Download Animal phylogeny in the light of the trochaea theory

Biological Journal ofthe Linnean Society ( 1985), 25; 243-299. With 9 figures
Animal phylogeny in the light of the
trochaea theory
CLAUS NIELSEN
Zoologisk Museum, Universitetsparken 15,
DK-2100 Copenhagen 0 , Denmark
Accepted f o r publication I4 November 1984
Ultrastructural similarities unite Choanoflagellata and Metazoa as the Kingdom Animalia.
Metazoa (Porifera
Placozoa
Gastraeozoa) are characterized by the presence of collagen,
septate/tight junctions and spermatozoa. Porifera and Placozoa lack basal lamina, nerve cells and
synapses, which characterize Gastraeozoa (Cnidaria
Trochaeozoa). Cnidaria have cnidoblasts
and lack the multiciliate cells found in almost all Trochaeozoa (Gastroneuralia Protornaeozoa).
Gastroneuralia (Spiralia
Aschelminthes) have an apical brain and a pair of ventral nerves, a
blastopore which becomes mouth and anus, a mouth surrounded by a downstream collecting
system of compound cilia, and a mesoderm formed from the blastopore lips. Spiralia (Articulata
Parenchymia
Bryozoa) have spiral cleavage and 4d-cell mesoderm, whereas these characters are
lacking in Aschelminthes, which all lack primary larvae. Protornaeozoa (Ctenophora
+ Notoneuralia) have mesoderm from vegetal cells. Ctenophores have colloblasts. Notoneuralia
have a dorsal nervous system behind the apical area and form a new mouth surrounded by an
upstream collecting system of single cilia on monociliate cells; the blastopore becomes the anus
surrounded by a ring of compound cilia.
These features fit the trochaea theory, which proposes that Gastroneuralia and Notoneuralia
evolved independently from the trochaea, a blastaea with the blastopore surrounded by a ring of
rompound cilia, which were both locomotory and particle collecting.
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KEY WORDS: Evolution
cilia - nerve systems.
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Choanoflagellata
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Metazoa - life cycles - embryology - larval types
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CONTENTS
Introduction . .
Animal classification
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Phylum Choanoflagellata .
METAZOA.
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Phylum Porifera . . .
Phylum Placozoa . . .
CASTRAEOZOA(EUMETAZ0A)
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Phylum Cnidaria . . .
TROCHAEOZOA
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GASTRONEURALIA ( P R O T O S T O M I A )
SPIRALIA
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Phylum
Phylum
Phylum
Phylum
Phylum
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Annelida sensu lato
Echiura . . .
Gnathostomulida.
Onychophora
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Arthropoda sensu lalo
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0 1985 The Linnean
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Phylum Mollusca
Phylum Sipuncula
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PARE.jVCHYML1 (ACOELOMA TA)
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Phylum Nemertini
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Phylum Platyhelminthes (Turbellaria) .
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Phylum Entoprocta
Phylum Ectoprocta
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BRTO<OA
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ASCHELMINTHES (NEMATHELMINTHES. PSEUDOCOELOMATA)
Phylum Rotifera . . .
Phylum Acanthocephala .
Phylum Chaetognatha
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Phylum Nematomorpha .
Phylum Kinorhyncha
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Phylum Loricifera . .
Phylum Priapulida . .
Phylum Gastrotricha . .
PRO TORNAEO(0A
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Phylum Ctenophora . .
NOTONEURALIA
BRACHIATA
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CTRTOTRETA
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Pterobranchia
Phoronida .
Brachiopoda .
Echinodermata
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Phylum Enteropneusta
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Chordata
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Phylum Urochordata . . .
Phylum Cephalochordata . .
Phylum Vertebrata . . .
Discussion of characters used in the classification of phyla
Pelago-benthic life cycles . . . . . . .
Fate of blastopore/origin of definitive mouth . .
Larval ciliary bands . . . . . . . .
Nervous systems . . . . . . . . .
Cleavage patterns . . . . . . . . .
Mesoderm and coelom
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Ultrastructure and special cell types . . . .
Biochemistry . . . . . . . . . .
Conclusion
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Acknowledgements
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References . . . . . . . . . . . .
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INTRODUCTION
Phylogenetic theories embracing the whole animal kingdom almost inevitably
fall into two parts: reconstruction of hypothetical ancestral forms and
arrangement of phyla on the branches of a phylogenetic tree . The morphology
of the ancestral forms must be deduced from the knowledge of living animals.
since the palaeontological record gives no evidence about the earliest animals .
The trochaea theory proposed by Nielsen & Nrarrevang (1985) presents a
series of hypothetical ancestors of the major metazoan groups constructed
mainly on the basis of the structure of larval ciliary bands and nervous systems
of living animals . In the present paper I arrange the animal phyla according to
this theory - with a number of additions - and discuss the more important
characteristics used .
The discussions are based almost exclusively on the literature, and I have
ANIMAL PHYLOGENY
245
NOTONEURALIA
benthic adulls
GASTRONEURALIA
new moulh surrounded by neolroch
benthic adults larvae wilh
proto- mela- and telolroch
lour new openings from archenteron
Cnidaria
ecloderm and enloderm
mullicellular!ly
Figure I. Main stages in the early development of the animal kingdom. Hypothetical ancestral
forms encircled. From Nielsen & Nerrevang (1985).
tried to go back to the primary publications to avoid the layers of secondary
interpretations which in many cases obscure the clarity of the original reports.
The trochaea theory proposes a series of changes in structure and function of
the blastopore, ciliary bands and nervous systems during animal evolution (Fig.
1 ) . In the following classification the animal phyla have been arranged
according to this theory (Fig. 2), which will then be tested by checking the
predicted combinations of characters of each phylum. A number of
morphological, embryological and biochemical characters have been considered
and are finally discussed separately.
The highly modified, parasitic Orthonectida and Dicyemida have been
omitted from the discussion because their position appears obscure.
It goes without saying that the aim of this paper - to establish a hierarchical
can only be
classification of the animal kingdom reflecting its evolution
achieved by considering monophyletic groups, i.e. groups consisting of an
ancestral species and all its descendants.
~
ANIMAL CLASSIFICATION
The traditional division of organisms into animals and plants has in recent
years been abandoned in favour of the division into prokaryotes (Monera) and
eukaryotes, the latter group being divided into a varying number of kingdoms
(see, for example, Margulis, 1981: 18-19). Common to most of these new
classifications is that the kingdom Animalia is restricted to comprise the
multicellular, heterotrophic organisms (Metazoa). There is not much agreement
C. NIELSEN
246
ARTICULATA
t * Annelida s I
t * Echiura
Gnathostomulida
0 Onychophora
Arthropoda s I
1 Mollusca
Sipuncula
*
PARENCHYMIA
1 Nemertini
Platyhelminthes
BRYOZOA
1 Entoprocta
Ectoprocta
t o Rotifera
o Acanthocephala
o Chaetognatha
o Nematoda
o Nematomorpha
o Kinorhyncha
o Loricifera
0
0
6 Pterobranchia
4 Phoronida
U1
*
\'* Echlnodermata)
Brachiopoda
Enteropneusta
CHORDATA
U Urochordata
Uo Cephalochordata
U 0 Vertebrata
Priapulida
Gastrotricha
J
Larval characters
1
4
downstream collecting systems
with compound cilia
upstream collecting systems
with single cilia on monociliate cells
spiral cleavage
0 no primary larvae
0 lecithotrophic development
with neural tube
Adult characters
u
6
complicated gill slits
upstream collecting systems
with single cilia on monociliate cells
Figure 2. A phylogenetic tree of the animal kingdom. T h e occurrence of a number of important
characters are indicated.
about the classification of the unicellular organisms and especially the
relationships of the heterotrophic groups are unsettled (see, for example, Taylor
1978).
