Contributions to Zoology, 71 (1/3) 101-113 (2002)

SPB Academic Publishing bv, The Hague

and in of Divergence convergence early embryonic stages metazoans

Frietson Galis ¹ & Barry Sinervo2

1 Institute ofEvolutionary and Ecological Sciences, Leiden University, P.O. Box 9516, 2300 RA Leiden,

2 Netherlands, [email protected]: Biology’ Department, University of California Santa Cruz, [email protected].

Keywords: evolutionary conservation, pleiotropy, cleavage, , organogenesis, multicellularity,

Abstract and in Conservation, convergence divergence patterns

of gastrulation 104

and in Conservation, convergence divergence early The early stages oforganogenesis in metazoans differ drastically organogenesis 106 between order such and classes. The higher taxa as phyla seg- What conservation of of causes early stages organo- mented in the of germ band stage insects, nauplius stage crus- to the at genesisrelative divergence seen other taceans, and the neurula/ stage in are stages 109 examples ofthis diversification. In striking contrast with this Modularity and the divergence of form in late is divergence, the similarity of these stages within these taxa, organogenesis 110 i.e., within insects, crustaceans, and vertebrates. The early sta- The relationship between divergence of early and of ges organogenesis, orphylotypic stages, have, thus, remained late ontogenetic stages 111 in very similar most species since the evolutionary origin of the Early diversification foloowed by stasis of early taxa. These phylotypic stages are considerably more similar to stages of organogenesis 111 each otherthan to the earlier stages ofcleavage and gastrulation. Conclusion 111 Cleavage and gastrulation stages display not only great variability, Acknowledgements 112 but of also striking examples apparent convergence among species References 112 in different for in the of phyla, example many cases epiblastic

in This leads the situation cleavage yolk-rich eggs. to paradoxical that the overall similarity ofcleavage and gastrulation stages is in than of Introduction general higher among metazoans the early stages of organogenesis, but within phyla and classes the situation is the

We discuss reverse. data on cleavage, gastrulation, and early The of early stages cleavage and gastrulation are organogenesis and evaluate possible causes for conservation, often similar remarkably among metazoans (Gil- homoplasy, and diversification in an attempt to throw light on bert and Raunio, 1997; fig. The this situation. 1). succeeding stage, paradoxical In addition, we discuss a hypothesis is far diverse has to the organogenesis, more meta- that been proposed explain diversity of early stages among than and of organogenesis at the level of metazoans and the similarity zoans cleavage gastrulation (Gilbert and

and within many phyla classes. Raunio, 1997). Paradoxically, embryologists have

for noticed a long time that within most higher order

taxa, e.g. or class, early organogenesis is Contents considerably less variable than earlier stages (Seidel,

1960; Anderson, 1973; Sander, 1983; Hall, 1996;

Introduction 101 Elinson, 1987). In particular when we judge simi- due to Similarity conservation or homoplasy 102 larity relative to the number of options available and in Conservation, convergence divergence patterns of for the stage under consideration. Towards the end cleavage 102 of diverse Mechanistic causes of cleavage patterns 102 gastrulation relatively ontogenetic pat-

terns Understanding of diversity 103 converge to a highly similar stage. Examples

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of such similar celled limited highly stages during early organo- stage. Only a number of permuta-

in genesis are: the extended/segmented germ-band tions are possible with a few undifferent-

stage of insects, the nauplius stage of crustaceans, iatedcells. In contrast, the diversity ofmulticellular

and the neurula/pharyngula stage of vertebrates clonal propagules, which lack such a reset to a single-

(Seidel, 1960, Anderson, 1973; Sander, 1983; Elin- celled stage, is indeed remarkably high.

arises because ofeither similar selec- son, 1987; Hall, 1996; Grbic, 2000; Dahms, 2000; Similarity

