules: their forms appear to be expressions of intrinsic
developmental programmes. Although organisms must, of

ELS subject area: Evolution and Diversity of Life

How to cite:
Newman, Stuart A; and Muller, Gerd B (February 2010) Morphological
Evolution: Epigenetic Mechanisms. In: Encyclopedia of Life Sciences
(ELS). John Wiley & Sons, Ltd: Chichester.
DOI: 10.1002/9780470015902.a0002100.pub2

course, exchange energy and matter with the external world

to stay alive, the general architectures and ne details of the
forms they assume are taken to have become independent
of the external environment.
But consideration of the mechanisms of morphogenesis
and pattern formation revealed by modern developmental
biology suggests that at early stages in their evolution the
forms of metazoan organisms were not generated in such a
rigid programmatic fashion. Rather, the earliest multicellular organisms must have been moulded by their
physical environments to a much greater extent than contemporary organisms and, with regard to the generation of
three-dimensional form, were more like certain materials of
the nonliving world than are their modern, evolved counterparts. See also: Eukaryotes and Multicells: Origin;
Multicellular Organs and Organisms
Present-day organisms are characterized by redundancies of gene action and highly integrated signalling
networks which ensure that developmental pathways
are reliable and resistant to perturbation. In contrast, the
most ancient multicellular creatures were simple cell
aggregates that arose by adhesion of originally free-living
cells, or by the failure of the same to separate after mitosis.
Although the single-celled progenitors were themselves the
sophisticated products of a billion years or more of evolution, the steps that made them multicellular could have
been as simple as a single mutation that rendered a cell
surface protein sticky, or even a change in the ion content of
the sea that provided a pre-existing protein with this new
property. Once this occurred, and it probably occurred
more than once in the history of life, living organisms
became susceptible to new sets of determinants: initially the
forces that mould what physicists refer to as soft matter
along with the inherent self-organizing capabilities of
chemically and mechanically excitable materials, and later
other conditional form-generating processes, such as tissue
inductive interactions. We refer to these conditional, nonprogrammatic determinants collectively as epigenetic
mechanisms (Newman and Muller, 2000). See also: Beyond
the Genome; Epithelial Branching; Modelling of Plant
Growth and Development; Nonlinear Dynamics and
Chaos

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Morphological Evolution: Epigenetic Mechanisms

Physics of Multicellularity and the

Origin of Body Plans
Multicellular organisms rst arose more than 600 Ma. By
approximately 540 Ma, at the end of the Cambrian
explosion, virtually all the bauplans or body types seen in
modern animals (the Metazoa) already existed (Conway
Morris, 2006) (the complex plants arising later). Although
the early world contained many unoccupied niches within
which new organismal forms could ourish, this alone can
neither account for the rapid profusion of body plans once
multicellularity was established, nor for the particular
forms that bodies and organs assumed. In particular,
metazoan bodies are characterized by axial symmetries and
asymmetries, multiple tissue layers, interior cavities, segmentation and various combinations of these properties.
The organs of these creatures are organized in similar ways,
on a smaller scale. Just as we recognize that liquids, clays,
taut strings and soap bubbles can take on only limited,
characteristic arrays of shapes and congurations, it is
reasonable to ask what the characteristic spectrum of forms
would have been for ancient multicellular matter. Such
matter consisted of cells producing numerous gene products, some of which were released, and some of which
remained at the surface, providing the means for cell
aggregation. The highly integrated genetic mechanisms of
pattern formation and morphogenesis seen in present-day
organisms could not have been present at the dawn of
multicellularity. Rather, as will be described, the body and
tissue forms we have come to associate with modern
multicellular organisms were already inherent in the
material make-up of their ancient, less programmed
ancestors (Newman et al., 2006). See also: Adhesive
Specicity and the Evolution of Multicellularity; Cambrian Radiation; Chordate and Vertebrate Body Plans

