Download Morphological evolution and embryonic developmental diversity in

HYPOTHESIS
531
Development 137, 531-539 (2010) doi:10.1242/dev.045229
© 2010. Published by The Company of Biologists Ltd
Morphological evolution and embryonic developmental
diversity in metazoa
Isaac Salazar-Ciudad*
Most studies of pattern formation and morphogenesis in
metazoans focus on a small number of model species, despite
the fact that information about a wide range of species and
developmental stages has accumulated in recent years. By
contrast, this article attempts to use this broad knowledge base
to arrive at a classification of developmental types through
which metazoan body plans are generated. This classification
scheme pays particular attention to the diverse ways by which
cell signalling and morphogenetic movements depend on each
other, and leads to several testable hypotheses regarding
morphological variation within and between species, as well as
metazoan evolution.
Key words: Pattern formation, Morphogenesis, Body plan
evolution, Evolution of development, Mechanisms of development
Introduction
The conservation of developmental processes, especially that of
genes and gene expression patterns (Gilbert, 2006; Carroll, 2001),
has traditionally received a lot of attention in evolutionary
developmental biology. Differences at the level of genes and gene
interactions among metazoan groups have also been studied (Lynch
and Wagner, 2008). However, few studies have integrated the
available information about different stages of development to
understand the commonalities and differences in the overall process
of development among metazoa. Earlier work identified gross
developmental similarities and differences between metazoan
groups that led to their classification into three types of development
(Davidson, 1991; Davidson et al., 1995; Wray, 2000). These
similarities in development are suggested to relate to similarities in
the body plan or in the life cycle of the different species.
This article introduces a classification scheme that incorporates
the information about additional species and about later stages of
development that has accumulated since the publication of these
previous reviews. I also propose new hypotheses about the
relationship between signalling and morphogenetic movements in
the classification of developmental types. Particular attention is
given to the distinction between morphostatic and morphodynamic
developmental mechanisms (Salazar-Ciudad et al., 2003). In
morphostatic mechanisms, major signalling events occur before the
onset of morphogenetic movements, whereas in morphodynamic
mechanisms, cell signalling and morphogenetic mechanisms occur
at the same time or in a closely interlinked manner (Fig. 1). Previous
work (Salazar-Ciudad and Jernvall, 2004) suggests that this
distinction has important implications for our understanding of
Grup de Genòmica, Bioinformàtica i Evolució, Departament de Genètica i
Microbiologia, Universitat Autònoma de Barcelona, Cerdanyola del Valles, 08193,
Spain.
*Author for correspondence ([email protected])
developmental dynamics and for how development affects
evolution. However, this previous work focused on individual
developmental mechanisms that act only between specific
developmental stages. Here, the focus is not on specific stages, but
instead on the entire period of development. Thus, the previous
classifications are revised to take into account the diversity of events
in metazoa over the course of development. On the basis of the
relative timing and of the interdependence between major signalling
events and morphogenetic movements in early, mid and later
development in different metazoan groups, I distinguish five major
types of development among metazoa, and propose four hypotheses
regarding the connection between developmental type and final
body plan, morphological variation within and between species, and
vertebrate evolution.
I have chosen to define developmental types because many
unrelated species show similarities in the relative timing of
developmental signalling and morphogenetic movements, and
because such developmental types relate to types proposed by other
authors (Davidson, 1991). This classification scheme exists, to a
large extent, for convenience and does not imply that metazoan
development falls into a rigid set of discrete classes without
intermediates. In fact, part of the aim of this article is to explain how
one developmental type could evolve into others. Note that this
classification is not about whether early development is based on
autonomous or inductive specification, but about the more general
interrelationship between signalling and cell movement throughout
development. Note, also, that it only incorporates metazoan groups
for which sufficient information about developmental signalling and
morphogenetic movements in several stages of development is
available.
Developmental mechanisms
For the purposes of this article, developmental mechanisms can be
defined as specific gene networks that, by regulating specific cell
behaviours (such as cell division, apoptosis, signal or extracellular
matrix secretion, changes in adhesion and differentiation), are
responsible for the transformation of one spatial distribution of cell
types (here, such a distribution is called a ‘pattern’) into another
(Salazar-Ciudad et al., 2003). From this perspective, development
can be described as a sequence of transformations between patterns,
each produced by specific developmental mechanisms that change
the pattern in one developmental stage into the pattern of the next
stage (Salazar-Ciudad et al., 2003) (Fig. 1).
Basic developmental mechanisms: inductive versus
morphogenetic
Three fundamentally different developmental mechanisms,
autonomous, inductive and morphogenetic, can be distinguished. In
autonomous mechanisms, pattern transformation is achieved by cells
changing their expression state without cell signalling (SalazarCiudad et al., 2003). For example, a spatially heterogeneous egg
produces, after cleavage, a resulting pattern in which different
DEVELOPMENT
Summary
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HYPOTHESIS
Development 137 (4)
Morphoautonomous
Morphostatic
pattern, is also transformed). Such movements are a consequence of
specific changes in cell behaviour, like cell division, adhesion or
extracellular matrix secretion. They can involve a small number of
cells or the collective behaviour of large groups of cells. Only a few
cells are involved, for example, in directed mitosis (Salazar-Ciudad
et al., 2003), in which inherited (Bowerman and Shelton, 1999)
cytocortical structures mechanically interfere with the mitotic spindle
to reorient the direction in which daughter cells bud off. By contrast,
a large group of cells is involved, for example, in the invagination of
epithelia driven by apical cell constriction (Keller et al., 2003).