Galis et al., 2002). During cleavage and gastrula- tion pressures and/or stringent constraints. In the

conservation of tion the overall case of constraints, similarity among metazoans is, thus, morphological

greater than during early organogenesis, but, within patterns arises either because no genetic variation

is or because many higher order taxa the reverse is the case and produced, invariably negative pleio-

effects are associated with similarity is higher during early organogenesis than tropic changes. Similarity in have four during cleavage and gastrulation. For instance, the a phylogenetic context, thus, can causes;

rapid divisions during cleavage of polyembryonic 1) shared ancestral traits insects and mammals resemble each other more than plesiomorphy, (inherited similarity evolved once); the segmented germband stage and the neurula/ 2) synapomorphy, shared derived traits (novel simi- pharyngula stage, respectively, i.e., the early orga- larity evolved once); nogenesis stages (see below). On the other hand, due to common within mammals of different 3) homoplasy adaptational pres- phylotypic stages spe-

sures, or cies are more similar than cleavage and gastrula- 4) homoplasy due to developmental constraints tion stages and the same holds for the segmented derived traits band in To (convergent adaptive promoting germ stage insects (see below). under- trait correlation). stand the evolutionary origin of this counterintuitive

situation it is necessary to know whether similar-

ity is the result of conservation, convergence, or Conservation, convergence and divergence in parallel evolution. patterns of cleavage

Mechanistic causes of cleavage patterns Similarity due to conservation or homoplasy

During cleavage, the zygote rapidly divides into It is assumed that usually similarity among early smaller cells. many Patterns of cleavage are deter- is the result of embryonic stages evolutionary con- mined of by a small number mechanistic factors, servation (Seidel, 1960; Sander, 1983; Buss, 1987; variation in which allows a high diversity of cleav- Even Baer Raff, 1996; Hall, 1996). though von One mechanistic age patterns. factor is the amount

did not believe in evolution (1828) by descent, and distribution of vitelloprotein within the zygotic he was the first to that early changes in ' propose cytoplasm (Gilbert, 2000). Yolk impedes cleavage. ontogeny were more likely to have cascading con- In with little zygotes yolk, cleavage usually sepa- than later when of devel- sequences changes most rates the into distinct cells (holoblastic

has taken place. Although this in opment already cleavage, as sponges, sea urchins, lancelets, most

constraint is real In evolutionary undoubtedly (Buss amphibians and mammals). zygotes with a large its has recently been 1987), importance challenged yolk component, cleavage only occurs in the part

the revelation of considerable variation in of by early the cytoplasm with little or no yolk. Cleavage

In embryonic stages. addition, evolutionary con- proceeds only in this part (meroblastic cleavage), servation of early embryonic stages may be less leading in cephalopods, fishes, reptiles and birds strong than previously thought because of similar- to a germinal disc on the surface of a large yolk ity due to convergent or parallel evolution (ho- mass (epiblastic cleavage, Figs, la and b), and in moplasy). Similarity is almost unavoidable in the some crustaceans and some insects to a superficial early ontogenetic stages of metazoans because of layer of embryonal cells with yolk in the center the complete reset that occurs at the initial single- (periblastic cleavage). For example, most amphib-

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I. Fig. Convergence. Meroblastic, epiblastic cleavage in the (A) cephalopod Loligo pelalei (after Claus and Grobben, 1917) and (B) in the longnose gar Lepisosteus osseus (after Balfour, 1881).

ians exhibit holoblastic cleavage. However, eleu- Nutrients obtained can be from either yolk, ma-

therodactyline frogs with derived yolky also ternal eggs tissues, or the environment. Specializations have secondarily derived epiblastic cleavage (Elin- for nutrition embryonic uptake can arise as Given the son, 1987). adaptive value of high yolk a direct of consequence constraints, e.g. yolk con-

volume for progeny survival and the extreme con- straints (see above), or as adaptations to specialized

of or vergence epiblastic periblastic cleavage among conditions. For example, evolution of mammalian diverse taxa, cleavage mechanisms thus, to appear, viviparity has led compaction, a conspicuous

constrained to evolve as a result of selection for in specialization which loosely arranged blastomeres nutrient rich eggs (cause 4, above). huddle and suddenly together form a compact mass The second mechanism is the and angle timing (Gilbert,, 2000). Compaction and associated intra- of mitotic spindle formation, and thus, the orienta- cellular changes function during embryonic implan- tion of cleaving cells: (various spiral protostomes), tation in the uterus. Compaction is involved in the