embryogenesis, but would have also arisen in primitive

metazoan ancestors in the course of evolution due to lax
regulation of gene expression, a novel conguration automatically emerges. As seen in experiments in which cells
which only dier in surface adhesion are randomly mixed,
the dierent populations will sort out, forming a multilayered structure with interfaces between the layers, across
which cells will not intermix (Steinberg, 2003). This sortingout behaviour may be driven entirely by dierential adhesion, but it is also promoted by dierences between the cell
types in the tension the cytoskeleton exerts on the cortical
cytoplasm just beneath the cell surface (Krieg et al., 2008).
Subdivisions of tissues based on dierential anity, if (as is
often the case) they also represent distinct cell lineages, are
termed compartments. See also: Adhesive Specicity and
the Evolution of Multicellularity
This phenomenon is similar to what occurs when two
immiscible liquids, such as oil and water, are shaken
together and allowed to separate. In cellular systems,
in place of the chemical free energy whose minimization
governs the phase separation of liquids, an energy function
at the cellcell interface that combines adhesive strength
and cellcortex tension is minimized (Krieg et al., 2008).
Gastrulation, the set of developmental processes by which
tissue layers and their relative positions are achieved during
embryogenesis, is a hallmark of most metazoan groups.
Although the precise spatiotemporal organization of such
behaviours has come under the control of gene expression
programmes in present-day organisms, they likely originated in the minimization of interfacial energy that drives
the sorting-out behaviour of dierent cell populations.
See also: Cleavage and Gastrulation in Leech Embryos;
Cleavage and Gastrulation in Mouse Embryos; Cleavage
and Gastrulation in the Sea Urchin; Cleavage and
Gastrulation in Zebrash Embryos

Adhesion, differential adhesion and cortical

tension

Diffusion, concentration gradients and

lateral inhibition

The advent of cellcell adhesion early in the history of

multicellular life opened up possibilities for the moulding
of bodies and their tissues that were unavailable to singlecelled organisms. The primary reason for this is that different physical processes predominate at dierent spatial
scales the shapes and forms of macroscopic objects, such
as multicellular aggregates, are inuenced by physical
determinants dierent from those that noticeably aect
microscopic objects, such as individual cells.
Cell adhesion is the dening condition of multicellularity. When all the cells in a cluster have the same
number of adhesion molecules on their surfaces, they will
form a solid (i.e. not hollow) spherical ball. Many embryos
start out with, or pass through, such a conguration, and
uniform balls of cells are found in fossil beds of the Ediacaran period at the dawn of animal evolution. If cells within
an aggregate have dierent degrees of adhesiveness, as
occurs in a regulated fashion in later stages of animal

Diusion is a physical process that produces either

molecular uniformity or nonuniformity depending on
the time and spatial scale over which it acts. Over the
dimensions of an individual cell diusion would quickly
erase any heterogeneity. But since the intracellular environment is crowded and complex, free diusion plays only a
limited role in the cell interior. On the scale of a cell
aggregate, in contrast, diusion promotes the formation of
gradients of released molecules (Crick, 1970). In ancient
cellular clusters, a group of cells that released a product at a
higher rate than their neighbours either by a spontaneous, stochastic eect or because something in their
environment induced them to do so would have taken on
a privileged, organizing role in the aggregate. It is not
necessary that the organizer cells be predetermined: once
they arise they have global patterning consequences,
imparting a spatially nonuniform microenvironment to the
clusters cells.

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Morphological Evolution: Epigenetic Mechanisms

The patterning role of a diusible molecule is enhanced if

it signals surrounding cells not to acquire the same state or
produce the same molecule, an eect known as lateral
inhibition. Since the unicellular organisms that preceded
the Metazoa had biochemical circuitry enabling them to
switch between alternative states (see later discussion), it
would have not taken much additional genetic evolution to
form regulatory networks known as reactiondiusion, or
local autoactivationlateral inhibition (LALI), systems
(Meinhardt and Gierer, 2000). Such systems can generate
spatial periodicities such as in the digits of the limbs and
dentition of vertebrates, hair follicles in mammals and
bristles in insects, and pigment patterns in sh and snails
(Turing, 1952; Meinhardt, 2008; Newman et al., 2008).
Present-day embryos continue to employ diusible signal
molecules (called morphogens) to generate regional differences during development, but the propagation of their
eects have often become, over the course of evolution,
integrated with other cell functions. See also: Modelling of
Plant Growth and Development; Vertebrate Embryo:
Establishment of Left-Right Asymmetry