There is, however, one group of unicellular heterotrophs, the choanoflagellates, which show detailed similarities with metazoans, especially sponges.
The choanoflagellates have mitochondria with flat cristae like those of most
metazoan cell types but unlike almost all other unicellular heterotrophs
(including the ciliates) (Taylor, 1978), and like most metazoan monociliate cells
they possess an accessory centriole (Hibberd, 1975). The structure of
choanoflagellates and sponge choanocytes was compared by Hibberd (1975),
who found that the structure of both the collars of pseudopodia and of the
undulating cilia with vanes and root systems are so similar that close
relationships between the two groups are strongly indicated. There are no
indications that choanoflagellates are related to any of the autotrophic groups
(Hibberd, 1975) nor is there any evidence of relation to any other
zoomastigophoran group (Taylor, 1978; Levine et al., 1980).
As the choanoflagellates thus appear to be more closely related to metazoans,
especially sponges, than to any other organism I find it natural to classify them
ANIMAL PHYLOGENY
247
together, and instead of proposing a new name I prefer to expand the
circumference of the kingdom Animalia to include the choanoflagellates.
The following scheme shows the arrangement of the major animal groups. I
have chosen not to give special names to supraphyletic groups which comprise
only one phylum. Phyla are in ordinary script and supraphyletic names are in
capital letters.
ANIMALIA
Choanoflagellata
Porifera, Placozoa
METAZOA
GASI'RAEOZOA
{
{
Cnidaria
{
GASTRONEURALIA
Ctenophora
TROCHAEOZOA
PROTORNAEOZOA
NOTONEURALIA
Phylum CHOANOFLACELLA
TA.-The choanoflagellates are clearly unicellular organisms,
either solitary or forming colonies of cells united in a jelly-like material. The
usually solitary Codosiga botytis sometimes occurs in groups of two to five on a
common stalk and connected by a short cytoplasmic bridge, but these bridges
are interpreted as remnants of the division process (Hibberd, 1975).
Life histories involving both motile colonial stages and sessile and motile
solitary stages have been described (Leadbeater, 1983). Sexual processes have
not been observed, and it is not known whether the observed stages are haploid
or diploid.
The feeding apparatus of a cylinder or narrow funnel of rod-shaped
pseudopodia surrounding an undulating cilium with an extracellular
microfibrillar vane transporting water away from the cell body is a character
shared with the sponges (Hibberd, 1975). Structures of a few other unicellular
organisms are superficially similar with a circle of pseudopodia and a long
cilium, but both their function and their detailed structure show that these
structures are not homologous with the collared units of the choanoflagellates.
Actinomonas (? Heliozoa) has a circle of rod-shaped pseudopodia which are more
openly spaced than those of the choanoflagellates and an undulatory cilium
with two rows of hairs transporting the water towards the cell body (Fenchel,
1982). Pedinella and its relatives (Chrysophyceae) have a circle of short
pseudopodia and an undulating cilium with a paraxial rod and two rows of
hairs transporting the water towards the cell body (Moestrup, 1982). Naegleria
(? Amoebina), which sometimes has one or more cilia surrounded by
pseudopodia, and which was used by Kummel (1962) as a model for the starting
point for the evolution of choanocytes, also transports water towards the cell
(Willmer, 1956).
METAZOA
Multicellular animals are characterized by a division of labour between cells,
which has necessitated a more intimate intercellular contact than that observed
in choanoflagellates. It is possible that multicellularity has arisen independently
in lines leading to sponges and gastraeozoans (eumetozoans). There are,
however, a number of biochemical, ultrastructural and morphological
248
C. NIELSEN
characters which are shared by sponges and gastraeozoans, suggesting a
monophyletic origin of metazoans. Septateltight junctions seal off the internal
extracellular space, which is of fundamental importance in metazoan
architecture (Staehelin, 1974). The cells communicate inter alia by means of the
acetylcholine/cholinesterase system. Freeze-fracture studies of the basal parts of
the cilia (flagella) of protists and metazoans (Bardele, 1983) have demonstrated
diverse patterns of intermembranous particles in the unicellular organisms,
whereas all metazoans from sponges to vertebrates show a ‘ciliary necklace’ of
3(-5) strands of particles. Also, collagen appears to be a metazoan invention
(Adams, 1978).
A further indication of the monophyletic nature of the metazoans is provided
by the similarity of their spermatozoa; most are monociliate (flagellate) and
possess condensed chromatin and mitochondria (or specializations from this
type; see, for example, Bacetti & Afzelius, 1976). The cilia of flagellates and of
algal microgametes show a n immense variation (see, for example, Moestrup,
1982).
Phylum PORIPERA:
A number of different cell types can be recognized in the
adult sponge, and the cells are united by various types of cell junctions; septate
junctions have been reported both from calcareans and demosponges (Green &
Bergquist, 1979) and from hexactinellids (Mackie & Singla, 1983), but gap
junctions (see Unwin & Zampighi, 1980) have not been observed (Mackie &
Singla, 1983). An extracellular matrix contains collagenous fibres, but a basal
lamina is lacking (Garrone, 1978).
The extracellular vane of the cilia (flagella) which is well known in the
choanoflagellates and in the freshwater sponges (Feige, 1966) has now been
observed in a number of marine sponges (N. Boury-Esnault, Paris, pers.
comm.). In the hexactinellids the collared units are enucleate and partially
separated from a large syncytial system, but the general features of the collar
and cilium are the same as in the other sponges (a ciliary vane has not been
reported) (Mackie & Singla, 1983). The cilia of the choanocytes undulate in the
same way as those of choanoflagellates, but the cilia of the larvae beat like those
of many metazoan larvae, having a spiral metachronal pattern (Bergquist el al.,
1979). Some sponge larvae are superficially almost indistinguishable from some
of the larvae of turbellarians and cyclostomatous bryozoans.
The hexactinellids apparently lack contractile elements, but other sponges
have myocytes surrounding the contractile oscula. The myocytes contain
aligned filaments resembling myofilaments, and cholinesterase appears to be
restricted to these cells; acetylcholine has been detected in some sponge cells, but
synaptic connections have not been observed (Thiney, 1972; Bergquist, 1978).
Typical nerve cells have not been observed, and Bergquist (1978) described the
network of myocytes as an integrative system which can conduct stimuli.
Mackie el ad. (1983) strongly suggest that coordination of the ciliary activity in
hexactinellids is mediated by electrical impulses, but action potentials have, so
far, not been recorded in any sponge (Bergquist, 1978).
The large invagination from which the ciliated chambers arise in calcareous
sponges is not an archenteron (Lemche & Tendal, 1977). There is nothing to
indicate that the sponges have passed through a gastraea stage. I therefore
regard them as derived from the blastaea independently of the gastraeozoans.
ANIMAL PHYLOGENY
249
Phylum PLACOZOA:
Trichoplax is a creeping, flat, irregular, circular to lobate
organism with no anteroposterior orientation. It consists of a ‘dorsal’ epithelium
of flattened, monociliate cells and a ‘ventral’ epithelium of tall gland cells and
monociliate cells. The rather narrow lumen between these two epithelial layers
contains scattered stellate cells (Grell, 1980). The cilia show the usual root
system with an accessory centriole, and there are junction complexes between
the cells, but a basal lamina has not been reported (Ivanov et al., 1982). Eggs
and early cleavage stages have been observed in a few cases (Grell, 1972) but
sexual reproduction and embryology are largely unknown. Spermatozoa,
‘ciliary necklace’ and acetylcholine/cholinesterase have not been investigated.