Although many cells might activate the same molecular chain of
events, the mechanical binding between cells and the different
mechanical properties at the borders of the invaginating epithelium
result in the distinct positioning of cells in the invagination (Forgacs
and Newman, 2005). Developmental mechanisms have been
classified into several types (see Salazar-Ciudad et al., 2003).
Weak morphodynamic
Strong morphodynamic
Fig. 1. Schematic of four different types of combined
developmental mechanisms potentially employed in metazoan
embryonic development. The original egg cell and the end results are
assumed to be the same to highlight that the differences between
these mechanisms are based on the interdependence and the temporal
co-occurrence of cell signalling and cell movement, and not on the
amount of signalling or cell movement per se. A start pattern in the
form of a stereoblastula-like group of cells is depicted on the left. The
resulting patterns for each mechanism are depicted on the right, and
intermediate patterns are depicted in the middle row. In
morphoautonomous mechanisms, different cell types arise
autonomously; later, each cell type follows a precisely regulated
sequence of activation of morphogenetic mechanisms to produce a
resulting pattern. In morphostatic mechanisms, major signalling events
occur before the onset of morphogenetic movements, whereas in
morphodynamic mechanisms, cell signalling and morphogenetic
mechanisms occur at the same time or in a closely interlinked manner.
So-called weak morphodynamic mechanisms involve only short-range
signalling and modest cell movement, whereas strong morphodynamic
mechanisms involve long-range signalling and large cell
rearrangements. The colours indicate different cell types (i.e. cells that
express different genes). Cells are depicted as circles, and in larger
embryos, epithelia and mesenchyma are represented as filled shapes.
Black arrows indicate extracellular signal secretion (induction); white
arrows indicate cell movements.
daughter cells receive different parts of the egg cytoplasm. In
inductive developmental mechanisms, cells change their patterns of
gene expression in response to extracellular signals from other cells
(Salazar-Ciudad et al., 2003). By contrast, in morphogenetic
developmental mechanisms, pattern transformation does not involve
signalling, but cells moving or being moved towards different spatial
locations (as a consequence, the spatial distribution of cell types, the
Most animal species utilise all of the types of developmental
mechanism described above. The question then arises of how
inductive and morphogenetic mechanisms are combined: does the
inductive mechanism occur first, which is also referred to as
‘morphostatic’, or do the inductive and the morphogenetic
mechanisms occur together, which is also known as
‘morphodynamic’? The logic of these combinations is very
different. In morphostatic mechanisms, inductive mechanisms
establish different expression patterns in cells at different locations,
and then these patterns trigger specific morphogenetic mechanisms.
Thus, the spatio-temporal coordination of cell behaviours required
to acquire a final morphology is attained by cells that follow a
program independently of later extracellular signals (Fig. 1). By
contrast, in morphodynamic mechanisms, cells are signalling while
moving (or while being moved). The spatio-temporal coordination
of cell behaviours required for proper development is not attained
by following a pre-specified developmental program, but instead by
cells constantly re-adjusting their behaviour according to the signals
they receive in the places to which they move or get moved to, as
well as to the signalling and mechanical effects they produce there
and along their way.
In addition, there are also morphoautonomous mechanisms, in
which different cell types arise by autonomous mechanisms, and later
each cell type follows a precisely regulated sequence of activation of
morphogenetic mechanisms to produce the resulting pattern.
Pattern formation simulation studies (Salazar-Ciudad and
Jernvall, 2004) suggest that when the same inductive and
morphogenetic mechanisms are combined for the same amount of
genetic change, morphodynamic mechanisms lead to more
morphological variation than do morphostatic mechanisms.
Morphodynamic mechanisms also produce more complex
morphologies in the sense that there is a larger diversity of spatial
arrangements of cell types within the pattern produced (in other
words, more different sub-patterns within a pattern). Morphostatic
mechanisms, instead, produce simpler and more gradual variation,
in which the parts of a pattern (sub-patterns) can change more
independently (as explained below). Thus, this type of mechanism
produces a simpler relationship between genotype and phenotype,
that is to say a simpler genotype-phenotype map.
It is possible to qualitatively understand this relationship between
developmental dynamics and the variation generated (Fig. 2). In
inductive mechanisms, the spatial distribution of the cells that send
a signal is linearly transferred to the cells that receive the signal (Fig.
