INTEGR. COMP. BIOL.

, 43:3–10 (2003)

The Origin of Metazoan Complexity: Porifera as Integrated Animals1

WERNER E. G. MÜLLER2
Institut für Physiologische Chemie, Abteilung Angewandte Molekularbiologie, Universität,
Duesbergweg 6, D-55099 Mainz, Germany

SYNOPSIS. Sponges [Porifera] are the phylogenetically oldest metazoan phylum still extant today; they share
the closest relationship with the hypothetical common metazoan ancestor, the Urmetazoa. During the past
8 years cDNAs coding for proteins involved in cell-cell- and cell-tissue interaction have been cloned from
sponges, primarily from Suberites domuncula and Geodia cydonium and their functions have been studied
in vivo as well as in vitro. Also, characteristic elements of the extracellular matrix have been identified and
cloned. Those data confirmed that all metazoan phyla originate from one ancestor, the Urmetazoa. The
existence of cell adhesion molecules allowed the emergence of a colonial organism. However, for the next
higher stage in evolution, individuation, two further innovations had to be formed: the immune- and the
apoptotic system. Major defense pathways/molecules to prevent adverse effects against microbes/parasites
have been identified in sponges. Furthermore, key molecules of the apoptotic pathway(s), e.g., the pro-
apoptotic molecule comprising two death domains, the executing enzyme caspases, as well as the anti-apo-
ptotic/cell survival proteins belonging to the Bcl-2 family have been identified and cloned from sponges.

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Based on these results—primarily obtained through a molecular biological approach—it is concluded that
cell-cell- and cell-matrix adhesion systems were required for the transition to a colonial stage of organization,
while the development of an immune system as well as of apoptotic processes were prerequisites for reaching
the integrated stage. As the latter stage already exists in sponges, it is therefore likely that the hypothetical
ancestor, the Urmetazoa, was also an ‘‘integrated colony.’’

INTRODUCTION 1896, p. 18). However, until recently it was generally

The origin of Metazoa is to some extent still enig- accepted that the choanoflagellates were the sister
matic despite the progress that has been achieved in group to Metazoa (see Nielsen, 2001). Even though
the last years by molecular studies. The evolution of sponge choanocytes are similar to choanoflagellates
the Metazoa from unicellular/colonial organisms oc- and are composed of a single flagellum, surrounded by
curred some 1,300–600 Myr ago in the pre-Ediacaran a microvillar collar, the long-standing view of a ho-
period (Conway Morris, 1998). Morphological contri- mology of these types of flagella/cilia (Kent, 1881;
butions to understanding of the transitional stages to Lackey, 1959) could not be substantiated (Karprov and
the Metazoa suggest a colonial origin of Metazoa (see Efremova, 1994). Now, based on the study with pro-
Dewel, 2000). This view implies that, based on the tein molecules, Fungi are regarded as the nearest-
Beklemishev’s cycles of duplication and individuation neighbor kingdom of the Metazoa (Schütze et al.,
(Beklemishev, 1969), after duplication of an individual 1999), a conclusion which is supported by others (Bal-
and the formation of a colony this entity has to un- dauf et al., 2000).
dergo individuation again. It has been pointed out that During the past 10 years unequivocal support for
two such cycles were necessary in early evolution for the monophyly of metazoans has been presented
the emergence of Metazoa: first the transition to mul- (Müller, 1995) from molecular studies, from analysis
ticellular organisms, with the sponge grade of orga- of specific cell adhesion molecules and their receptors
nization, and second the change to the modularized as well as of the extracellular matrix in sponges, and
ancestor of the Bilateria (Dewel, 2000). especially by combination of these data with morpho-
Recent phylogenies based on rDNA have suggested, logical studies (see Dewel, 2000). The assumption that
that the Metazoa are polyphyletic. The proposal sug- all metazoan phyla are of monophyletic origin has
gested that the Porifera/Cnidaria evolved separately been widely accepted (see Borchiellini et al., 2001).
from the Triploblasts; both having originated indepen- For the molecular biological analyses the two demo-
dently through aggregation of protists belonging to sponges Suberites domuncula and Geodia cydonium
two different lineages (Christen et al., 1991). This have been used. The facts compiled also imply that the
view is based on the early idea that sponges (Porifera) ancestor of all metazoans was a sponge-like organism,
are grouped with the Protozoa (Spencer, 1864, p. 302). which I termed Urmetazoa (Müller, 2001). This new
Later, ontogenetic evidence provided the basis for step in understanding of the basal animal phylogeny
sponges to be considered as metazoans (Haeckel, is the platform for answering the next pressing ques-
tion of the origin of individuation in Metazoa, again
regarding Porifera as living fossils, descendants of a
1 From the Symposium New Perspectives on the Origin of Meta-
colonial ancestor. The step of individuation taken by
zoan Complexity presented at the Annual Meeting of the Society for
Integrative and Comparative Biology, 3–6 January 2002, at Ana- sponges was also a prerequisite for the further progress
heim, California. in evolution of the Porifera to the level of Cnidaria
2 E-mail: [email protected] (Dewel, 2000; Fig. 1).