The lack of basal lamina indicates that Trichoplax is on the same evolutionary
level as the sponges, and it can be interpreted as a flattened, benthic blastaea
with the ‘ventral’ side specialized for feeding and locomotion.
GASTRAEOZOA (EUMETAZOA)
An embolic gastrula stage corresponding to the evolutionary gastraea is
observed in representatives of most of the eumetazoan phyla, collectively called
Gastraeozoa here, but all sorts of specializations have evolved in connection
with large amounts of yolk and/or placental nourishing of the embryos.
In the gastraea, ectoderm and entoderm came into close apposition, and since
a basal lamina almost without exception is found at the basal side of both
ectoderm and entoderm cells in all gastraeozoans, it probably evolved at this
stage. Ectoderm and entoderm are thus not in direct contact, and cell junctions
are probably never formed between cells of these two layers - except of course a t
the opening of the archenteron.
The presence of special nerve cells with synapses (and action potentials?) and
of gap junctions (arrays of membrane particles (connexons) forming cylinders
with an inner diameter of about 1.5 nm; see Unwin & Zampighi, 1980) are
probably gastraeozoan characteristics indicating a higher level of coordination
between the cells (Mackie & Singla, 1983).
The choanocytelike cells found in many gastraeozoans (see, for example,
Rieger, 1976) have shorter pseudopodia than choanoflagellates and sponge
choanocytes and lack the ciliary vane, probably because they are not engaged in
particle collecting. They may, nevertheless, be interpreted as belonging to the
same cell type (cyrtocytes; see Kiimmel, 1962).
Phylum C.\ID.~RIA:
The cnidarians have two cell layers, ectoderm (epidermis)
and entoderm (gastrodermis), separated by a membrane without or with cells.
They have only one gut opening, which functions both as mouth and anus.
Gastrula stages with a normal archenteron formed through emboly are found in
the life cycles of several anthozoans and medusozoans (Tardent, 1978). The
solid, lecithotrophic planula larva which has been regarded as characteristic of
the cnidarians as a whole has apparently evolved several times, either in
connection with deposition of large amounts of yolk in the egg or in connection
with brood protection. Gastrula and planula larvae have well developed apical
organs (Chia & Bickell, 1978).
Adult cnidarians have a net of epithelial nerve cells with a number of circular
concentrations (Spencer & Schwab, 1982). Synapses comprise both the
C. NIELSEN
250
polarized type known from all higher metazoans ( trochaeozoans) and symmetric
synapses believed to be primitive Uha & Mackie, 1967).
The ectodermal cells also comprise myoepithelial cells, which may be in
contact with the exterior and have a single cilium or they may have sunk into
the interior to form large muscles (D. M. Chapman, 1974). Ciliated cells, both
of larvae and adults, are monociliate (Chia & Crawford, 1977), even when the
cilia are united into compound cilia, as in the ciliary membrane of some
zoanthid larvae (Nielsen, 1984). The cnidoblasts are a spectacular speciality of
the phylum (Picken & Skaer, 1966).
Ectoderm and entoderm are separated by a basal lamina, which is thin and
acellular in some hydrozoan polyps, whereas it is thick, jelly-like and with
scattered cells in the medusae (G. Chapman, 1966; Hausman, 1973). The cells
of the mesogloea originate through diffuse immigration from the ectoderm and
perhaps also from the entoderm. The basal lamina/mesogloea may function
both as an attachment for the muscle cells and as a sort of gelatinous skeleton
(mesoskeleton; see G. Chapman, 1974).
The cnidarians are thus at the gastraea stage, and in contrast to the
trochaeozoans they lack multiciliate cells and true mesodermal muscle cells.
TROCHAEOZOA
Trochaea, the hypothetical ancestor of the trochaeozoans, had the general
structure of gastraea but had a ring of multiciliate cells with compound cilia
(the archaeotroch) functioning as a downstream collecting system around the
blastopore (Fig. 3). Ciliary bands of this structure are found in almost all
neotroch
gill pore
00
pore
apical organ
blastopore
Blastaea + Gastraea
+ Trochaea +Protornaea
gastral pores
-
Tornaea
mouth
hydropore
anus
Figure 3. Evolution of a series of hypothetical holoplanktonic ancestors. From Nielsen & Nerrevang
(1985).
25 I
ANIMAL PHYLOGENY
marine phyla having pelagic larvae. All phyla ‘above’ the Cnidaria are
therefore united in the group Trochaeozoa. The specialization of the cells
around the blastopore was accompanied by the evolution of an associated nerve
concentration with connections to the anterior, sensory apical organ, which
could thus provide information for the locomotory activity of the animal. Such
nerves along the bands of compound cilia, for example a prototroch nerve, are
known from a number of invertebrate larvae.
GASTRONEURALIA (PRO T O S T O M I A )
Gastroneuron, the hypothetical ancestor of the gastroneuralians, is envisaged
as a rather small organism with a pelago-benthic life cycle. The larva was a
trochopore type and the adult stage had a simple, tube-shaped gut, ventral,
locomotory cilia, and a nervous system consisting of an apical/frontal brain
connected via circumoesophageal nerves to a double, ventral, longitudinal nerve
(Fig. 4). It had a primary body cavity, but ectomesodermal elements, for
example in the form of muscles, were probably already present at this stage.
Mesoderm originating from various parts of the blastopore lips is found in
spiralians and aschelminths, and it is possible that this type of mesoderm was
also invented a t this evolutionary stage.
The cells of the three bands of compound cilia of the trochophore (specialized
parts of the archaeotroch of the trochaea) were multiciliate and it appears that
the multiciliate condition of other epithelial cells became established at an early
stage of gastroneuralian evolution (see Rieger, 1976). The few examples of
monociliate cells used in feeding or locomotion in positions where multiciliate
cells are found in related types must be regarded as specializations (discussed in
connection with the respective phyla).
The trochaea theory predicts that the blastopore will generally become
divided to form mouth and anus. This pattern is seen in a typical form in only a
few groups scattered throughout the phyla, but an enormous variation is
encountered both within and between the phyla. The ‘typical’ gastroneuralian
ventral views
lateral views
ventral views
lateral views
Figure 4. Evolution of gastroneuron, the hypothetical ancestor of the gastroneuralians (right), from
a specialized, pelago-benthic trochaea (left). From Nielsen & Nerrevang ( 1985).
252
C. NIELSEN
nervous system with an apical/frontal brain and a paired ventral nerve is found
in most of the phyla, but - as could be expected - the nervous system is strongly
modified both in sessile forms (e.g. bryozoans) and in forms with specialized
locomotory habits (e.g. nematodes).
As the structure of the nervous system appears to be a better, and especially
more constant, character of the group than the fate of the blastopore, I have
chosen to use the name Gastroneuralia instead of the somewhat more familiar
Protostomia.
The radiation of the Gastroneuralia has been enormous, but there are a
number of common tendencies. With increasing size the one-layered ectoderm
became weak as a body wall and mesodermal elements became associated as a
strengthening element, in many cases in the form of a peritoneum. Also, with
increasing size the ciliary movements became insufficient for locomotion, food
capture and transport through the gut, and new mechanisms evolved utilizing
muscles. The primary body cavity had the function of a fluid skeleton in the
larvae (as in entoproct larvae today) and various types of body cavities lined by
mesoderm could have evolved as adaptations to different locomotory habits.