DEVELOPMENT
Combined developmental mechanisms: morphostatic
versus morphodynamic
HYPOTHESIS
A
D
B
C
E
F
Fig. 2. Diagrams representing a group of mesenchymal cells that
emit a signal (black dots). The different shades of blue (in the
mesenchyme) and green (in epithelia) depict different signal
concentration thresholds (and thus possibly the induction of different
mesenchymal types). (A)The mesenchymal cells are depicted by the
black circle. Note that the spatial distribution of the signal at different
concentrations is a linear extrapolation of the shape of the signalemitting tissue. (B)The signal arises from a part (black) of a folded
epithelium (green) and diffuses in the mesenchyme (blue) without
being able to cross the epithelium. (C)Here, the invaginated epithelium
encloses less space, which causes less signal dilution. As a result, larger
amounts of epithelium receive high signal concentrations. The same
number of dots are depicted in B and C. (D)In epithelia with more
complex shapes, the mesenchymal areas are not linear extrapolations of
the shape of the signal-emitting tissue or of the diffusion space. Note
that the borders of these areas have different curvatures at different
distances from the source as a result of the different shapes of the
diffusion space. (E,F)In E, diffusion is occurring before the invagination,
whereas in F it is occuring afterwards. Morphostatic mechanisms
involving signalling and invagination produce the three spatial
distributions of mesenchymal types depicted in blue (E).
Morphodynamic mechanisms can produce the shapes in E and F and
others at intermediate stages of the invagination. Thus,
morphodynamic mechanisms can generate a larger diversity and
disparity of spatial distributions.
2A). When the space in which the signal is diffusing is simple, then
changes in the diffusion rate of the signal (or in its secretion rate or
in receptor concentration) lead to simple variations in the spatial
distribution of the cells that receive the signal (Fig. 2B,C). However,
when the signal is diffusing in a more complex space, then more
complex, non-trivial changes in the spatial distribution of the signal
will be caused by changes in the diffusion rate of the signal (Fig.
2D). In other words, depending on the shape of the space in which
the signal is diffusing, it will be more or less diluted in different
directions, effectively ‘channelling’ signal diffusion in specific
directions (Fig. 2D). The shape of this space also depends on the
relative distances and orientations between the cells that send a
signal and the cells that receive it. This channelling is responsible
for the complex relationship between genotypic and phenotypic
variation and the larger diversity of morphologies attainable by
morphodynamic mechanisms. It is also more prominent in
morphodynamic mechanisms because here, signalling tends to
happen in more diverse and complex morphological spaces. Given
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that signalling takes place while cells move, channelling can happen
several times and result in different outcomes as it takes place in
different morphological contexts (taking into account that the
morphology of the embryo is changing; Fig. 2E,F). In morphostatic
mechanisms, by contrast, signalling occurs early in development,
when morphogenetic mechanisms have not yet acted; thus, the
morphological context is likely to be relatively simple. The shape
and the material properties of territories also channel the spreading
of the forces and the relative movements elicited by morphogenetic
mechanisms (Beloussov, 1998; Keller et al., 2003; Forgacs and
Newman, 2005). In general, channelling can make local spatial
asymmetries in one part of a pattern have an effect on other parts of
a developing pattern (which also explains the fact that parts of a
pattern are largely independent in morphostatic mechanisms when
compared with morphodynamic mechanisms).
Types of development
In the following, I describe different types of metazoan development
on the basis of the overall organization of development in terms of
the interdependencies between communication and movement in
cell collectives, as described in the previous section.
Type A: nematodes, spiralians and some small phyla
In the roundworm (nematode) C. elegans, the first cell division after
fertilisation separates the prospective anterior half of the embryo
from a posterior cell, which inherits the so-called P granules from
the fertilised zygote (Gönczy and Rose, 2005). These granules are
involved in reorienting the direction of the mitotic spindle in a
second division (directed mitosis), in which the most posterior cell
(P3) inherits the P granules. Meanwhile, the anterior cell, called AB,
divides along the anterior-dorsal axis. This leads to a blastomere
arrangement in which only one AB daughter cell is in contact with
P3, and thus receives a signal expressed by P3. Later, inductive
interactions between cells that contain and do not contain P granules
(Gönczy and Rose, 2005) lead to additional diversity of fate
commitments and mitotic orientation.
During C. elegans gastrulation, two specific epithelial cells (the
E cells) constrict their apical side to get internalised into the embryo
(Nance et al., 2005) and drag another cell in the same direction.
Although the cells involved experience only modest movements of
one or a few cell diameters, these movements lead to new spatial
arrangements for the cells receiving and sending extracellular
signals that allow the induction of subsequent patterns. Thus, early
C. elegans embryos employ a morphodynamic mechanism in which
inductive mechanisms and morphogenetic mechanisms (either
directed mitosis or invagination) are interdependent in the
production of pattern transformations. Morphodynamic mechanisms
that involve only short-range signalling and modest cell movements
are called weak morphodynamic mechanisms in this article (Fig. 1),
whereas morphodynamic mechanisms that involve long-range
signalling and large cell rearrangements are called strong
morphodynamic mechanisms.
Later developmental stages in C. elegans involve the formation
of organs by rather modest amounts of cell movement. Meanwhile,
the dorsal intercalation of polarized cells (convergent extension),
ventral closure due to cell migration, and the extension and
contraction-driven elongation of the body produce the typical
morphology of the worm (Chisholm and Hardin, 2005). These later
stages are often considered to rely on morphogenetic mechanisms
that are regulated on the basis of previously established gene
expression patterns (Simske and Hardin, 2001). Thus, overall, C.
elegans development might be considered to be rather morphostatic.