Cell polarity, lumen formation and

elongation
The rst multicellular organisms were likely to have been
composed of cells with a uniform, or random, distribution
of adhesive molecules on their surfaces. Many modern cell
types, in contrast, are polarized, capable of allocating different molecular species to their apical and basolateral
regions. The targeting of adhesive molecules, or antiadhesive molecules, to specic regions of the cell surface
has dramatic consequences. A tissue mass consisting of
motile cells that are nonadhesive over portions of their
surfaces will readily develop cavities or lumens (Tsarfaty
et al., 1994). If such spaces come to adjoin one another as a
result of random cell movement, they will readily fuse.
Lumen formation could therefore have originated as a
simple consequence of dierential adhesion in cells that
express adhesive properties in a polarized fashion. See also:
Adhesive Specicity and the Evolution of Multicellularity;
Multicellular Organs and Organisms
Signicantly, the rst morphologically complex multicellular organisms, represented by the Ediacaran fossil
deposits dating from more than 600 million years ago, were
solid-bodied creatures. Among modern groups, the coelenterates such as comb jellies and hydra are forms with
a single lumen, whereas echinoderms (e.g. starsh) and
vertebrates have both a digestive tube and a surrounding
body cavity. By around 580 Ma animals with distinct body
cavities appeared in the fossil record. Over the following 50
million years all the major animal phyla had arisen. It has
been speculated that the advent of polarized cells, and the
straightforward physical consequences of this step, may
have provided the basis for the rapid profusion of body
types during the late Precambrian and Cambrian periods.
See also: Cambrian Radiation; Diversity of Life

Another type of cell polarity pertains to cell shape. The

spherical clusters that comprise the early embryonic stages
of many present-day species and the embryo-like fossils of
the Ediacaran deposits (Yin et al., 2007) contain cells that
are themselves round or amorphous. But some cells can
undergo planar polarization, which causes them to
lengthen in the plane perpendicular to their apico-basal
axis. These planar-polarized cells will tend to maximize
their adhesive contacts along their long axes. The resulting
intercalation will lead to a simultaneous shortening of the
multicellular aggregate in the direction of the cells long
axes and (because of mass conservation) a lengthening in
the orthogonal direction, a process termed convergent
extension (Keller et al., 2000). The elongated body axes,
characteristic of most animals, likely have their evolutionary origin in the collective behaviour of cells capable
of undergoing planar polarization.

Oscillations, morphogenetic fields and

segmentation
The existence in all cells of positive and negative biochemical feedback loops will often lead to temporal oscillations in one or more molecular component (Goldbeter,
1996). The cell cycle is in fact based on such oscillations.
Others of these periodic activities may have no explicit
functional roles, arising as spontaneous side eects of the
gene regulatory circuitry rather than as the expression of an
evolved network.
Once cells that were capable of exhibiting such oscillations became incorporated into aggregates or primitive
tissues, the eect of scale was again played out in terms of
novel, physically determined eects. Weakly interacting
oscillators of all kinds tend spontaneously to come into
synchrony, and living cells, ranging from bacteria with
articially engineered biochemical oscillators to heart cells
in tissue culture, are no exception. Since no special mechanisms are needed to bring about synchronization, it would
have occurred in any primordial cluster of cells that contained oscillatory circuits. This phenomenon is employed
in the paraxial mesoderm of vertebrate embryos, where it
coordinates cell states and behaviours over broad regions
of tissue (Giudicelli et al., 2007).
Synchronization of oscillating cell states is probably the
basis of many of the phenomena described as morphogenetic elds by classical embryologists (Newman and
Bhat, 2009). In certain cases like the vertebrate embryo the
oscillation underlying the paraxial mesodermal eld is
manifested when tissue cohesivity becomes linked to a
particular phase of the molecular clock (Dequeant and
Pourquie, 2008). Segmentation (called somitogenesis in
vertebrates) has apparently been independently evolved
more than once in the history of the animals (i.e. arthropods, annelids, vertebrates or arthropods+annelids and
vertebrates), and is likely in some cases to be a byproduct of
developmental dynamics rather than a functional adaptation. See also: Somitogenesis in Vertebrate Development