radial (various deuterostomes), and rotational of the (mam- separation inner cell mass (from which the mals) cleavage. embryo will develop) from the trophoblast (which The third mechanism is differential cell adhe- provides fetal contributions to the placenta). Inter- sion. Differential adhesion can cause important shape estingly, polyembryonic insects have independently for instance in differences, compaction in mam- evolved compaction, together with early separation mals and polyembryonic in which blas- of wasps, embryonic and extraembryonic cell lineages tomeres are not loosely packed but very closely (Grbic et a! because ., 1998), presumably endopara- in joined together; or coeloblastulas, in which the sitism similar imposes spatial constraints as vivi- blastula is hollow of a ball of cells instead a solid of parity (an example cause 3 above). ball as in stereoblastulae. Locomotor demands also influence cleavage (Buss, 1987). Free-living dispersal stages have ex- Understanding of diversity and similarity ternal ciliated cells and internal dividing cells. This

configuration appears to be largely the result of in Diversity can be understood locomotor cleavage patterns demands combinedwith a universal meta- in terms of for life such adaptations embryonic as zoan constraint (an of example cause 1) - cells nutrient and maternal deter- uptake, locomotion, cannot divide when ciliated (Buss 1987). Metazoan mination. cells have only one microtubule center, which can

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be used either for a mitotic spindle or for cilia, axons, Conservation, convergence and divergence in

dendrites and other microtubular specializations. patterns of gastrulation

Thus, cilia are concentrated on the surface and

dividing cells without cilia are inside propagules During gastrulation, the blastula undergoes a se-

to prevent interference with locomotion. ries of dramatic morphogenetic movements that

Maternal determination. Buss (1987) argued that result in a multilayered embryo, the gastrula. Mor-

selection for maternal determination has the of that lead shaped phogenetic processes gastrulation to evolution of cleavage. Determination of early de- germ-layer differentiation are bewilderingly diverse.

via maternal factors that contribute velopment cytoplasmic pro- Processes to gastrulation are:

vides a powerful means for the mother to prevent

of cell line the of oth- where sheet of cells proliferation one at expense a) invagination, a moves ac-

thus establish selection the level of into the blastula towards the side ers, helping at tively opposite

the individual. The amount of development under (Fig.2a);

in maternal control is necessarily limited; only a fi- b) unipolar ingression, which individual cells

nite number of maternal cytoplasmic factors can migrate inwards at one end of a blastoderm be provided to the zygote. Unequal cleavage po- (Fig.2a);

tentially increases effectiveness of maternal con- c) multipolar ingression, in which individual cells

trol. In unequal cleavage, some cells differentiate migrate inwards from all points of the blasto- and begin zygotic transcription (end of maternal coel;

control) and thus lose the capacity to become germ d) epiboly, the migration of apical cells over the

cells, whereas others continue as undifferentiated other blastula cells, thus forming an external and divide under maternal control. Differentiated layer of cells (Fig. 2b);

cells usually lose the capacity to divide, which is e) involution, the moving in of a layer of cells so

become cells. Un- that it the inner side of the why they can no longer germ spreads over outer

equal cleavage typically occurs in taxa with spiral layer of cells (Fig. 2b);

cleavage such as turbellarians, annelids and mol- f) primary delamination, in which the cells of a

luscs (Buss, 1987). blastoderm divide such that one daughter cell

is Polyembryony. Cleavage radically different remains at the surface and the other one moves

in polyembryonic parasitic wasps relative to other to the interior (Fig. 2c); and

insects (Grbi et al, 1998). Cleavage is holoblas- g) secondary delamination, in which a solid tis-

cells tic, and the zygote produces not one, but many sue of segregates into two layers. Usually

small Cellularization combinations of form of embryos. occurs immediately, these processes part

whereas in most other insects droso- and (including gastrulation, e.g. invagination multipolar

first divide into philids) nuclei a syncytium and cellu- ingression (Fig. 2a), involution and epiboly (Fig.

larization occurs later. Further specializations of' 2b).

compaction and early separation of embryonic and

extraembryonic tissues (see above) are probably The combinationof possibilities has led to a wide

caused the which is to of and by endoparasitic lifestyle, a variety morphogenetic processes between

certain extent convergent with viviparity in mam- within phyla and other higher taxa. Cnidarians, for

mals, i.e., living in another organism. example, exhibit seven different types of gastrula-