3
4 WERNER E. G. MÜLLER

(AF), which promotes the species-specific aggregation

of sponge cells.
The G. cydonium AF is a complex particle, com-
posed of several polypeptides. Three proteins associ-
ated with the AF from G. cydonium were identified in
detail; a galectin, a 36 kDa putative AF as well as an
86 kDa AF-associated polypeptide. In addition, the
proteoglycan-like core structure of the AF has been
characterized from M. prolifera. The G. cydonium gal-
ectin was cloned; sequence analysis revealed that those
aa residues which are involved in mammals in binding
of galectins to galactose are conserved in the sponge
sequence (Pfeifer et al., 1993). This observation was
taken as evidence in support of the monophyly of
Metazoa (Müller, 1995). The galectin links the AF-
complex to the membrane-associated aggregation re-
ceptor (AR) (Wagner-Hülsmann et al., 1996). The 36
kDa putative AF was recently cloned (Schütze et al.,
2001a). Its deduced aa sequence displays in the N-

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terminal portion high similarity to amphiphysin/BIN1
sequences found in Protostomia and Deuterostomia. In
addition, an 86 kDa AF-associated polypeptide has
been identified, whose predicted protein comprises
nine short consensus repeats (SCR) (Müller, 2003).
The core structure of the AF had been identified in
the AF-complex from M. prolifera as a polymorphic
proteoglycan-like molecule (Fernandez-Busquets et
FIG. 1. Hypothetical steps towards the evolution to the Urmetazoa
with the Porifera as the next closest taxon. Adhesion molecules were al., 1996).
required to allow the transition from a fungal-like ancestor to a co- Using the G. cydonium model sponge the putative
lonial system, a stage which made the further development of im- aggregation receptor (AR) was cloned (Blumbach et
mune- and apoptotic systems possible that led to the evolution of al., 1998). It comprises fourteen scavenger receptor
the Urmetazoa, as an integrated system.
cysteine-rich (SRCR) domains, six SCR repeats, a C-
terminal transmembrane domain and a cytoplasmic
tail. Competition experiments using recombinant AR
In the following review I present a summary of the or antibodies raised against this receptor, suggested
recent achievements in the understanding of principles that the adhesion molecule present in the enriched AF
of individuation in sponges, based on protein sequences binds to the AR. In addition, previous experiments also
functioning in the immune response and apoptosis, two indicated that the strength of binding of the AF to the
processes which play central roles in the maintenance cell surface AR is augmented by galectin (Wagner-
of development and homeostasis of metazoans. Hülsmann, 1996).
METAZOAN ORIGIN: MONOPHYLY Extracellular matrix molecules
The adhesion molecules in sponges provide solid In sponges the space between the external pinacod-
grounds for the view that all metazoan animals origi- erm and the internal choanoderm, the mesohyl, does
nated from one ancestor, the Urmetazoa (reviewed in not comprise a homogenous ground substance. It is
Müller, 2001 and 2003). These molecules were found composed, in addition to galectin, of the following
to represent major metazoan autapomorphies (see main elements: collagen, fibronectin-like molecules,
Müller, 1995 and 1997). and a minor component, dermatopontin, was also re-
cently identified, (Schütze et al., 2001b). These poly-
Adhesion molecules peptides form the extracellular matrix (ECM) which
Already since their first use by Wilson (1907) provides the platform for specific cell adhesion via the
sponges have been a traditional model for studies of integrin receptor, as well as for signal transduction and
cell-cell and cell-matrix adhesion (reviewed in Burger cell growth. As an example, it has been summarized
and Jumblatt, 1977; Müller, 1982). Primarily the two that in demosponges several cells are involved in spic-
marine demosponges, Microciona prolifera and G. cy- ule formation (Uriz et al., 2000). This process requires
donium, have been the most thoroughly studied spe- a series of complex pathways in which also the ex-
cies. In 1973 two groups succeeded in isolating and pression of silica-responsible genes is involved (Kras-
purifying both from M. prolifera (Henkart et al., 1973) ko et al., 2000 and 2002).
and G. cydonium (Müller and Zahn, 1973) the first Collagen is an autapomorphic molecule that is pre-
extracellular particle, termed an aggregation factor sent only in the Metazoa. In contrast to higher meta-
 THE ORIGIN OF METAZOAN COMPLEXITY 5