DEVELOPMENT
Development 137 (4)
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HYPOTHESIS
Development 137 (4)
Based on this example, a developmental type A could be defined
as using weak morphodynamic mechanisms at early developmental
stages, and as using morphogenetic mechanisms at later stages (Fig.
3A, part a).
There is some variation in the orientation of the early cleavage
events among nematodes, but given that these differences occur
mainly between only distantly related nematode clades, one can
postulate that early nematode development is rather conserved
(Schierenberg, 2006) when compared with that of arthropods or
vertebrates. For example, among all the nematodes studied, only one
species displays gastrulation occurring through the introgression of
a large number of cells (Schierenberg, 2005), as is normally the case
in echinoids, another type A developer.
The development of sea squirts (ascidians) follows a similar
sequence to that of C. elegans. Again, an asymmetrically positioned
and heritable cytocortical structure produces directed mitosis in the
posterior part of the embryo (Kumano and Nishida, 2007; Negishi
et al., 2007). In both cases, these successive small-scale cell
rearrangements are involved in determining the relative positioning
of cells that send and receive signals and, subsequently, in pattern
transformation (Nishida, 2005). Later development in ascidians
involves convergent extension and elongation in groups of tightly
bound cells that lead to the typical ascidian larval morphology
(Munro et al., 2006).
Most bristleworms (polychaetes), spoon worms (echiurans),
molluscs (except for cephalopods), peanut worms (Sipunculida),
Gnathostomulida, polyclad flatworms (polyclad Platyhelminthes),
and probably Mesozoans and tubeworms (Vestimentiphera) display
a similar, and possibly homologous (Henry 2002; Nielsen, 2005),
pattern of cleavage. Their sequence and orientation of cell division,
as well as their cell fates, are remarkably similar (Lambert, 2008).
Even among closely related species, however, there is evidence of
substantial variation in whether the earliest fate decisions during
Aa Type A
Ab Type A
B Type B
(indirect development)
e.g. Echinoderms
e.g. Nematodes
e.g. Cnidarians
M
?
M
MR
or
MD
I
WMD
M
I
C Type C
WMD
D Type D
e.g. Arthropods
E Type E
e.g. Drosophilids
M
I
e.g. Vertebrates
M
M
MD
MD
MD
I
I
cleavage are due to inductive mechanisms or to autonomous
specification (Kingsley et al., 2007; Gilbert and Raunio, 1997). In
addition, the later developmental stages of spiralian species are
poorly understood, so their classification as type A should be taken
as preliminary.
In type A development, early embryos are small, but most cells
are epigenetically distinct (i.e. they express different genes). In
proportion to their size, they have a large diversity of cell types, and
each cell type gives rise to a restricted and largely invariable part of
the adult body. Thus, any small variation or error in the induction of
a single cell type would produce proportionally large changes in late
development. This variation would also probably be amplified, as it
could alter the direction of successive mitoses and thus preclude the
correct positioning of inducing and inducible cells in later stages. If,
on the contrary, induction happens between larger numbers of cells,
then variation or induction errors that affect the fate of one or of a
few cells would have relatively milder effects on later development.
Therefore, type A development might result in a general
entrenchment of early development and in the conservation of this
developmental type [although there are instances of early variation
in development associated with yolk-rich eggs (Raff and Snoke
Smith, 2009)]. This entrenchment is likely to be stronger when more
induction and movement events are required to accomplish full
development (for example, in the production of more complex body
plans).
This suggests that, in type A, variation is low in early stages and
increases progressively with developmental time. The so-called
hourglass model of development proposed that variation in animal
development is high in early and late development and low in the
middle stages (Ballard, 1981; Slack et al., 1993; Raff, 1996). In other
words, species within a clade should be most similar in intermediate
developmental stages and less similar in early and late stages (thus
providing a link between phylogeny and ontogeny). There is an
ongoing debate in the evolutionary developmental biology
community about the validity of this model. Some researchers
propose instead that variation is the smallest in early development
(von Baer, 1828; Arthur, 1997), whereas others suggest that
variation is greatest in mid-development (Bininda-Emonds et al.,
2003). Within species, type A development does not fit the hourglass
model; instead, it fits an inverted pyramid model, as has been
suggested for the whole of animal development (von Baer, 1828;
Arthur, 1997). The developmental program of very indirect
developers (meaning that the adult stage is reached after
metamorphosis from a larva that is very different from the adult)
could equally be thought of as consisting of two inverted pyramids
(one for the larval stage and one for the development of the adult
from set-aside cells; see Fig. 3A, part b). Therefore, either the
hourglass model does not hold for type A development, or the model
fits due to natural selection on variation within species.
I
Type B development is characterised by extensive cell signalling
that appears to occur concomitantly with extensive cell movements
(Fig. 3B). In contrast to other types of development, these signalling
and cell movement events occur in a relatively simple
morphological context, consisting mostly of only two germ layers.
Type B development is suggested to occur in cnidarians.