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Morphological Evolution: Epigenetic Mechanisms

Developmental-genetic toolkit, dynamical

patterning modules and animal development
The physical processes described earlier that mediate
morphogenesis and pattern formation can only act on cell
aggregates and tissues if molecular components capable of
harnessing them are present. In the case of the metazoans,
molecules of this kind were already in place before the
appearance of multicellularity, in the form of a subset of the
products of the developmental-genetic toolkit. The
toolkit genes, which specify proteins that regulate transcription as well as ones that regulate cell attachment,
communication and surface and shape polarity, are wellknown to perform corresponding roles across all the animal phyla (Wilkins, 2002). Many of these genes are present
in the Choanozoa, a sister clade of the Metazoa (ShalchianTabrizi et al., 2008). Choanozoans are generally unicellular
or transiently colonial (Lang et al., 2002). Their genetic
similarity with animals indicates that their common
ancestor with the animals, a Precambrian unicellular
organism, already had the capacity to mobilize forces that
could mediate the formation of multicellular clusters and
then shape and organize them. See also: Protozoan
Evolution and Phylogeny
The best-characterized choanozoan, the choanoagellate Monosiga brevicollis, contains several genes specifying cadherins, the family of proteins that mediate cell
cell adhesion in the embryonic tissues of all animal embryos
(Abedin and King, 2008). Since cadherins only perform
this function in the presence of sucient concentrations of
calcium ion, ambient conditions can have caused singlecelled organisms bearing these molecules to become
multicellular aggregates. Choanozoan genomes also specify lectins (glycan-binding proteins), domains of the
extracellular matrix (ECM) protein collagen and integrintype ECM receptors, functional portions of the morphogen
Hedgehog, as well as cell surface and intracellular components of the Notch pathway, which mediates lateral
inhibition in metazoan embryos (Ehebauer et al., 2006;
King et al., 2008; Shalchian-Tabrizi et al., 2008). Since
lateral inhibition is an intrinsically multicellular function,
the Notch pathway may have evolved in single-celled
organisms to perform the related role of inuencing the
choice between alternative cell states. See also: Cell Surface
Glycoconjugates; Drosophila Patterning: DeltaNotch
Interactions; Extracellular Matrix; Hedgehog Signalling;
Integrin Superfamily; Lectins
The Wnt pathway, including families of secreted ligands
and receptors, has two branches, one that mediates apicobasal cell polarity and the other planar cell polarity (Angers
and Moon, 2009). Although no Wnt components have yet
been identied in a choanozoan, two divergent basal
metazoans with simple but distinct body plans, the sponges, with a characteristic labyrinthine morphology, and a
placozoan, a solid-bodied three-layered organism, contain
Wnt pathway genes. The sponges have both branches of the
pathway (Adell et al., 2007) and the placozoan only the
apico-basal polarity branch (Srivastava et al., 2008). These
4

ndings suggest that a single-celled common ancestor of

these organisms either contained elements of both Wnt
pathways or that the planar cell polarity branch was lost in
the Placozoa lineage. See also: Mammalian Embryo: Wnt
Signalling; Placozoa; Porifera (Sponges)
The presumed single-celled ancestors of the Metazoa
therefore contained genes that took roles in the multicellular context dierent from the ones they had evolved to
perform, due to their products entering into associations
(termed dynamical patterning modules; Newman and
Bhat, 2009) with particular physical processes, forces or
eects. The results cellcell adhesion, lumen and compartment formation, generation of morphogen gradients,
convergent extension, segmentation, appendage formation
and skeletogenesis facilitated rapid morphological evolution during the early history of the animals. The morphological motifs that arose from the action of dynamical
patterning modules have been constant themes in the
generation of body plans and organ forms over the succeeding half billion years.