zoan phyla, which contain approximately 20 different

types of collagen, in sponges only two groups of col-
lagen molecules have been identified, the fibrillar col-
lagen and the type IV-related collagen (reviewed in
Garrone, 1998). Exposito and Garrone (1990) were the
first to sequence a collagen cDNA from a sponge. Re-
cently, it was shown that cells of S. domuncula express
a collagen gene in response to the growth factor my-
otrophin (Schröder et al., 2000). The cDNA for S. do-
muncula collagen was isolated; the deduced aa se-
quence shows that the collagenous internal domain is
rather short with only 24 G-x-y collagen triplets FIG. 2. Molecules from G. cydonium comprising Ig-like domains.
(Schröder et al., 2000). Structure of the receptor tyrosine kinase (GC-RTK), as well as of
A further major component of the ECM is fibronec- the sponge adhesion molecules (SAM), the long form GC-SAML,
tin. Evidence has been presented, suggesting that and the short form GC-SAMS, from G. cydonium. The building
blocks are: Pro-Ser-Thr(P/S/T)-rich domain, Ig-like domains 1 (Ig
sponges also contain fibronectin. In 1981 Labat-Robert 1) and 2 (Ig 2), transmembrane domain (TM), juxtamembrane region
and colleagues described a protein in sponges, which (JM) and TK-domain (TK). The length of the stretches of the re-
cross-reacted with antibodies raised against vertebrate spective deduced aa domains are given. The position of the ITIM-
fibronectin (Labat-Robert et al., 1981). During our motif in the cytoplasmic region of the G. cydonium GC-SAML

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search for fibronectin we were able to demonstrate that (spanning aa533 to aa538 of the polypeptide) is marked.
in G. cydonium, there are protein(s) that cross-react
immunologically with human anti-fibronectin antise-
rum (Müller, 1997). A subsequent screening for the of the evolution from the COLONIAL STAGE to an INTE-
respective cDNA revealed a protein which consists of GRATED STAGE, the step towards individuation (Fig. 1).
three putative modules; a fibronectin module type-III,
a SRCR unit and a SCR repeat; this sponge protein METAZOAN INDIVIDUALITY: IMMUNE MOLECULES
was called a ‘‘multiadhesive protein’’ (Pahler et al., Adhesion of cells is the basic property and prereq-
1998a). uisite for a functional immune system. Therefore, it
One major class of receptors which interact with the can be assumed that during evolution elements or mol-
ECM are the integrin receptors, membrane-anchored ecules developed which became functional not only as
heterodimer receptors composed of a- and ß-subunits. adhesion molecules but also as elements of the im-
After the identification of collagen in the ECM sub- mune response. One well known example is the im-
sequent screening produced the integrin receptors in munoglobulin (Ig-) domains which are building blocks
the marine sponges G. cydonium (Pancer et al., 1997) of polypeptides that participate in cell adhesion, mus-
and S. domuncula (Wimmer et al., 1999). cle contraction, and immune defense (Nezlin, 1998).
One additional sponge membrane receptor that Later in evolution these domains served as immune
should also be mentioned here, is the receptor tyrosine molecules.
kinase (RTK). RTKs are restricted to the Metazoa. The The early metazoans, the hypothetical Urmetazoa,
first RTK from lower metazoa was identified and lived in an aquatic environment and consequently were
cloned from G. cydonium (reviewed in Müller and exposed to a massive load of both pro- and eukaryotic
Schäcke, 1996). As schematically outlined in Figure 2 organisms trying to invade and destruct them. It is
(GC-RTK), the deduced polypeptide sequence com- amazing that sponges have the capacity to process
prises: (i) the extracellular part with a Pro/Ser/Thr-rich their own volume of water every 5 seconds in order
region, and two complete immunoglobulin-like (Ig- to extract edible material (Vogel, 1977); this fact sup-
like) domains, (ii) the transmembrane domain, (iii) the ports the notion that they are exposed to a huge num-
juxtamembrane region and (iv) the catalytic tyrosine ber of bacteria and also viruses present in the seawater
(TK)-domain. A ligand for this RTK, a mucus-like (see Gonzales and Moran, 1997). To cope with these
protein, was also identified (Schütze et al., 2001b). threats sponges have developed an efficient chemical
defense system (Proksch, 1994) as well as humoral
Metazoan-fungal relationship and cellular defense mechanisms (Müller et al.,
Using protein DNA sequences from sponges, espe- 1999a). Studies on the immune system in sponges
cially those from adhesion molecules, the monophy- have been performed with the focus on the mecha-
letic origin of the Metazoa was established (Müller et nisms by which (i) these animals react against mi-
al., 2001a). Using those molecules which function in crobes/parasites and (ii) respond to non-syngeneic tis-
signal transduction, growth control and defense, a sue.
common ancestry with Fungi was established (Schütze In recent studies it has been reported that there are
et al., 1999; Müller et al., 2001a); Figure 1. Already pathways which control fusion and rejection during
before such a relationship could be proposed (Bor- histo-(in)compatibility reaction in the Porifera (Müller
chiellini et al., 1998). The existence of cell-cell- and et al., 1999a, 2001b). Although this had been expected
cell-matrix adhesion molecules was used as evidence from the precise historecognition reactions that were
6 WERNER E. G. MÜLLER