The cleavage and gastrulation of cnidarians has been described
as highly variable (Grassé, 1953; Grassé, 1997; Tardent, 1978;
Gilbert and Raunio, 1997), even within species (Fritzenwanker et
al., 2007; Magie and Martindale, 2007). The morphology of the
gastrula seems to be quite variable between individuals in the
DEVELOPMENT
Type B: cnidarians
Fig. 3. Metazoan hour-glass models. The diagrams depict, for each
type of development, a plot with an estimation of the amount of
variation (x-axis) along developmental time (y-axis). To facilitate
comparison, all plots are the same size, but this is not meant to imply
that development is equally long or variable in all groups. The green
areas in the plot give a coarse estimation of the relative use of inductive
(I) or autonomous (A) mechanisms, and the white areas indicate the
same for morphogenetic mechanisms (M). The bar at the right side of
each plot indicates the intervals of developmental time during which
morphodynamic (MD), weak morphodynamic (WMD),
morphoregulatory (MR) or morphoautonomous (MA) mechanisms
might be active.
HYPOTHESIS
Development 137 (4)
Type C: short-germ-band segmentation and sequentially
segmenting arthropods
Type C development is characterised by being morphostatic (or
weakly morphodynamic) in its early stages and strongly
morphodynamic in later stages and in segment-specific development
(Fig. 3C). It is found in some arthropods, as discussed below.
Most arthropods have centrolecithical eggs, meaning that the yolk
is located in the centre of the egg cytoplasm. In some species, early
karyokinesis occurs without accompanying cytokinesis. Then, most
nuclei migrate to the surface of the egg and cellularize (Anderson,
1973), thereby forming an epithelium (blastoderm). In other species,
highly asymmetric mitoses directed perpendicularly to the egg
surface produce a superficial blastoderm (Anderson, 1973). The
blastoderm gives rise to ectoderm and, through a gastrulation
process, to mesoderm. The endoderm arises either from the central
yolk-rich cells or from the mesoderm (Dawydoff, 1949; Haget,
1977; Campos-Ortega and Hartenstein, 1985).
Gastrulation occurs either by the invagination of a ventral midline
in the ectoderm or by individual cell introgression of the mesoderm
(Dawydoff, 1949; Anderson, 1973; Haget, 1977). This is
accompanied by the proctodeum and stomodeum, invaginations that
form the most anterior and posterior parts of the digestive system
and that guide the engulfment of the inner yolk mass and the
subsequent formation of the midgut. These movements co-occur
with signalling and might involve morphodynamic mechanisms.
Species that fit type C development include those arthropods in
which several segments become visible more or less at once and in
which later segments form progressively in a posterior sequence.
Segments form as ventral thickenings of the ectoderm; later on, the
ectoderm grows dorsally to displace the non-segmented ectoderm,
and the mesoderm grows dorsally in between the ectoderm and the
forming endoderm (Anderson, 1973).
In the Malacostraca class of crustaceans, posterior segments arise
from a posterior growth zone in which clearly ordered rows of
mesodermic and ectodermic teloblasts divide asymmetrically to
produce most of the cells in the posterior segments (Scholz and
Dohle, 1996). In many non-Malacostracean crustaceans, a
conserved free-living stage (nauplius larva) is produced first;
subsequently, additional segments arise through the asymmetric
division of mesodermic and ectodermic teloblasts in the posterior
part of the larva (Weygoldt, 1994). In myriapods (Chipman and
Akam, 2008), spiders (Dawydoff, 1949) and short-germ-band
insects (Anderson, 1973), segments also arise from a posterior
growth zone. Both proliferation and cell intercalation might be
involved in segment formation.
In type C developers, segmentation has been suggested to occur
through some autonomous or signalling-based clock-like
mechanism (Newman, 1993; Salazar-Ciudad et al., 2001; Peel et al.,
2005; Choe et al., 2006; Damen, 2007; Pueyo et al., 2008; Choe and
Brown, 2009; Pechman et al., 2009). At least in spiders
(Schoppmeier and Damen, 2005) and myriapods (Chipman and
Akam, 2008), the signalling molecules Notch and hairy have been
suggested to play a role in periodic segment formation. None of the
hypotheses proposed for periodic segment formation is
morphodynamic. Appendage development, at least for legs, involves
reciprocal signalling between cells co-occurring with intensive cell
proliferation during appendage growth (Angelini and Kaufman,
2005), and thus is likely to use strong morphodynamic mechanisms.
Thus, type C development is defined as morphostatic (or weakly
morphodynamic) in its early stages and as strongly morphodynamic
in later and in segment-specific development.
Variation in type C development has not been systematically
studied. Which anterior segments form first is variable between
species (Anderson, 1973; Haget, 1977). The number and type of
segments seems to be relatively conserved within major taxonomic
groups of arthropods. The expression patterns of the genes involved
in the early stages of segmentation do not seem to be widely
conserved (Liu and Kaufman, 2005). By contrast, the segmentation
genes themselves have widely conserved patterns of gene expression
among arthropods (Gibert, 2002).
Type D: long-germ-band insects
Type D development is similar to type C development except that it
is more morphostatic (including appendage development; Fig. 3D).