In conclusion, cleavage patterns are diverse, but tion (Gilbert and Raunio, 1997). In insects, there

important similarities occur because of evolution- are drastic differences in gastrulation between short,

due to similar and band ary convergence embryonic adapta- intermediate, long-germ insects, polyem-

tions and constraints. The most even more derived. Within striking examples bryonic wasps being of convergent embryonic adaptations are compac- teleosts and mammals, gastrulation is highly vari-

tion in mammals and polyembryonic insects and able (Collazo et al, 1994; Viehbahn, 1999); for

in the disc of rodents is epiblastic cleavage yolk-rich embryos. example, embryonic cup-

instead of and inverted shaped flat, germ layers are

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Fig. 2. of and (A) Diversity gastrulation. Invagination unipolar ingression during gastrulation in the echinoderm Holothuria tubulosa Balfour (after 1881). (B) and involution in the echiuranBonellia viridis in Epiboiy (after Spengel Balfour 1881). (C) Primary delamination in the cnidarian Geryona spec, (after Claus and Grobben, 1917).

with endoderm outside and ectoderm inside. in as cleavage, mainly related to locomotion and

Gastrulation is diverse but also characterized nutrient and by uptake. Viviparous oviparous gastru- similarity due to similar constraints and selection lating embryos have numerous adaptations relevant pressures. The important selection toward in pressures are, living eggs and other maternal tissues

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(Gilbert and Raunio, 1997; Grbic, etcil, 1998). The enabling embryonic inductions; neurulation is a

constraint on simultaneous ciliation and cell divi- classic example. The infinite diversity of subse-

sion of blastulae also holds for free-living gastru- quent organic forms arguably begins with such

lae and leads again to ciliated outer cells (Buss, inductions of tissue layers and organ systems. How-

constrains dur- in order 1987). Yolk also cell movements ever, to develop organ systems, inductive

cell ing gastrulation such as in the organizer region events require topologically adjacent popula-

(Arendt and Nubler-Jung, 1999); the blastoporal tions, a requirement that seems to form a stringent

constraint the of canal of reptiles and primitive streak of birds and spatio-temporal on outcome gas-

trulation. mammals are presumably specializations associated

with this constraint.

Further constraints follow from the type of blastula Conservation, convergence and divergence in present at the start of gastrulation. In blastulae with early organogenesis an outer layer of ciliated cells, for instance, epi-

is would boly not possible; dividing cells cover After germ layers are formed during gastrulation, ciliated cells and preclude locomotion (Buss, 1987). cells interact with one another and rearrange them- Invagination is only possible in hollow blastulae selves This during organogenesis. stage among meta- (cocloblastulae). In solid blastulae, such as blasto- zoans is far more diverse than earlier discs and stages. stereoblastulae, invagination is not pos- However, as mentioned before, within most high sible, and rather epiboly plays an important role. order taxa, early organogenesis is far less variable As noted above, this is an example of cause 4, in than earlier stages (Seidel, 1960; Sander, 1983; Hall, which adaptative evolution of embryonic nutrition 1996; Elinson, 1987). Examples of great similarity promotes correlated adjustments in other develop-

of occur the mental post-gastrulation stages during seg- processes. mented germ-band stage of insects, the nauplius Diversity of gastrulation and cleavage patterns stage of crustaceans, and the neurula/pharyngula are mirrored by diversity of genetic interactions at of vertebrates (Figs 3 and 4; Sander, 1983; the molecular level. Comparisons of well-charac- stage Grbi et al., 1998; Dahms et al, 2000). Recent data terized taxa (insects versus vertebrates) show that

on interactions confirm that within-taxa networks genetic gene underlying early development al- similarity is highest shortly after gastrulation low for substantial molecular reorganization (Hol- (Da- 2000, Holland, 2000). For land, 2000; Damcn etal, 2000; Staubcr etal mcn, example, expres- , 2001). sion of segment-polarity and Hox However, evolutionary conservation is probably also patterns genes

in insects are more similar to each other than those important (dc Robertis et al, 1994). Holland (2000) of earlier concludes, for example, that there are similarities acting genes.

in The distribution of these gene expression during protostome and deuteros- phylogenetic patterns of of that simi- tome gastrulation, but it is not clear to what extend early stages organogenesis suggests

is due to conservation and not they arise from actual conservation as opposed tos larity convergence

Sander convergence. (Damen, 2000). (1983) introduced the term

The larger number of cells during gastrulation, phylotypic stage, as these stages can be seen as

increased levels of and for the or taxa to which differentiation, large per- typical phylum higher they

mutations of interacting processes generate near belong. Although phylotypic stages are more con-

infinite variation in served than earlier or later gastrulation patterns. Yet, para- developmental stages,

the not doxically, process of gastrulation is far more we are suggesting that there is not important diverse than the final end product, gastrulae invari- variation (see for example Minelli and Schram; 1994

have two and ably or three germ layers never more Richardson, 1999); rather, what matters is that there (Hall, 1999). Organ systems emerging from germ is less variation than at earlier and later stages. layers arc similarly conserved; skin and nervous Apparently developmental stages evolve at differ- from ectoderm; system digestive tube from endo- ent rates, and constraints to evolutionary change derm. A outcome of the key of are after process gastrula- particularly strong at stages shortly gas- tion is that sheets of cells come into thus contact, trulation when axis patterning occurs.