Interplay of Generic and Programmatic Mechanisms of Development

The combined eects of the various physical properties that
were generic to the earliest multicellular aggregates made
virtually inevitable a profusion of layered, hollow, elongated, segmented, appendage-bearing forms early in the history of metazoan life. Although the somatic organization of
these ancient organisms resembled in many respects that of
their modern counterparts, their developmental modes and
mechanisms were very dierent. In particular, the conditional and interactive nature of the physical forces that
moulded these early organisms are likely to have rendered
them morphologically plastic (West-Eberhard, 2003), with
given genomes often being consistent with reversibly interconvertible forms. Only with the subsequent evolution of
genetic redundancy and biochemical integration, leading to
genetic co-optation of forms that originated with strong
physical dependence by hardwired regulatory circuitry,
would organisms of the more familiar modern variety have
emerged: entities in which bodily form is achieved with
decreased participation of external physical forces and
increased dependence on programmatic genetic control
(Newman et al., 2006; Figure 1).
Although natural selection, particularly of the stabilizing and canalizing variety, plays an important role in such
genetic assimilation, the basic morphological motifs and
phenotypes which are subject to selection were largely
manifestations of the inherent properties of cell aggregates
and tissue masses rather than incrementally achieved
adaptations. The recognition that the origination of morphological motifs may be dierent from the means of their
realization in present-day organisms represents a contribution of evolutionary developmental biology (EvoDevo)
that departs from classical evolutionary narratives.

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Morphological Evolution: Epigenetic Mechanisms

See also: Evolutionary Developmental Biology: Developmental and Genetic Mechanisms of Evolutionary Change;
Evolutionary Developmental Biology: Gene Duplication,
Divergence and Co-option; Genetic Redundancy

Epigenetics of Advanced Development

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 organisms 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. (2006).

Once basic body plans were established, selection for biochemical integration, promoting physiological homeostasis and developmental reliability stabilized the
relationship between genotype and phenotype. The dominant role of genetic control in these more advanced
developmental systems is undisputed, and its proximate
workings in modern species represent the primary research
focus of modern developmental biology. But even in highly
controlled forms of development the realization of
morphology, particularly at the level of organogenesis,
continues to depend on nonprogrammatic, epigenetic
mechanisms. Among these are physicochemical, topological and biomechanical factors, as well as generic, stochastic and self-organizational properties of developing
tissues, and the complex dynamics of interactions between
these tissues (Salazar-Ciudad et al., 2003). Although there
is ample empirical evidence for the participation of these
factors in individual ontogenies, their inuence in setting
trajectories of morphological evolution is only recently
coming to be incorporated into the framework of evolutionary theory (Muller, 2007; Salazar-Ciudad, 2006).
See also: Morphology and Disparity through Time

Nonprogrammed processes of development

Genetically controlled development acts through a host of
biomolecules by which cells regulate one anothers activities
(Davidson, 2006). At the initial stages of development the
relationship between gene expression in a given cell and the
resulting behaviour of that cell and its neighbours can be
direct and rather immediate. Subsequent phases of development, however, involve increasing numbers of dierentiated cell populations that produce molecular environments
of ever greater variety and complexity. The composition of
these local microenvironments inuences cells in a broadening, combinatorial fashion and the behaviour of individual cells becomes highly context dependent. With
intensifying complexity of interactions, the developmental
processes become increasingly removed from direct and
exclusive control by the genome. And unless specic mechanisms exist to oppose their actions, the material properties
of tissue primordia will continue to be of decisive importance
in the organization of embryonic structures.
Many of these contextual and generic determinants of
development are the same as or related to the dynamical
patterning modules described above. Others are due to
more complex tissue properties (Larsen, 1992). Instructions for general processes and even for very specic events
in development can arise from the internal environment,