It is found in insects of the orders Hymenoptera, Diptera and
Lepidoptera
Drosophila melanogaster and most species of Diptera,
Lepidoptera and Hymenoptera have a long-germ-band development,
in which all segments form at the same time from a blastoderm that
covers the surface of the embryos. In Drosophila melanogaster,
substantial patterning occurs in the syncytium: transcription factors
diffuse between nuclei and activate their own transcription or that of
DEVELOPMENT
starlet sea anemone Nematostella vectensis, and different modes
of gastrulation have been suggested within Nematostella (Magie
and Martindale, 2007).
From early on in Nematostella development, two signalling
centres exist: one near the presumptive mouth that expresses fgf8
(Matus et al., 2007), wnt (Kusserow et al., 2005), dpp and chordin
(Rentzsch et al., 2006); and a second one at the other extreme of the
body that expresses fgf1 (Matus et al., 2007). These signalling
centres thus form an oral-aboral axis.
In Nematostella, apical constriction of the oral pole cells initiates
the bulging of the ectoderm in the blastocoel (Magie, 2007). These
cells develop filopodia with a strong adhesive affinity for the
blastocoelic side of the ectoderm. This pulling appears to be the
driving force for invagination. Several transcription factors start to
be expressed at different levels in the oral-aboral axis, in the
directive (dorsoventral) axis [a bilateral axis (Finnery et al., 2004)]
and in the growing endoderm.
Signalling appears to occur concomitantly with cell movements in
cnidarians. In Hydra (Bosch and Fujisawa, 2001), it has been
proposed that the relative proportion between two signals, one
diffusing from the aboral pole and another one diffusing from the oral
pole, could be responsible for the specification of intermediate
structures along the oral-aboral axis. If this is the case, simple changes
in body shape and size might not greatly affect the resulting pattern.
It is not clear, however, if such diffusion gradients are present in all
cnidarians or only in species with a high regenerative capacity.
Cell movements seem to be more extensive and to involve more
cells in type B than in type A development. Apparently, cells in the
early embryos of type B developers are not as differentiated from
each other as they are in the embryos of type A developers.
Accordingly, signalling seems to occur between larger collectives of
cells. Thus, it is likely that errors or small variations in signalling
will have proportionally milder effects than in type A development.
This is consistent with the large variability of early development and
with studies (Martin, 1997; Fritsenwanker et al., 2003) indicating
that cnidarian embryos are able to withstand substantial
rearrangements of cells and cell numbers. Later stages of
development are likely to also be variable (at least, there is
substantial variation between the adults of different species), and
thus cnidarians might fit the hourglass model within species, and
possibly also between species.
535
HYPOTHESIS
additional transcription factors (Gilbert, 2006). Pattern
transformation occurs by an inductive mechanism, in which
maternal genes (expressed in the anterior and posterior of the egg)
regulate a lower layer of gap genes (expressed in specific segments
along the anteroposterior sequence). These, in turn, regulate pairrule and segmentation genes, which are expressed as regularly
spaced stripes along the anteroposterior axis. Each stripe arises
through a combination of positive and negative inputs from genes in
the upper layer.
After cellularization, a well-studied hierarchical inductive
mechanism leads to the expression of anteroposteriorly oriented
stripes along the dorsoventral axis (Moussian and Roth, 2005). This
anteroposterior and dorsoventral patterning occurs without much
cell movement. Gastrulation consists of the invagination of a ventral
midline along the whole body length, similar to type C development
(Leptin, 1999). Extensive folding and movement of the ectoderm
also occurs during germ band elongation, retraction and closure
(Campos-Ortega and Hartenstein, 1985). Later movements co-occur
with cell signalling and could involve morphodynamic mechanisms.
Overall, type D development appears to be more morphostatic
than type C development (including appendage development), from
which it probably originated.
In insects, examples of type C and type D development can be
found even within species of the same genus. In general, most
arthropods have a relatively conserved segmented stage, late
developmental stages that lead to variable adult morphologies, and
early variation in the amount of yolk and in the number of segments
formed at once. Thus, the hourglass model, as initially proposed
(Ballard, 1981; Slack et al., 1993; Raff, 1996), could hold for variation
between species and, perhaps, within species.
Type E: vertebrates
Type E development is characterised by extensive cell signalling that
appears to occur concomitantly with extensive cell movements (Fig.
3E). In contrast to type B development, strong morphodynamic
mechanisms occur in relatively complex morphological contexts
(Fig. 2E). Type E development is found in vertebrates.
Compared with type A development, type E development does
not employ extensive cell signalling until the embryo has a large
number of cells. Even after the first signalling events, the embryo
is partitioned into territories that comprise large numbers of
equivalent or nearly equivalent cells (in contrast to type A
development).
The gastrulation of type E developers involves embryo-wide cell
movements. These movements are often associated with and
continued by the elongation of the body owing to extensive cell
intercalation (Keller et al., 2003). Gastrulation and elongation
movements co-occur with extensive cell signalling. During
gastrulation in Xenopus (Bouwmeester, 2001), zebrafish (Rohde and
Heisenberg, 2007), chicken (Mikawa et al., 2004) and mice (Tam
and Loebel, 2007), the expression patterns of multiple signalling
molecules and their receptors, such as Wnts (Tada and Kai, 2009),
FGFs (Lea et al., 2009), PDGFs (Ataliotis and Mercola, 1997) and
nodal (Chea et al., 2005), change over time and space (Heisenberg
and Solnica-Krezel, 2008). Thus, it is likely that the spatial
distribution of the cells that receive these signals depends on how
morphogenetic mechanisms move them, and on how they move and
deform the signalling territories (thus affecting, over time, the spatial
distribution of the cells that receive a signal). As such, vertebrate
gastrulation probably uses strong morphodynamic mechanisms
(Shook and Keller, 2008).