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Fig. 3. (A) similar in Early organogenesis stages are very crustaceans. Nauplius stages in (A) Cyclops (from Dawydoff 1928). (B) Cirripedia species (from Claus and Grobben, 1917).

4. in vertebrates Fig. Early organogenesis stages are more similarthan earlier or later stages. Especially within amniotes the similarity is striking. Pharyngula stage in (A) Lacerta and (B) human (from Keibel 1904 and 1908).

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Fig. 5. Schematic robustness and effective When is figureexplaining (A) (B) modularity. (A) a parameter changed in a robust genetic

the not network, resulting phenotype does change (in this case illustratedwith the concentration of wingless (wg) and hedgehog (hh)

in the of the cells Modules are discernible and discrete units within ectoderm), (B) large genetic networks that have some autonomy and a clear location physical (Raff 1996). They can differ in the amount of connectedness. First ofall, all input to robust elements of

a module can be ignored, since it will have discernible no effect. A large proportion of robust components in a module therefore reduces potential connectivity. Low connectivity, with few connections having .small effects, implies high effective modularity. High

connectivity implies low effective modularity. From Galis et al. 2002

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Table Predictions of extended and What causes conservation of early stages of I. the robustness pleiotropy

relative hypotheses. organogenesis to the divergence seen at other stages? Effects ofmutations

Pleiotropy Robustness As there is abundant intra-specific genetic varia- hypothesis hypothesis tion for phylotypic stages of vertebrates and in- sects (Galis et ah, 2001, Galis and Metz, 2000, Gabs genetic mutational visible at the

variation phenotypic level hidden et ah, 2002), it would appear that conservation must, direct phenotypic effects potentially large small thus, result from strong stabilizing selection against dominance of direct haplo-insufficiency recessivity or mutations (Causes 1 and 2). Sander(1983) and Raff effects possible near recessi- that the of inter- (1996) hypothesize high degree vity action between modules is the major cause of pleiotropic effects many few conservation in the phylotypic stages. This high

interactivity (low effective modularity) causes mu- tations to effects that have multiple pleiotropic Wagner, 2000; Gibson and Wagner, 2000). There- become as As amplified development proceeds. fore, they suggest that conservation of the network effects ofmutations pleiotropic during embryogen- occurs despite accumulation of genetic changes esis are generally disadvantageous (Hadorn, 1961; because these changes have little phenotypic ef-

Wright, 1970) strong stabilizing selection against fect and mainly lead to hidden variation. The Ro-

mutations ensues. In this scenario, conservation is bustness Flypothesis was only proposed for the

due to selection muta- consistently strong against conservation of the segment polarity gene network tions via their effects. The interac- pleiotropic high during the phylotypic stage. Flowever, this stage

tivity betweenmodules an destabilized implies easily as a whole is conserved, and as the segment polar-

network of inductive events. Therefore, the effec- central ity genes act as an organizer to most pat- tive robustness is low Galis and Metz (Fig. 5). (2001) terning events during this stage, the hypothesis would studies in vertebrates recently analysed teratological need to be extended in order to have the presumed for of mutational reported phenocopies change. They evolutionary consequences. The Pleiotropy Hy-

found support for the of Sander and Robustness lead strong hypotheses pothesis Hypothesis to very and Raff (1983) (1996). Furthermore, they argue different predictions for mutations affecting the

that the low effective in the inductive modularity phylotypic stage (table 1). When evaluating the

interactions is the root for the not only cause conser- empirical evidence for these hypotheses in Droso-

vation of the as a whole, but also phylotypic stage phila, Galis et al. (2002) found strong support for for the much discussed and co- temporal spatial severe phenotypic effects of mutations, including

linearity of the Hox that characterizes this genes cascading pleiotropic effects. In addition, they found

stage. little evidence supporting effective robustness of Von Dassow and 2000) colleagues (1999, pro- the segment polarity network, or for interactions

posed an alternative for the hypothesis conserva- of the Hox genes or the organization of the stage tion of of the striped expression segment polarity as a whole.