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Morphological Evolution: Epigenetic Mechanisms

for example, maternal factors present in the egg (Badyaev

and Uller, 2009), or the external environment (including
the uterine environment in mammals), which can strongly
inuence development via its chemical composition, energy
supply, temperature, humidity, gravity, mechanical stress,
spatial connement, illumination intensity and periodicity,
etc. (Gilbert and Epel, 2009).
Many events of early development, such as the initiation
of the body axis or of neural tube formation, or of late
development, such as muscle individuation, innervation
patterns or blood vessel growth, depend on inductive
interactions between tissues. The sites of these interactions
are not necessarily predetermined, but may simply require
the meeting of a sender and a receiver tissue. Where this
actually occurs can depend on stochastic factors, such as
cell number, sizes of the primordia, distance between
competent tissues, etc. The activity of the embryo itself can
also contribute to the appropriate development of the size,
shape and arrangement of body components (Muller,
2003a). In consequence, the deployment of genetic information itself during all stages of development is under
epigenetic control (see also Jablonka and Lamb, 2005).

Rapid change and the origin of

morphological novelty
Because of the pervasive role of epigenetic processes in both
ancient and modern developmental systems, accounts of
morphological evolution cannot be reduced to the evolution of molecules and genes. Epigenetic determinants of
tissue morphogenesis are responsible for many heretofore
puzzling phenomena in morphological evolution, such as
instances of rapid morphological change and the emergence of new structural features at the subphylum level.
See also: Evolutionary Ideas: Darwin; Evolutionary Ideas:
The Modern Synthesis
Since gene change by mutation is relatively constant, the
general expectation of the standard theory was that the rate
of morphological change within a phylogenetic lineage
should also remain fairly constant. But, in strong contrast
to this prediction, the fossil record documents numerous
punctuated events (Eldredge and Gould, 1997; Jablonski,
2005). Molecular phylogenies, moreover, provide no indication that episodes of rapid morphological change in
recent species diversications must be accompanied by
accelerated genetic change. Analysis of inbred mouse
strains and of developmental perturbation experiments
lead to similar conclusions: rapid, extensive changes of
morphology are not necessarily linked to corresponding
amounts of genetic change. The epigenetic character of
developmental systems supplies the critical explanatory
mode missing from exclusively gene-centred accounts of
the tempo and mode of evolution (Newman, 2006; Muller,
2007). See also: Molecular Phylogeny Reconstruction
The epigenetic dimension of developmental systems can
also provide insight into another characteristic of morphological evolution that has up till now eluded explanation, namely the appearance of new characters in a
6

phylogenetic lineage. The generic, self-organizing and

conditional, interactive character of the epigenetic determinants discussed earlier provide a natural account for
such innovations (Newman and Muller, 2000; Muller and
Newman, 2005). Genetic change, intraembryonic tissue
interactions and interaction of the organism with the
external environment can all lead to the crossing of
thresholds in the equilibria of developmental interactions,
and the reactive properties of the aected tissues create
kernels of new morphological structures. Explanations of
novelty that invoke genetic change alone fail to address the
actual basis of phenotypic change. See also: Macroevolution: Overview; Origin of Novelties
For example, the relation between alteration in tensile
interactions among embryonic tissues and the appearance
of novel skeletal structures in the vertebrate embryo
(Muller and Streicher, 1989; Muller, 2003a) provide a
mechanism by which gradual evolutionary changes in the
proportions of pre-existing elements can abruptly generate
such novelties when developmental thresholds are crossed.
These system-specic byproducts of the evolutionary
modication of developmental processes take the form of
phenotypic innovations. Once in place, they are susceptible
to becoming reinforced and stabilized in their realization
by additional genetic change under standard Darwinian
selection regimes. The process described represents a rst
step towards the establishment of new homologues in
phylogenetic lineages.