SPIRALIA
The spiral cleavage pattern, characterized by the alternating dexiotrophic and
laeotrophic directions of the early cell divisions, the strong cell determination,
and the origin of the mesoderm from the 4d-cell, has long been used to
characterize a major invertebrate group. In some cases the name Spiralia has
been made synonymous with Gastroneuralia (Protostomia) (Salvini-Plawen,
1982), and the cleavage patterns of some of the phyla which are here included
in the Aschelminthes have been interpreted as modified spiralian, with duets or
monets instead of quartets (Costello & Henley, 1976). Typical spiral cleavage,
however, has been described only from the following phyla: Annelida, Echiura,
Sipuncula, Gnathostomulida (?), Nemertini, Platyhelminthes and Entoprocta.
However, in some species of these phyla the spiral pattern has been obscured by
large amounts of yolk or by placental nutrition, and it is, therefore, not
unexpected that it is partially or completely obscured in the Arthropoda and
0n ychophora.
Trochophores and similar larval types with prototroch and metatroch of
compound cilia functioning as downstream collecting systems, adoral ciliary
zone and gastrotroch of single cilia on multiciliate cells, and telotroch of
compound cilia, are known from many species of Mollusca, Annelida, Echiura,
Sipuncula, Nemertini, Platyhelminthes and Entoprocta. The planktotrophic
larvae are in most cases rather simple variations over the general trochophore
pattern, whereas the lecithotrophic larvae show a wealth of specializations.
The evolution of the spiral cleavage pattern and the retention of the
trochophore-type larva unite these phyla in one group.
The benthic adult of the ancestral spiralian moved on the bottom by means of
the gastrotroch cilia. Three evolutionary lines originated from this ancestor,
each having its characteristic mode of locomotion or life style:
( 1 ) burrowing or swimming forms moving by means of muscular action
(Articulata),
ANIMAL PHYLOGENY
253
(2) surface-dwelling forms gliding on the ventral ciliated ectoderm
(Parenchymia), and
(3) sessile forms with U-shaped gut and a single ventral ganglion (Bryozoa).
ARTICULATA
A number of spiralian phyla are often united under the name Articulata
because they show metamerism. The core group is the annelids in which the two
mesoderm cells (teloblasts) formed by the division of the 4d-cell give off a linear
sequence of paired mesodermal cell masses. These cell masses hollow out to form
segmental coelomic compartments (schizocoely), with muscles, nephridia and
other metameric structures arising from their walls. I t is generally accepted that
this arrangement of muscles around coelomic spaces evolved in connection with
a burrowing (or swimming) habit (Clark, 1964).
The adult of the ancestral articulate can thus be envisaged as a burrowing or
swimming organism which moved by means of the mesodermal muscles of the
body wall. Its mesoderm was organized as the lining of one or more coelomic
sacs.
There are, however, some phyla such as the sipunculans, which show obvious
affinities with the annelids but which show no signs of segmentation, and it may
well be that the earliest articulates had only one pair of coelomic cavities, which
appears sufficient for the burrowing process. Articulata may thus be a n
inappropriate name for the group if some of its phyla have never been
segmented, but it is used here because it is the most widely used collective name
for these phyla.
Phylum ANNELIDA
sensu lato: Among the annelids, many polychaetes have the
typical spiralian life cycle with spiral cleavage, the development of paired
coelomic sacs from the teloblasts, a planktotrophic trochophore, and a crawling,
benthic adult (Anderson, 1973). All types of blastopore closures seem to be
realized in the polychaetes: (1) the blastopore becomes mouth and anus
(Polygordius; Woltereck, 1904), (2) the blastopore becomes mouth (Eupomutus;
Hatschek, 1885), and (3) the blastopore becomes anus (Eunice; Akesson, 1967;
this type is very rare). Proto-, meta- and telotroch of compound cilia on
multiciliate cells have been observed in most polychaete larvae. I n Oweniu all
cells are monociliate (Gardiner, 1978), but since the larva of Oweniu exhibits the
normal gastroneuralian system of ciliary bands with prototroch, adoral ciliary
zone and metatroch forming a downstream collecting system, the monociliate
condition is regarded as a specialization within the polychaetes. Lecithotrophic
larvae usually lack the adoral ciliary zone and metatroch, and the telotroch is
absent in a number of types. In some species of Polygordius the larvae have the
area behind the metatroch (i.e. the post-oral area) enlarged posteriorly, forming
a ‘serosa’ that covers the developing segments, and there is a complete gut with
columnar epithelium; at metamorphosis the thin serosa bursts, and the larval
tissues are cast off or ingested (Woltereck, 1902). The mitraria larva of Oweniu is
superficially similar, but here the posterior segments of the metatrochophore are
retracted into the anterior segments (Wilson, 1932). Salvini-Plawen (1980)
regarded these larvae as representatives of the pericalymma type, together with
those larvae of sipunculans and molluscs which have a pre-oral fold covering the
254
C. NIELSEN
hyposphere of the larva; it is clearly incorrect to compare ‘serosa’-like structures
of pre-oral and post-oral origin.
Some polychaete trochophores have a nervous system corresponding
completely to that of the hypothetic gastroneuron larva, with ring nerves along
both prototroch and telotroch (Korn, 1960a; Heimler, 1980). The adult
annelids have the typical gastroneuralian nervous system with an apical brain,
circumoral nerves, and a pair of ventral longitudinal nerves.
The oligochaetes and the hirudineans have direct development, but are
obviously related to the polychaetes. The pogonophorans (including the
vestimentiferans; Jones, 1981) show spiral traits in the cleavage, and the
coelomic compartments of the tiny, tightly segmented opisthosome arise through
schizocoely in telomesoblastic cell clusters (Bakke, 1980). The dorsal-ventral
orientation of pogonophores was earlier much debated, but it is now generally
accepted that the large nerve trunk is ventral and that the group is closely
related to the annelids Clark, 1980; Southward, 1980).
Phylum ECHIURA:
The cleavage and early larval stages of some echiurians are
almost schematic spiralian, and the larva of Echiurus has all the ciliary bands of
the trochophore (Hatschek, 1880). The larval nervous system comprises apical
organ, a pair of commissures, a pair of ventral nerves, and prototroch,
metatroch and telotroch nerves (Balzer, 1917; Korn, 1960b). In later larval
stages segmentation occurs in the ventral nervous system (Korn, 1960b), but
segmentation is only weakly indicated in the benthic adults. Setae resembling
those of the annelids are found in some species both at the base of the trunk and
in two rings around the posterior end. The characteristics make it reasonable to
consider the echiurans as closely related to the annelids (see also Clark, 1969).
Phylum GNATHOSTOMULIDA:
The interstitial fauna comprises many microscopical,
superficially similar, ciliated species of turbellarians, gastrotrichs and annelids,
groups known also from other habitats. The rather recently discovered phylum
Gnathostomulida, however, appears to be restricted to the interstitial habitat,
and its affinities to other phyla are difficult to ascertain.
The development of Gnathostomula jenneri was studied by Riedl (1969), who
found spiral cleavage, but as in most other interstitial forms further development
is direct. The adults look like small turbellarians or archiannelids, and their
complicated jaw apparatus on a ventral pharyngeal bulb with mesodermal
muscles resembles that of eunicid polychaetes (Kristensen & Nmrevang, 1978).
In some species the copulatory organ has a stylet which superficially resembles
that found in turbellarians, but there is no similarity on the ultrastructural level
(Mainitz, 1977). A dorsal, non-permanent anal pore similar to that of some
turbellarians was observed by Knauss (1979). All epithelial cells are monociliate
with the exception of some sensory cells (Rieger, 1976; Kristensen & Nm-revang,
1977).