genes the in the during phylotypic stage insects, There are probably two reasons for the discrep-

segmented (and extended) band stage. They between the robustness for germ ancy predicted strong hypothesized that robustness of the segment polar- mutations by von Dassow and colleagues and the dy network within each should gene segment pro- weak robustness actually found. First, the organiz- vide a buffer effects of mutational function against phenotypic ing of segment polarity genes causes mu- In changes. robust networks, definition, tations in these have cascade of gene by genes to a pleiotropic

developmental noise and mutations do not lead to effects with and many auto-regulatory cross-regu- dear phenotypic effects because interactions gene latory interactions that provide a feedback on the tend to neutralize and in perturbations particular input of the segment polarity gene network. This m ake mutations recessive and Bums, 1981; (Kacser leads to a relatively low effective modularity and

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robustness. This feedback that modulates the axis input thyroid (HPT) governs metamorphosis (Hayes,

ofthe network is absent in the model of von Dassow 1997a,b) and is developmentally uncoupled from

al. concentration differences of the et Second, gene hypothalamic-pituitary-gonadal (HPG) axis,

products appear to have a crucial impact upon mor- which governs sexual maturation. This uncoupling

which leads sensi- has allowed for the evolutionof heterochronic phogenetic patterning, to a high many

tivity of the system to changes. Why has more changes, including paedomorphic lineages in urode-

robustness not evolved? Perhaps, within these stages les, e.g., Sirenidae, Amphimidae, Proteidae, Crypto-

the total number of interactions involved in mor- branchidae Gould, 1977). The uncoupling has further

phogenetic patterning is too limited to organize the allowed the evolution of alternative feeding mor-

in modular allow in larval anurans. pattern an independent way to phologies

greater robustness. The vulnerability to mutations In urodeles, deletion of thyroxine regulation has

of the conserved in led loss of the terrestrial adult most stage vertebrates, thus, to a phase and pae-

be shared the conserved larval forms in which sexual appears to by most stage domorphic matura-

A in insects. This points to an important role of pleiot- tion occurs in the juvenile form (Gould, 1977).

and selection in con- loss-of-function mutation in endocrine ropy stabilizing evolutionary simple an

servation. gene of major effect governing thyroxine regula-

Why are these early stages of organogenesis more tion is responsible for the evolutionary transition

conservedthan earlier and later stages? Earlier stages of the axolotl, Ambystoma mexicanum, which is

in from the A. are simpler form and for this reason mutations derived ancestral tiger salamander,

will probably have more of a chance to be success- tigrinum, which retains larval metamorphosis (Voss

ful, since it is more difficult to destabilize a simple and Shaffer, 1997). The deleterious pleiotropic ef-

such pattern than a more complicated pattern. Later stages fects of mutations arc presumably small be-

of organogenesis involve a higher number of in- cause ofmodularity of the endocrine system. Such

ductive interactions than during the phylotypic stage, modularity allows major potential to evolve.

which presumably allows a higher degree of modu- High thyroxine titer does not always induce an

larity. A high modularity implies that the effects aquatic-terrestrial metamorphosis because tissue-

of other mutations will mainly be limited to the module specific receptors and endocrine axes modu-

itself and not to other parts of the organism, which late the tissue-specificity of thyroxine. For example,

in turn increases the “evolvability” of the compo- prolactin promotes growth under low “stress”, but

under if the level the nent parts. stress, e.g., water drops, hy-

Let us examine an of a mechanism that axis example pothalamic-pituitary-adrenal (HPA) can rap-

promotes divergence after the phylotypic stage via idly trigger metamorphosis (Hayes, 1997a,b; Denver,

modularity, the role of modular endocrine regula- 2000). A beautiful example at a fine scale of modu- tion in promoting divergence. Furthermore we can larity provides the thyroxine-induction of anuran

how of late then perhaps see divergence ontoge- larval feeding structures (Hanken, 1988). In spade-

netic stages is strongly influenced by the divergence foot toad tadpoles, Scaphiopus spp., thyroxine

of early ontogenetic stages. ingestion induces a precocious transformation of

structures associated with the cranium into more

Modularity and the divergence ofform in late adult-like ones (Pfennig, 1992). Tadpoles in this organogenesis way adopt a carnivorous form if they ingest shrimps