described on tissue level (see: Hildemann et al., 1979 interacting in mammalian systems, the TNF-receptor,
and 1980), it was very surprising to discover that key were only recently cloned. The first potential gene in-
molecules involved in allo/auto-immunity in sponges volved in apoptosis of sponge cells, the MA-3 gene
share high sequence and functional similarity with from S. domuncula was identified (Wagner et al.,
those molecules which had been found to control his- 1998); the corresponding mouse MA-3 cDNA is as-
torecognition in deuterostomes. Among those are the sumed to encode an apoptotic molecule (Shibahara et
molecules comprising polymorphic Ig-like domains al., 1995). Subsequently both pro- and anti-apoptotic
(present in the sponge adhesion molecules [SAMs]), proteins have been cloned from both S. domuncula and
the allograft inflammatory factor (a sponge cytokine) G. cydonium, and their functions have been analyzed
as well as the (2–5)A system (control of infection) (see to some extent.
below), whose existence had not been reported in pro-
tostomes (Gamulin et al., 2000; Müller et al., 2001a). Metazoan pro-apoptotic molecules
This fact, that sponges have molecules/pathways in As the most promising segment to screen for a pro-
common only with deuterostomes (i) strongly supports apoptotic molecule, we selected the death domain part
the monophyly of Metazoa, (ii) underscores that the which is found in the mammalian apoptosis controlling
degree of individuality of sponge species is high and proteins Fas, tumor necrosis factor-a or its receptor,
(iii) suggests that sponges might/will become model and FADD (Cleveland and Ihle, 1995); it is absent in
organisms to understand the origin of vertebrate im- the nematode (Ruvkun and Hobert, 1998). This ap-
munity and diseases connected with it. proach was successful; the molecule isolated from G.