I am inclined to regard the gnathostomulids as a highly specialized,
interstitial annelid type and consequently to regard the monociliate condition as
a specialization similar to that observed in the polychaete Owenia. The coelomic
reduction described in a number of interstitial polychaetes (Fransen, 1980) and
the complete absence both of coelomic cavities and of segmentation in the family
Lobatocerebridae (see Rieger, 1980) indicate how the usual annelid architecture
with muscular movements involving the coelomic compartments as a
ANIMAL PHYLOGENY
255
hydrostatic skeleton can be changed in small organisms which glide on their
cilia instead. I t could, of course, be argued that evolution had proceeded in the
opposite direction, i.e. from non-coelomate forms gliding on cilia to coelomate
forms moving by means of muscles, and long evolutionary series involving
reductions must always be treated with some suspicion (cf. Remanonasus;
Stumpke, 1962). However, the interstitial habitat and the direct development
indicate the specialized nature of the group.
Phylum O.Z’YCHOPHORA:
The onychophorans have yolky eggs or placentally
nourished embryos and their cleavage pattern gives no clue to their
phylogenetic relationships. The early embryo of Peripatopsis capensis shows a
longitudinally elongated blastopore which becomes mouth and anus, as in
typical gastroneuralians (Balfour, 1883). The morphology and development of
the head in arthropods and onychophorans show so many similarities that
Weygoldt (1979) regards the onychophorans as the sister group of the
euarthropods. O n the other hand, the detailed similarities in the development
(fate maps) of certain onychophorans and clitellates is interpreted by Anderson
(1973) as an indication that the onychophorans are descended from the
clitellates, and further that they are the most primitive group within the
Uniramia (myriapods insects).
That the onychophorans belong to the articulate line is unquestionable, but
their relationships with annelids and arthropods is not yet clear.
+
Phylum ARTHROPODA
sensu lato: The arthropods (Chelicerata, Trilobita,
Crustacea and Uniramia) are usually treated as one phylum, but some recent
authors regard the four taxa as belonging to two or more separate evolutionary
lines (Manton & Anderson, 1979). However, the present discussion is less
concerned with the relationships between the arthropod groups than with their
evidently very close relationships with the other articulate groups.
The arthropods completely lack ciliated larvae and their embryology is in
most cases strongly influenced by large amounts of yolk. Some of the crustaceans
have an almost biradial cleavage (Bocquet-VCdrine, 1961), while others,
especially some cirripeds (Anderson, 1969), have a spiral cleavage. The
embryological fate maps show important differences between arthropods and
polychaetes (Anderson, 1973), and the interpretation of the type of cleavage is a
matter of discussion (Costello & Henley, 1976; Weygoldt, 1979). Mesoderm
formation shows some variation, but the origin of coelomic sacs from a
teloblastic zone can usually be recognized (Anderson, 1973).
The nervous system of the arthropods is of the typical gastroneuralian type
with an apical/frontal brain and a double ventral nerve.
The brain of the tardigrades is so similar to that of other uniramians (R. M.
Kristensen, Copenhagen, pers. comm.) that the tardigrades are here assigned to
that group, and the pentastomids are included in the crustaceans (see
Wingstrand, 1972; Riley el al., 1978).
Phylum Mo~r.ci.sc~:
Life cycles comprising planktotrophic larvae (mostly veligers)
and benthic creeping adults are common in most classes of molluscs. Spiral
cleavage and mesoderm formation from the 4d-cell have been described in a
great number of species. The blastopore may become (1) mouth (e.g. Limax;
Meisenheimer, 1896), (2) anus (e.g. Viviparus; Dau tert, 1929), or (3) obliterated
256
C. NIELSEN
(e.g. Haliotis; Crofts, 1937). The veliger larva has the typical gastroneuralian
system of prototroch, adoral ciliary zone and metatroch along the rim of the
velum. A telotroch is lacking in most larvae but is found in the test larva of
Neomenia (Thompson, 1960). I n the test larvae of protobranchs and
solenogasters the epithelium of the prototroch area is drawn out into a thin sheet
which covers the hyposphere more-or-less completely; the metamorphosis of
these larvae includes a shedding or infolding of the test (Drew, 1899; Thompson,
1960).
The nervous system consists of a brain, which originates from the
apical/frontal area, a ring around the oesophagus and two pairs of longitudinal
nerve cords. In the presumably primitive caudofoveates the lateral and ventral
cords fuse laterally in the posterior part of the body and are connected by a loop
over the anus as in the schematic gastroneuralian (Salvini-Plawen, 1972). The
coelom is restricted to a pair of gono-pericardial cavities.
The metameric nature of the molluscs has been much debated. Some authors
deny the existence of segmentation in the mesoderm (e.g. Salvini-Plawen, 1968),
but the investigations and discussions of Gotting (1980) and Wingstrand
(1985) lend new support to the view that the molluscan ancestor was segmented.
The molluscan type of serial repetition of organs has not been related to
confluence of rows of coelomic sacs, and it may have originated through
subdivision of one pair of coelomic sacs.
Phylum SIPWCULA:The sipunculans have a typical spiral cleavage but the
following development shows much variation, from a rather complicated
sequence with a lecithotrophic trochophore followed by a planktotrophic
pelagosphera to direct development (see Rice, 1981). In the various
trochophores, a prototroch, an adoral ciliary zone and a ‘metatroch’ can be
recognized, but usually not all three in the same species. In GolJingiu vulgare the
prototroch and the adoral ciliary zone cannot be distinguished (see Gerould,
1906), and in Sipunculus nudus a fold of ciliated epithelium (called the serosa),
probably representing episphere plus prototroch cells, overgrows the whole
hyposphere (Hatschek, 1883). This serosa becomes folded in after a short period
and all pelagosphera larvae swim by means of a powerful ciliary ring behind the
mouth. This ring, which at least in some species consists of compound cilia, is
usually described as a metatroch. However, its beating is in the direction
opposite to that of a normal metatroch, for the larva swims with the apical
organ in front and the metatroch does not collect particles (Jagersten, 1963;
Rice, 1981). Further investigations are needed to show whether this ciliary ring
can be interpreted as a metatroch (Gerould, 1906: 142) with reversed beat or as
an extra ciliary ring like the prominent ciliary girdles of the young Chaetopterus
larva (Cazaux, 1965). The larva has a large coelomic cavity, and in the adult
there is, in addition, a small coelomic canal surrounding the oesophagus and
sending one canal to each tentacle and one or a pair of compensation sacs
posteriorly; the origin of the small coelom is unknown (Gruner, 1982).
Metamorphosis is rather gradual. The apical organ sinks in and becomes the
brain, and a pair of circumoesophageal nerves come to connect the brain and an
unpaired ventral nerve cord (Hatschek, 1883).
There are so many similarities between sipunculans, echiurans, annelids and
molluscs, that these phyla must be closely related (Clark, 1969; Gruner,
ANIMAL PHYLOGENY
257
1982). Metamerism is only faintly suggested in echiurans and has not been
observed at all in sipunculans. This may represent a reduction from a segmented
state, for anterior septa are reduced in polychaetes with an eversible pharynx,
and the same functional constraints must be connected with a retractable
introvert. O n the other hand, the absence of metamerism in sipunculans may be
primitive, indicating that the early articulates were non-segmented.
PARENCHYMIA (ACOELOMATA)
The nemerteans and the flatworms have traditionally been regarded as closely
related because of the similarities both in development and in adult structure
(Gibson, 1972; Odening, 1984).