Origin of Morphological Homology

The evolution of morphological phenotypes is a continuing
process of generation and organization of anatomical
structures. Recurrent units of morphological organization
with common ancestry have traditionally been called
homologues, and have been used for systematic and taxonomical purposes for centuries. Their establishment and
the basis of their stability, however, have eluded explanation within the classical evolutionary framework. But new
concepts provided by EvoDevo, including the relationship,
described earlier, between genetic and epigenetic factors of
morphogenesis, enable a causal-mechanistic account of
morphological evolution and homology. Homology has
thus become a core component of an expanded evolutionary framework (Pigliucci and Muller, 2010). See also:
Homology in Character Evolution
Three steps have been described in the establishment of
morphological homology, namely the generation, the xation and the autonomization of individualized constructional elements (Muller and Newman, 1999). As
discussed earlier, the rst step, the generation of new
building elements, will often be a consequence of dynamical patterning modules and other epigenetic properties
of developmental systems under changed conditions
(Figure 2a). Next, the xation of new elements within
existing body plans will occur with the progressive integration of phenotypic, developmental and genetic levels of

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Morphological Evolution: Epigenetic Mechanisms

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 1c) 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 organisms 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 organisms 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 noveltys 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 1b and c).

interaction, typically as a result of standard scenarios of

natural selection. Phenotypic novelties initially brought
about by epigenetic mechanisms will increasingly come to
rely on genetic control for their ontogenetic realization.
Since selection favours the genetic linkage of functionally
coupled characters (Burger, 1986), functional interdependencies that become established at the phenotypic

level will contribute to a further locking in of new characters and will gain increasing organizational importance
as increasingly elaborate design features are incorporated.
The result is an ever closer mapping between genotype and
phenotype (Figure 2b).
But the evolution of homology does not stop at this
point. Once new building elements have become integrated
into the body design of a taxon, they can gain independence
from the mechanisms responsible for their initial establishment. This is suggested by those cases in which dierent
ontogenetic pathways are employed for the realization of
the same structures in dierent species. Skeletogenesis in
sea urchins, for example, involves the use of dierent progenitor lineages in direct developing species than it does in
those that pass through a larval stage (Wray and Ra,
1989). The orbitosphenoid, a component of the skull,
develops as membrane bone in worm lizards but as
replacement bone in other vertebrates (Bellairs and Gans,
1983). Meckels cartilage of the mandibular arch is induced
by the endoderm in amphibians but by the ectoderm in
higher vertebrates (Hall, 1983). Segmental development
in long germ band insects such as the fruity diers
considerably from this process in short germ band insects
like beetles, whereas the resulting structures are clearly
homologous. In other cases the expressed genes and eventual molecular make-up of embryonic structures have
changed during evolution of a lineage (Kiontke et al.,
2007). See also: Evolutionary Developmental Biology:
Homologous Regulatory Genes and Processes
These examples demonstrate that the same phenotypic
end-point can be reached by alternative developmental
modes and pathways. In other words, morphological
homology persists while its molecular, genetic and developmental components become free to drift (True and
Haag, 2001), a process that has been termed autonomization (Muller and Newman, 1999; Figure 2c). But since
the homologues themselves are maintained as constructional units of the phenotype, they assume a role as
independent organizers of body design and of the evolving
gene regulatory hierarchy (the Organizational Homology
Concept; Muller, 2003b). In this account, phenotypic
organization and the evolution of morphological form
becomes strongly determined by the specic set of homologues that a phylogenetic lineage has acquired.

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Further Reading

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 Darwins Dilemma. New Haven: Yale University
Press.
Minelli A (2003) The Development of Animal Form: Ontogeny,
Morphology, and Evolution. Cambridge, NY: Cambridge University Press.
Muller GB and Newman SA (eds) (2003) Origination of Organismal Form: Beyond the Gene in Developmental and Evolutionary Biology. Cambridge, MA: MIT Press.
Ra R (1996) The Shape of Life: Genes, Development, and the
Evolution of Animal Form. Chicago: The University of Chicago
Press.
Sole R and Goodwin B (2000) Signs of Life. New York: Basic
Books.

Bonner JT (1996) Sixty Years of Biology: Essays on Evolution and

Development. Princeton, NJ: Princeton University Press.

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