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cydonium even comprises two death domains (Wiens
METAZOAN INDIVIDUALITY: APOPTOTIC MOLECULE et al., 2000a). Sequence comparisons revealed that the
Apoptosis in sponges two domains found in the sponge molecule are to be
grouped within the death domain family. It was
Until recently (Wiens et al., 2000a, b) it was pro- claimed before that the death domain found in humans
posed that the physiological cell death is restricted to comprises relationship to ankyrin motifs (Boldin et al.,
multicellular organisms, which have separate germ and 1995), an assumption which could be substantiated
somatic cells (Vaux et al., 1994). Originally it was also experimentally (Müller et al., 2001a). Functional
suggested to divide the process of physiological cell assays were performed with allografts from G. cydon-
death into (a) ‘‘programmed cell death,’’ describing ium which revealed that in rejecting tissue a strong
the developmentally regulated elimination of specific increase of the expression of the death domain-com-
cells during embryogenesis (Lockshin and Williams, prising gene (GCDD2) occurs (Wiens et al., 2001).
1964), and (b) ‘‘apoptosis’’, describing morphological
changes of dying cells (Kerr et al., 1972). At present, Caspases
these terms are used interchangeably; therefore, we use In vertebrates, the death domain containing recep-
the term apoptosis. In the last three years it has become tors/adapter molecules interact intracellularly with the
apparent that apoptosis is not restricted to metazoans caspase-8 proenzyme through the death-effector do-
that have separate cell lines, but came about during the main with a similar region in the caspase (Grütter,
transition from the common ancestor of all metazoan 2000). An adapter-mediated oligomerization causes an
phyla to the phylogenetically oldest metazoan taxon, activation of the procaspase(s) which undergo cleav-
the Porifera (reviewed in Müller et al., 1998). age and finally heterodimerization (Cory and Adams,
Two lines of evidence led us to assume that sponges 1998). Finally, upstream caspase(s) activate pro-cas-
are also provided with complex apoptotic pathways. In pase-3 which in turn is split into the large and small
1992 Pfeifer and others found that a factor could be subunits that activate after heterodimerization a factor
identified in xenografts from G. cydonium that cross- necessary for the DNase activity to degrade chromatin
reacted immunologically with an antibody raised into the nucleosomal fragments the sign of apoptosis
against a mammalian tumor necrosis factor (TNF). The (Fig. 3B).
Mr was determined to be 30 kDa hinting at a relation- In Bilateria a series of caspases are involved in the
ship to the mammalian TNF. Furthermore, it was tuned control of apoptosis, starting with caspase-8 in
shown that sponge cells have a high level of telome- the cascade and ending with caspase-3. Interestingly
rase activity, when they are present in the state of cell- enough, until now, only one gene has been identified
cell contact [both in intact organism and in prim- in G. cydonium which encodes two transcript forms,
morphs] (Koziol et al., 1998). Consequently we pos- both for caspase-8 and for -3 equivalents (Fig. 3A).
tulated that, in order to maintain a defined ‘‘Bauplan,’’ Two deduced procaspases have been identified, which
sponge cells in tissue organization must undergo ap- were termed CAS3lpGEOCY [long form] and
optosis (Wagner et al., 1998). Recently, we could iden- CAS3spGEOCY (short form) (Wiens, to be published).
tify in sponges homeobox genes, e.g., a LIM/homeo- CAS3lpGEOCY can be considered as the procaspase-
box encoding protein, which are involved in organo- 8 equivalent, due to the presence of the CARD domain
genesis in higher metazoan phyla (Wiens et al., sub- (Hofmann et al., 1997). The—probably alternatively
mitted). However, in spite of intense efforts, the gene spliced product—procaspase-3 equivalent (CAS3sp
encoding the potential TNF as well as the receptor GEOCY) lacks CARD, but like the CAS3lpGEOCY
 THE ORIGIN OF METAZOAN COMPLEXITY 7

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FIG. 3. Apoptotic pathway in sponges. A. Alignment of the two G. cydonium caspase-3-related polypeptides, deduced from the long (GEO-
CYCAS3l) and short form (GEOCYCAS3s) of the corresponding cDNAs. Identical amino acids are in white on black. The borders of the large
subunit and of the small subunit ( large/small subunit ), the CARD segment ( CARD ) as well as the two signatures ( z- sign-1/2 -z ) are marked.
B. Schematic representation of the known, or suspected members of the apoptotic pathways in sponges. In the extrinsic pathway, the apoptotic
signal is initiated by ligand (TNF-like molecule) receptor (TNF-receptor [TNF-rec]) binding which causes the binding of the adapter molecule,
the sponge death domain containing molecule. This leads intracellularly to a recruitment of the procaspase-3l (an equivalent to procaspase-8).
After activation, followed by heterodimerization of the small (S) and the large subunit (L), this caspase activates the executing procaspase-3s
(an equivalent to procaspase-3) which finally causes apoptosis through limited proteolysis and activation of a DNase. In a second pathway
other activation processes initiates the cell-death pathway which is under the control of the Bcl-2 and related proteins. If Bcl-2 interacts with
Bad apoptosis can proceed; however if Bad becomes trapped by 14–3–3 it undergoes functional inactivation.