The most characteristic common feature is their acoelomate structure, in
which a compact mesenchyme fills the whole space between the body wall and
the gut. The connective tissue of turbellarians and nemerteans has been
investigated by Pedersen ( 1983) who found much variation in the turbellarians:
a rather simple structure in the acoels and several specialized structures in the
polyclads, which in this respect resemble the nemerteans. The free-living forms
have an ectoderm with multiciliate cells, which are locomotory in the smaller
forms, whereas muscular movements are involved in the locomotion of the
larger forms. The gut is a simple elongate sac in small species but bears
numerous diverticula in larger forms. Serial repetition of reproductive structures
in nemerteans and in some turbellarians must be regarded as pseudometamerism, and embryologically there are no traces of formation of coelomic
pouches as in the articulates.
Cleavage is spiral with 4d-mesoderm in some turbellarians and nemerteans.
The planktotrophic larvae (Muller’s larva of the polyclads and the pilidium of
the nemerteans) can be regarded as modified trochophore larvae but lack an anus.
All parenchymians apparently lack the ability to synthesize chitin Ueunieaux,
1982).
Phylum NEMERTI.M:
Most nemerteans have direct development but some of the
heteronemerteans have a planktotrophic larva. Cleavage is spiral and mesoderm is
formed from the 4d-cell (at least in some species). The blastopore becomes the
mouth of the larva, but an anus is not formed in the larva. The characteristic
pilidium larva has a ring of large compound cilia along the lower margins of the
bell-shaped body (pers. obs.), an apical organ, in some species with multiciliate
collar cells (Cantell et af., 1982), and a general ciliation of the exterior surface of
the body. In certain larvae (Pilidium recurvaturn and P. incurvatum; Dawydoff,
1940) a ring of apparently compound cilia is found around a ‘posterior’
elongated part of the body. This larval type can be interpreted as a modified
trochophore with a non-differentiated prototroch-metatroch and with a
telotroch around the ‘anal’ region. In the more usual pilidium larvae the whole
posterior part of the body with telotroch has disappeared (Jagersten, 1972).
Metamorphosis involves the formation of a series of ectodermal invaginations
(usually seven) which fuse and whose internal walls form the ectoderm of the
small adult (an anterior invagination forms the proboscis); the external walls of
the sacs are shed together with the ‘larval’ ectoderm at metamorphosis.
The adults have rhabdites, an epithelium of multiciliate cells, and a nervous
system with a brain and a nerve ring encircling the anterior end of the proboscis
12
258
C. NIELSEN
sheath and a pair of longitudinal ganglionated cords (Gibson, 1972). The
proboscis coelom, which functions as a hydrostatic organ everting the proboscis,
is a nemertean speciality. The blood vascular system is a t least partially lined by
a continuous endothelium, and Ruppert & Carle (1983) propose that i t may be
interpreted as a system of highly modified coelomic canals.
The nemertean larval types (although very specialized in many species) may
give a clue to the understanding of the turbellarian larvae as further modified
trochophores. The compact mesenchyme and the rhabdites further indicate
turbellarian relationships.
Phylum PLATYHELMI.NTHES
( TURBELLARIA)
: Trematodes and cestodes are regarded
as specialized (turbellarians and Ehlers ( 1985) united them in the group
Neodermata which he considered to be the sister group of the Dalyellioida.
The archoophoran type appears to represent the primitive stage both with
regard to development (entolecithal eggs, spiral cleavage) and adult
morphology. Most polyclads have a typical spiral cleavage, although the
‘macromeres’ 4A-D are very small; the 4d-cell is the mesoderm cell as in the
molluscs (Henley, 1974). The Miiller’s and Gotte’s larvae of polyclads are
probably planktotrophic and have a band of longer cilia on multiciliate cells;
this band of cilia perhaps represents the prototroch which is drawn out on a
series of lappets or tentacles (Ruppert, 1978). These tentacles have the same
structure as the tentacles of the entoprocts, although it is not known if the
ciliation consists of single cilia or compound cilia. Some of the Gotte’s larvae
described by Dawydoff (1940) resemble pilidium larvae in general body form.
None of the larvae have an anus. The nervous system of Miiller’s larva shows
detailed similarities to that of polychaete trochophores (Lacalli, 1983).
Metamorphosis is a rather gradual process, in which the larva elongates and
loses the tentacles. In acoels (and some polyclads) cleavage follows a spiral
pattern with duets instead of quartets (Henley, 1974). The two remaining
archoophoran groups, Catenulida and Macrostomida, are mainly limnic, and it
appears possible that only the polyclads have retained the gastroneuralian
planktotrophic larva.
The morphology of the adults shows many characteristics which appear
‘primitive’, for example the absence of anus, gonadal walls and female
gonoducts in some acoels, but these features may just as well be seen as
secondary simplifications. The nervous system comprises an anterior brain and
one to four pairs of longitudinal nerve cords, but the variation is considerable,
and in some of the acoels the whole nervous system is a subepidermal plexus
with a concentration around the statocyst (Beauchamp, 1961). The detailed
similarities between the spiral cleavage of some of the polyclads and that of some
of the molluscs and annelids clearly links the flatworms to the spiralian line.
BRTO(0A
Following my earlier work (Nielsen, 1971, with detailed references; 1977), I
unite entoprocts and ectoprocts in the group Bryozoa because I regard the
ectoprocts as derived from entoproct-like ancestors. Both groups have a pelagobenthic life cycle with sessile adults. As in several other sessile groups the adults
have a U-shaped gut, a strongly concentrated central nervous system, and a
budding process which involves ectoderm and mesoderm only; this budding
ANIMAL PHYLOGENY
259
usually leads to the formation of colonies. The ganglion is formed as an
invagination from the ectoderm in both entoprocts and ectoprocts. The fully
formed ganglion is solid in entoprocts, gymnolaemates and stenolaemates, but
retains a cavity from the invagination in the phylactolaemates. The
‘neuralation-like, formation of the ganglion has led Salvini-Plawen ( 1980: 418)
to characterize the phylactomaematous ectoprocts as typical ‘oligomerans’, but
he has apparently overlooked the similarities in the formation of the ganglion of
the other ectoproct groups and the entoprocts.
The adults are filter-feeders which strain particles from the water by ciliary
mechanisms that are quite different in entoprocts and ectoprocts. This
difference and differences in the morphology of the mesoderm are discussed
below. Photoreceptors occur both in some entoproct larvae and in certain
gymnolaemate larvae (Woollacott & Zimmer, 1972; Woollacott & Eakin, 1973;
Hughes & Woollacott, 1980); they consist of a cell with a tuft of tightly packed
cilia (which lack the ATPase arms in the entoprocts), a type of photoreceptor
reported nowhere else in the animal kingdom (Coomans, 1981a ) .
Phylum ENTOPROCTA:
The entoprocts have a typical spiral cleavage with
mesoderm formation from the 4d-cell, b u t the spiral pattern is obscured in
species with placental nourishment of the embryos (as in Loxosomella vivipara).
The larvae are typical trochophores with a prototroch of compound cilia in
front of the mouth, an adoral ciliary zone of single cilia continuing in a
gastrotroch in some species, and a metatroch of compound cilia (pers. obs.); a
telotroch is not present, and in many species the area of the gastrotroch is
specialized as a ciliated foot, just as in several mollusc larvae.