(which contain high levels of thyroxine (Pfennig,

This The endocrine control of late organogenesis is for- 1990, 1992). precocious response to thyrox-

ine has evolved times in with carnivo- matted into modules and allows for considerable many taxa potential to evolve. A classic example involves rous larvae and finds an extreme morphological thyroxine regulation of amphibian metamorphosis expression in species that have evolved cannibal- during larval development, which has become ism (Hanken, 1993; Pfennig and Collins, 1993). uncoupled from the development of reproductive structures of the adult. The hypothalamic-pituitary-

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The relationship between and divergence ofearly Early diversification followed by stasis of early late ontogenetic stages stages of organogenesis

The processes that lead to the evolution of The of of large diversity early stages organogenesis among yolk-rich eggs arises apparently from di- mainly phyla and the similarity within several phyla and rect selection on later stages of development. Egg other higher order taxa suggests an early phase of size and the yolk content are result ofmaternal effects diversification the rapid in evolution of metazoans, and can increase the course ofevolution to a thresh- followed by evolutionary stasis of these discrete

old size where the feeding larval form can be lost taxon-specific stages. Buss (1987) has proposed the and a non-feeding larval form evolves (Vance, 1973; following explanation for this phenomenon. The Raff, 1996). Divergence of early stages, thus, fa- diversification early rapid has happened during the cilitates the divergence of later stages also (see early chaotic phase in the evolution from unicellu- Sinervo and McEdward, 1988). The evolution of a lar to multicellular individuals (presumably dur- non-feeding larva from a feeding larva further ing the Cambrian explosion). During the evolution facilitates the evolution of direct development al- of individuality the level of selection has shifted

even more Direct lowing divergence. development from individual cells to that of the individual. Early has evolved many times independently in diverse during this transition, somatic mutations in cells taxa. The following example of plethodontid sala- that could gain access to the reproductive cells had manders shows how direct development can lead a chance to be maintained in future generations (as to further specialization and divergence. occurred in plants). Later, when selection was firmly Plethodontid salamanders undergo direct devel- established at the level of the individual, heritable in and opment large yolky eggs the juveniles hatch mutations were limited to those that happen both into a miniature adult form. During metamorpho- in the and in the short germ-line, period before germ- sis in most salamander families, hyobranchial ele- line sequestration. This scenario is intuitively that ap- ments form larval gills are transformed into but pealing, surprisingly little research has yet been the tongue projection feeding apparatus of terres- carried out to further investigate this trial important adults. In contrast, in plethodontids where in question evolutionary biology. Mutagenesis ex- aquatic larval function was lost during the evolu- periments with simple colonial and theo- tion of direct organisms development, hyobranchial structures retical modeling could probably contribute to a better develop directly for adult function. In addition, the understanding. groupevolved a lungless condition, respiring through

the skin and buccal cavity. Freedom from both

feeding and respiratory constraints allowed elabo- Conclusion rate tongue projection mechanisms to evolve in some

plethodontid salamanders as is seen in the bolito-

glossines Rapid progress that has been made in understand- (see Wake and Larson, 1987). This ex- ing and of ample, thus, illustrates how the evolved maternal genetic morphogenetic patterning sev-

effects eral invertebrate and model allows on egg size have led to a breaking of func- species to in tional us determine cases whether constraints on development and form thereby many similarity

arises from conservation or Unfortu- allowing novelty to arise. Interestingly, at the same convergence. for invertebrate time new nately, taxa, we lack crucial constraints arose (yolk that impedes cell many information that allows for division) promoting evolutionary conservation of meaningful interpreta- earlier tions. that ontogenetic stages. Emergent patterns suggest at least two

The evolution of in amniotes via phenomena are responsible for the phenomenon that vivipary egg

retention overall within metazoans is (Laurin et al. 2000) provides another exam- similarity greatest during ple of how the early embryonic of cleavage and divergence in early ontogenetic stages stages gastru- allows diversification of later lation, whereas in ontogenetic forms by yet many taxa early organo-

niches to genesis is more similar and conserved. allowing be filled that cannot be filled by First, the of egg-laying animals. similarity cleavage and gastrulation is not only

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