Development 137 (4)
The development of later organs, such as the brain, the limbs and
the teeth, has also been suggested to rely on morphodynamic
mechanisms (Salazar-Ciudad and Jernvall, 2002; Salazar-Ciudad et
al., 2003; Salazar-Ciudad, 2008).
The use of induction between larger groups of cells might allow
early variation in the number of cells that receive a signal to have
less dramatic effects on later development (as described), which
would make an hourglass pattern of variation between
developmental stages feasible. Except for mammals, this variation
seems to involve, mainly, the amount of yolk. This does not
necessarily have dramatic effects on adult morphology (del Pino and
Elinson, 1983; del Pino, 1989; del Pino and Loor-Vela, 1990),
although the morphogenetic movements involved can be quite
different (Shook and Keller, 2008).
Other types
At least cephalopods (Lemaire, 1970; Boletzky et al., 1989; Lee et
al., 2003), ctenophores (Freeman, 1976), clitelates (Shankland and
Bruce, 1998; Weisblat, 2007), some yolk-poor arthropods
(Weygoldt, 1994) and some yolk-rich echinoderms (Raff and Snoke
Smith, 2009) probably constitute their own developmental types
(although not enough information about them is available yet). In
spite of these gaps, the classification scheme set out above can be
helpful in shedding some light on certain evolutionary questions, as
detailed in the next section.
Developmental types and metazoan phylogeny
Type A development is found in the three main clades of metazoa:
Ecdysozoa (e.g. nematodes), lophotrochozoa (e.g. spiralian) and
deuterostomes (e.g. tunicates). This indicates that the common
ancestors of types C, D and E might have had type A
development. This possibility resembles the turbellarian-like first
hypothesis about metazoan phylogeny, according to which a
simple small animal with spiralian-like cleavage, as seen in some
extant turbellarians, is the ancestor of all bilaterians (Hyman,
1940; Salvini-Plawen, 1978). An alternative hypothesis, not
considered in Davidson’s classification, is the gastrea hypothesis
(Nielsen and Noerevang, 1985), which proposes that the origin of
Bilateria might be a gastrula-like organism that originated from
some cnidarian-like ancestor (presumably a type B developer).
This would imply that all developmental types originated from
type B, and that type A development would have appeared
multiple times as a secondary adaptation to the small body size of
planktotrophic and interstitial life-styles that are typical of many
current type A developers.
At a coarse descriptive level, there seems to be an association
between developmental type and some aspects of the body plan
(with several phyla using the same developmental type), and this is
the first hypothesis that I propose in this article. Phyla that use type
A development tend to be small and to have relatively simple body
plans with few cell types, each of which is preferentially localized
to one part of the body (Davidson, 1991; Davidson et al., 1995), and
with organs composed of one or only a few cell types that are
derived from the same germ layer (Bell and Mooers, 1997; Bonner,
2004). Type C and D developers have body plans that can be
considered as more complex because they have more cell types (Bell
and Mooers, 1997). In addition, each of these cell types is not
exclusive to one part of the body, but is distributed in iterated
patterns along the anteroposterior axis, and functional organs are
often made up of several cell types (with each organ having a
specific pattern). The same occurs in type E developers, but with a
DEVELOPMENT
536
less clearly iterated pattern than in type C and D. Type B developers
tend to have larger bodies than most type A developers, but have few
cell types, and these are generally arranged in only two epithelia.
This first hypothesis could be tested by looking at the
development of more species within each group. If the hypothesis is
correct, species in the same phylum should have the same type of
development. Exceptions would be expected for species with a body
plan that is substantially different from that of the rest of the phylum
(for example, for cephalopods among molluscs, or for cirripeda
among crustaceans). Most phyla with simple and small bodies are
still poorly understood at the developmental level. Hypothesis 1
would be falsified if these species do not employ type A
development. Note that this requires experimental work on
development that not only focuses on identifying genetic
interactions, but that also studies morphogenetic movements and
how these affect and are affected by signalling.
Davidson’s classification (Davidson, 1991) is similar to the one
proposed here, but neither the importance of morphogenetic
mechanisms nor the distinction between morphodynamic and
morphogenetic mechanisms is considered in detail. Davidson’s type
I is comparable to the type A described here, whereas his type II is
similar to types C and D. Additionally, his classification combines
vertebrate and cnidarian development; here, these groups are
assigned to the separate types E and B.
The second hypothesis that I propose states that species with the
same type of development exhibit commonalities in morphological
variation and in the genotype-phenotype maps that they produce.