The larvae of some species of Loxosomella settle on their frontal organ, retract
their hyposphere and reorganize the material of the larval organs, except for the
gut. The gut rotates about go”, a new ganglion forms from an invagination of
the new ventral epithelium, a row of tentacles with a ciliary apparatus
(probably homologous with that of the larva) develops, and the atrium of the
small adult reopens. Larvae of other species of Loxosomella and Loxosoma have
external or ‘internal’ budding, and the larvae disintegrate after the release of the
buds. The larvae of Pedicellina and Barentsia settle on the ring of cells above the
retracted prototroch and hyposphere, and after a rotation of the gut of about
180” and the same reorganization as that observed in Loxosomella, the atrium
opens again.
In the adults the tentacles have a usual downstream collecting system with
lateral compound cilia and an extended adoral ciliary zone (Nielsen &
Rostgaard, 1976). The space between the body wall and the gut is partially
filled with irregular mesodermal cells, muscles and, in pedicellinids and
barentsiids, the peculiar star-cell complex, which is supposed to create some
circulation in the fluid between these elements (Emschermann, 1969).
Phylum ECTOPROCTA:
All ectoprocts are colonial. Most species have lecithotrophic
larvae without a gut, and in species with planktotrophic larvae the larval gut
disintegrates at metamorphosis. The polypides all originate through a budding
process.
The gymnolaemates are regarded as the most primitive group. The
stenolaemates show a very specialized larval development with polyembryony
and precocious development of the cuticle covering the primary disc; they also
260
C . NIELSEN
possess a most unusual adult body plan with the mesoderm detached from the
ectoderm of the body wall and forming the ‘membranous sac’ (Nielsen &
Pedersen, 1979). The phylactolaemates, by some authors regarded as primitive
because the lip is interpreted as a prosome, are freshwater forms with placentally
nourished embryos with precocious budding; the free-swimming stage can thus
be compared to a small colony. The horseshoe shape of the lophophore in most
species can be interpreted as an adaptation to a large polypide size (see Mundy
et al., 1981).
The gymnolaemates have bilateral cleavage, and the planktotrophic
cyphonautes larva, which apparently is found in both cheilostomes and
ctenostomes, can be regarded as the most primitive ectoproct larva. Several
steps of the embryology are unfortunately poorly known, for example mesoderm
formation. The larva swims by means of cilia from a ring of multiciliate cells
(corona). These cilia are not grouped into compound cilia, but their effective
stroke is directed away from the apical organ, and I interpret the corona as a
modified prototroch which is not involved in feeding. Small particles are
strained from the water by the U-shaped ciliated ridge behind the mouth. This
ciliary system has the same structure and function as that of the adult tentacles,
i.e. two rows of cells, each with a row of single cilia forming an upstream
collecting system (Strathmann, 1973). The upstream collecting system with
multiciliate cells is clearly different from the system with monociliate cells found
in larvae of echinoderms, phoronids and brachiopods, and the two types are
considered non-homologous.
There is considerable variation in the settling of gymnolaemate larvae, but
some larvae, for example those of Bulbellu and Victorella (Braem, 1951) and
Bowerbankia (Reed, 1978), settle on the ring of cells above the retracted
prototroch and hyposphere after the glands of the adhesive sac have given off
the secretion that attaches the metamorphosing larva to the substratum. This is
very similar to the process found in larvae of the colonial entoprocts, and I
believe that the ancestor of the ectoprocts had the same type of metamorphosis.
The body cavity of ectoprocts functions as a fluid skeleton in the movements
of the polypides. The mesoderm covers most of the body wall and the gut, but
its origin is obscure both embryologically and in the budding process (especially
in the stenolaemates). I interpret the fluid skeleton of the ectoprocts as an
elaboration of that found in the entoproct larvae, such as Barentsia, with the
body wall strengthened by mesoderm arranged in a layer. There is no trace of
trimery in the embryology of the ectoprocts (Hondt, 1982), and the partial
division of the body cavity into tentacle coelom and body coelom, which have
been compared to the mesosome and metasome of notoneuralians, is more
similar to the division observed in the sipunculans.
The funicular system is a series of narrow mesodermal tubes which connect
the gut with the cystid walls (Lutaud, 1982) (and in ctenostomes the guts of
neighbouring zooids through the interzooidal pores); in phylactolaemates the
narrow lumen is surrounded by a basal lamina, and the system thus has the
general morphology of a blood vascular system (Carle 8z Ruppert, 1983). Blood
vascular systems have obviously evolved several times, and there is not much to
indicate that this system is homologous with the blood vascular system of
phoronids and brachiopods, where the vessels mediate transport between
tentacles, gut and gonads.
ANIMAL PHYLOGENY
26 1
Consequently, the ectoprocts are regarded as derived from a colonial
entoproct-like ancestor which had a fluid skeleton, a metamorphosis like that of
Pedicellina, and larval budding as in several of the loxosomatids.
ASCHELMINTHES (NEMATHELMINTHES, PSEUDOCOELOMATA)
The close relationship between nematodes, nematomorphs, gastrotrichs,
kinorhynchs, rotifers and acanthocephalans has been stressed by a number of
authors (e.g. Andrassy, 1976; Coomans, 1981b; Hartwich, 1984), and also the
priapulids are often referred to this group. The new phylum Loricifera is clearly
related to priapulids and kinorhynchs. The chaetognaths are treated here
because an intracellular, ‘internal’ cuticle has been found in Eukrohnia (Arne
N~rrevang,Copenhagen, pers. comm.) .
Coomans has (1981b) clearly indicated the main problem involved in
investigating the phylogeny of these groups: important characteristics unite the
phyla in groups of two or three, but it is very difficult to find a single positive
characteristic which can be used to define the whole group. Both embryology and
adult morphology show definite gastroneuralian patterns, but at present the
aschelminthes can only be distinguished from the spiralians by the lack of both
spiral cleavage and of pelago-benthic life cycle. This is clearly unsatisfactory.
The cleavage patterns of rotifers, acanthocephalans and gastrotrichs have even
been interpreted as modified spiralian (Costello & Henley, 1976), but none of
the aschelminth groups have been claimed to have a spiral pattern with quartets
(or duets) and mesoderm formation from the 4d-cell. The interpretation of
rotifer and gastrotrich cleavage as spiralian with only one quartet (‘monet’; see
Costello & Henley, 1976) is not in accordance with the cell lineage of the
gastrotrich Turbanella as described by Teuchert (1968; see Table 3).
Further development varies but the fusion of the lateral blastopore lips
characteristic of the gastroneuralians is seen in nematodes (Muller, 1903) and
gastrotrichs (Teuchert, 1968). The mesoderm originates from the posterior and
lateral blastopore lips in some nematodes (Boveri, 1899) and from a ring of cells
surrounding the blastopore in some gastrotrichs (Teuchert, 1968).
None of the phyla have a pelago-benthic life cycle and only the rotifers have a
ciliary feeding structure of the trochophore type.
The most characteristic feature of the group is probably the morphology of
the mesoderm, which in the shape of muscle cells lines the body wall (and in
some cases also the gut) more-or-less completely. There is no trace of coelomic
sacs, and the body cavity can best be described as a primary body cavity
(blastocoel) more-or-less completely lined with mesodermal muscles. A blood
vascular system is lacking as a consequence of the lack of coelomic epithelia. The
nervous system consists, in most groups, of a ring around the oesophagus and a
number of longitudinal cords (orthogonal nervous systems; see Reisinger, 1972).
As will become apparent from the following discussions of the individual
phyla, rotifers and acanthocephalans (and perhaps also chaetognaths) form one
group, and kinorhynchs, loriciferans, priapulids, nematodes and nematomorphs
another group (to which the gastrotrichs are more loosely attached).