sequence, comprises the cleavage sites for the forma- Metazoan anti-apoptotic/cell survival proteins
tion of the subunits as well as the two caspase family In addition to the activation of the apoptotic process
active sites (Fig. 3A). Functional studies indicate that through TNF/TNF-receptor further pathways have
the two forms of the sponge caspases act in G. cydon- been described in Bilateria, which include activation
ium in the apoptotic pathway. through growth factor deprivation, heat shock or bac-
8 WERNER E. G. MÜLLER

terial infection (Nicholson and Thornberry, 1997), plex synthesis of spicule formation (Krasko et al.,
pathways which have also been described in sponge 2002).
systems (Wagner et al., 1998). The signal transduction At the next level of integration, the cell-matrix ad-
pathway initiated by those factors can be blocked by hesion system supports the integration of the function-
the function of molecules belonging to the Bcl-2 fam- al units of sponges. The major extracellular molecules
ily (Nicholson and Thornberry, 1997). in sponges are collagen fibrils, which interact with in-
In line with the biological evidence that in both S. tegrin receptors on the cell surface, followed by G-
domuncula and in G. cydonium apoptosis can be ini- protein and kinase-mediated signal transduction pro-
tiated by environmental stress factors, e.g., bacterial cesses (Wimmer et al., 1999).
load (Wagner et al., 1998) or cadmium (Wagner et al., Cell-cell- and cell-matrix adhesion are the basis for
1998) an intense screening for members of the Bcl-2 the COLONIAL STAGE of the metazoans and prerequisites
family was started. This effort resulted in the func- for the establishment of integrated systems. These ad-
tional analysis of the anti-apoptotic/cell survival pro- hesion systems alone are not sufficient for individua-
teins from these two sponge species (Wiens et al., tion. The stage of individuation can only be reached
2000a, b, 2001). The proof that the sponge gene prod- after the acquisition of an immune system which is
uct acts as a cell survival protein was performed by paralleled or complemented by a mechanism that elim-
transfection studies using mammalian cells. It could be inates unwanted, which accumulates during develop-
shown that mammalian cells transfected with the ment in a multicellular organism; this process is
sponge Bcl-2 related gene confer resistance against termed apoptosis. Sponges have an amazingly com-

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heat shock and growth factor deprivation (Wiens et al., plex immune system, which acts against invading mi-
2001). crobes or parasites. Furthermore, the immune system
Besides the molecules of the Bcl-2 family other is the basis for the individualization; mechanisms have
polypeptides are also known to prevent apoptotic path- been formed during evolution, which allow for dis-
ways, among them is 14–3–3 molecule which, under crimination between self/self and self/non-self.
‘‘cytoprotective’’ conditions, interacts with the pro-ap- Apoptosis is the mechanism in Metazoa that guar-
optotic Bad after this protein has undergone phos- antees homeostasis. The characteristic apoptotic mol-
phorylation through Akt. If Bad is bound to 14-3-3 it ecules have been identified in sponges which, together
has lost its binding capacity to the Bcl-2 related mol- with the functional studies performed, demonstrate
ecule Bcl-xL (Zha et al., 1996). Also this pathway, that these earliest of metazoans are provided with key
where 14-3-3 is involved in protection against man- regulatory elements for controlled development, tissue
made pollutants, e.g., PCB, has been demonstrated in homeostasis and defense against pathogens.
G. cydonium (Wiens et al., 1998); Fig. 3B. Taken together, the phylogenetic oldest, extant meta-
Taken together, the bulk of evidence shows that zoan phylum, the Porifera, are provided with complex
sponges have a complex apoptotic machinery, which immune and apoptotic systems that allow the forma-
allows the elimination of unwanted tissue (e.g., in allo- tion of an INTEGRATED SYSTEM (Fig. 1). Considering the
transplantation) and very likely also in the establish- fact that the different sponge species are not ‘‘amor-
ment of an organized body plan. phous, asymmetrical creatures’’ as suggested (Pech-
enik, 2000), but comprise a defined phenotype, a
CONCLUSION: URMETAZOA AS COMPLEX AND sponge might be defined as ‘‘integrated colony’’ or an
INTEGRATED ANIMALS individual, composed of functional units, allowing the
The question from which organism the Urmetazoa formation of a defined body plan.
evolved remains open. Frequently, the choanoflagel-
lates have been considered as the sister group of the ACKNOWLEDGMENTS
Metazoa. However, cytological data contradict this This work was supported by grants from the Deut-
view (Karprov and Efremova, 1994), and molecular sche Forschungsgemeinschaft, the Bundesministerium
sequence data from proteins are not available from für Bildung und Forschung Germany [Center of Ex-
choanoflagellates. In view of existing data it appears cellence ‘‘BIOTECmarin’’] and the International Hu-
more likely that the Urmetazoa share a common an- man Frontier Science Program (RG-333/96-M).
cestry with the Fungi (Schütze et al., 1999).
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