The extensive use of morphostatic and weak morphodynamic
mechanisms in type A development would allow, in accordance with
this hypothesis, gradual variation and a relatively simple relationship
between genotype and phenotype. This could facilitate fast
responses to small but frequent changes in selective regimes. Thus,
type A development might not just be ancestral; it could also be a
very adaptive way to generate small body plans in which each part
can be changed in a relatively independent way.
Hypothesis two can be empirically falsified by looking at the
patterns of morphological variation that arise in groups that employ
different types of development. Type E development should
produce, within a species, variation that differs more between
individuals compared with type C and type D development, and
especially compared with type A and type B development.
Comparisons between phenotypes that arise through mutation
(Driever et al., 1996; Kamath et al., 2003) or between mutation
accumulation lines should indicate whether, as expected, type E
development produces a more complex genotype-phenotype map
than type C and type D development, and especially a more complex
one than types A and B.
The third hypothesis that I propose states that different types of
development correlate with different amounts of variation at
different stages of development. This hypothesis is summarized in
Fig. 3 (as discussed in the previous sections) and could be falsified
by directly measuring the variation among individuals within a
given species at different stages of development and by comparing
these patterns of variation between different species with similar and
different developmental types. There are some studies partially
addressing this question by using discrete characters (Poe and Wake,
2004) but, as of yet, no morphometric data are available.
The evolution of type E development
In principle, large complex body plans, such as those of
vertebrates, could be produced through short-range cell-to-cell
inductions and through the late activation of morphogenetic
HYPOTHESIS
537
mechanisms, as is the case in type A developers. If this is so, then
why do vertebrates make such extensive use of morphodynamic
mechanisms? The discussion above suggests that morphodynamic
mechanisms are able to produce more diverse and also more
complex morphologies for a given genetic complexity. Thus, on
average, fewer genetic changes are required to attain a (adaptive)
pattern with morphodynamic mechanisms than with morphostatic
mechanisms. The fourth hypothesis that I propose states,
correspondingly, that complex body plans have evolved owing to
a gradual transition towards developmental types with a higher
interdependence between cell signalling and morphogenesis.
Consequently, type E development might not have evolved
because of an adaptive advantage, but because it is a simpler way
(i.e. one requiring fewer mutations) to produce larger and more
complex body plans. In that sense, type E development could
have evolved through an increase in the amount of time in which
inductive mechanisms act together in a type A development
setting, or by allowing their interdependence (if type E evolved
from type B). Hypothesis 4 could be falsified by checking
whether, among chordates, a simpler morphology (for example,
that of lampreys and hagfish) correlates with a more extensive use
of morphodynamic mechanisms, especially if this simplicity is
not the outcome of secondary evolution from a more complex
morphology.
It is interesting to note that, except for molluscs, type A
developers tend to have, as mentioned, relatively simple body plans
as adults compared with those of type C, D and E developers.
Cephalopods are probably among the largest and most complex
molluscs; interestingly, they do not seem to use type A development
either (Lemaire, 1970; Boletzky et al., 1989).
It has been suggested (Newman et al., 2006) that early metazoa
did not use type A development, but morphogenetic and reactiondiffusion-like inductive mechanisms that led to early variable
morphologies with a complex relationship between genotype and
phenotype and to relatively large sizes, as seen in the Ediacaran
fauna (Xiao and Laflamme, 2009). In this scenario, type A
development could have evolved as an adaptation to small body size.
The evolution of type C and type D development
The evolution of type C development from type A development
might also have been associated with an early increase in cell
number and with a relative temporal delay of major early
inductive events. The adaptive radiation of arthropods has been
suggested to correlate with the specialization of their multiple
appendages (Williams and Nagy, 2001; Minelli and Fusco, 2005;
Angelini and Kaufman, 2005; Adamowicz et al., 2008). This
could correlate with the larger independence between parts that is
possible in morphostatic mechanisms and with the use of
morphodynamic mechanisms for appendage development (except
in type D).
Type D development might have arisen as a morphostatic
derivation of type C development. This could correlate, at least in
drosophilids, with the relatively small amount of morphological
divergence compared with the number of species and the vast time
periods since the divergence from common ancestors in each group
(Tamura et al., 2004). It has been suggested that new morphostatic
mechanisms that arise (or are recruited) through mutations and that
are able to produce the morphologies originally produced by
morphodynamic mechanisms would be favoured by conservative
selection (Salazar-Ciudad and Jernvall, 2004), and thus would lead
to the apparent canalization or conservation of drosophilid
morphology.
DEVELOPMENT
Development 137 (4)
HYPOTHESIS
Conclusions
In this article, I suggest that, in spite of the contingent nature of
evolution, general inferences about the evolution of development
and its effects on morphological evolution might be possible. This
work draws some conclusions about how different types of
development could influence the patterns of morphological
evolution in a group and how the overall structure of development
itself might evolve. More detailed analyses of development types
and of their phylogenetic distribution, together with analyses of the
patterns of morphological variation within groups, will probably
become available in the near future and might refute or refine the
hypotheses proposed above.
Acknowledgements
I thank Stuart Newman, Janna Fierst, Ronald Jenner, Scott Gilbert and David
Vicente Salvador for useful comments. This work was supported by the Ramón
y Cajal program.
Competing interests statement
The author declares no competing financial interests.
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