Phylum ROTIFERA:
The rotifers have no larval stage, but many species are filter
feeders with a downstream collecting system consisting of prototroch (trochus),
adoral ciliary zone and metatroch (cingulum), exactly as in the trochophore
262
C. NIELSEN
(Beauchamp, 1907; Strathman et ul., 1972). Both prototroch and metatroch
consist of compound cilia (pers. obs.). This system is well developed in solitary
planktonic species and in colonial or sessile species. In creeping species the
ciliary system is usually much modified
Beauchamp (1965) interpreted the cleavage pattern as a modified spiral
cleavage without the usual 90” shifts in the directions of the spindles and with
only two quartets of micromeres, whereas Costello & Henley (1976) described i t
as a spiral cleavage with ‘monets’ instead of quartets. The cell lineage (Table 1 )
has only general traits in common with spiral cleavage (with quartets), and the
origin of the mesoderm is completely unknown. I t must be concluded that the
cleavage is not of the spiralian type, and it appears that new studies on the
cleavage pattern of this and the other aschelminth phyla will prove more fruitful
than mere reinterpretations of old descriptions.
Table 1. Cell lineage of Asplunchnu; based on Jennings ( 1896), Nachtwey ( 1925)
and Beauchamp (1956)
b ,-ectcderm
b, , -ectoderm
b,,-entoderm
c , -ectoderm
c, ,--ectoderm
c, ,-entoderm
L CD
d ,-ectoderm
d ,-ectoderm
d ,-abortive
d,-abortive
G-germinal
cell
ANIMAL PHYLOGENY
263
The non-ciliated body wall consists of a syncytial epithelium with an electrondense intracellular layer (intracellular cuticle) perforated by narrow canals lined
by the outer cell membrane (Storch & Welsch, 1969). The mesoderm is
represented by distinct muscles and does not form a continuous layer. The
pharynx consists of an epithelial cell layer, which forms the trophi, and a layer
of mesodermal muscles (Koehler & Hayes, 1969). The nervous system comprises
a bilobed ganglion dorsal to the pharynx, formed as an invagination from the
epithelium and with nerves to the gut and various sense organs, and a pair of
lateroventral ganglionated cords (Hyman, 1951).
On the basis of the structure of the ciliary system the rotifers must be
regarded as typical gastroneuralians which originally had a pelago-benthic life
cycle; the planktonic types may be interpreted as neotonic, while the creeping,
benthic types without trochus and cingulum have acquired a direct
development (this conclusion was also drawn by Jagersten, 1972).
Phylum ACAXTHOCEPHALA:
The relationships of parasitic groups are often difficult
to make out and this is especially the case with organisms which, as the
acanthocephalans, have no primary larval stage. The cleavage pattern of the
acanthocephalan egg is also difficult to interpret because of the elongate
ellipsoidal shape of the egg (Meyer, 1928, 1931, 1938).
O n the ultrastructural level, important similarities have been established
between acanthocephalans and rotifers, indicating close phylogenetic
relationships between the groups: ( 1 ) the ectoderm is, at least in some regions,
syncytial with an intracellular electron-dense layer pierced by narrow infoldings
of the cell membrane; this intracellular cuticle seems to be unique (Storch &
Welsch, 1970) (but see also Chaetognatha); (2) the surfaces of the muscle cells
show specializations unknown elsewhere in the animal kingdom (Whitfield,
1971); (3) the spermatozoa are similar and resemble those of nematodes and
nematomorphs (Whitfield, 1971).
Phylum CHAETOCNATHA:
There is at present no generally held opinion on the
relationships of the arrowworms, and attempts have been made to relate them
to almost all phyla from nematodes to vertebrates (Ghirardelli, 1968).
The egg contains a small roundish body which can be followed during the
first cleavages, and the cell with this ‘germ cell determinant’ gives rise to the
germ cells (Elpatiewsky, 1909). Development (Burfield, 1927) comprises a
coeloblastula stage followed by a gastrula stage, in which a pair of primordial
germ cells can be recognized in the archenteron, opposite to the blastopore; the
blastopore marks the posterior pole of the embryo, but soon closes. A pair of
lateral folds of the entomesoderm forms anteriorly and expands posteriorly,
carrying the germ cells with it, to divide the archenteron into a median gut
and U-shaped posterolateral cavity (coelomj, from which a pair of anterior sacs
soon become separated. A stomodaeum is formed at the anterior end, and the
mouth breaks through as a ventral slit. The backwards growth of the two folds
proceeds differently in the posterior part of the embryo, where the median
cell layers of the folds, which form the gut, stop growing. The lateral cell layers,
however, come into contact and finally divide the U-shaped body cavity into a
pair of lateral sacs. Each of these sacs later becomes divided by a transverse
septum just behind the newly formed anus. A ventral ganglion is formed as a
pair of epidermal thickenings along most of the length of the ventral midline.
C. NIELSEN
264
The nervous system comprises a dorsal cerebral ganglion, connected through
a pair of circumenteric connectives to an elongate subenteric ganglion, which
gives off 12 pairs of small lateral nerves and a posterior pair of large nerves
(Burfield, 1927).
An intracellular cuticle like that of rotifers has been observed in Eukrohnia
(Arne Norrevang, Copenhagen, pers. comm.) .
The formation of the coelomic cavities is definitely reminiscent of that of the
notoneuralians, especially some of the brachiopods, but the development and
morphology of the nervous system are decidedly gastroneuralian. Mesoderm
and coelom formation show considerable variation (see the discussion of
mesoderm and coelom in the following section), so I have chosen to put
emphasis on the nervous system and to regard the chaetognaths as
gastroneuralians. The early appearance of special germ cells is characteristic of a
number of aschelminths.
Phylum NEMATODA:
The nematodes are a highly specialized group. Cilia have
been abandoned and the locomotory system is based exclusively on longitudinal
muscles working against a hydrostatic skeleton; the rather stiff but elastic body
wall with a tough, three-layered collagen cuticle permits only small changes in
the shape of the animal (Coomans, 1981b). This design has made
intussusceptive growth of the cuticle difficult and all nematodes go through four
moults.
Cleavage is of a characteristic type with a T-shaped four-cell stage; the
pattern is highly determined and the complicated cell lineage of Parascaris
equorum (as Ascaris megalocephala) was worked out at the beginning of this century
(see Table 2). There is an inconsistency in the paper of Muller (1903, text p. 6
Table 2. Cell lineage of Parascaris equorum; based on Boveri (1899), Muller
(1903) and Strassen (1906); the notation is that of Boveri
(
S:( = AB)-ectoderrn
YI-right
f
f
I
r
c*
11
~
LcII-right posterior mesoderm
fyI-left posterior ectoderm
y 11-left
pz
[EM%*
{
mst
MSt
posterior ectoderm
c
{
m-right
posterior mesoderm
anterior mesoderm
st-stomodaeum
{ p r l /.-left anterior mesoderm
~ u-stomodaeum
r
E-entoderm
*Cells which undergo chromosome diminution.
ANIMAL PHYLOGENY
265
and diagram p. 24): the text is in accordance with the descriptions and
illustrations of the papers of Boveri and Strassen (see Table 2), while the
diagram shows that the MSt-cell divides to form M and St instead of mst and
paz. The erroneous diagram has been elaborated and reproduced in several
modern textbooks, where there is accordingly not agreement between the
diagrams and the illustrations. The mesoderm is formed from five cells and
forms a horseshoe at the posterior half of the blastopore before it disappears into
the primary body cavity. The ‘gastroneuralian’ lateral constriction of the
blastopore, which leaves mouth and anus as the remaining parts of the
blastopore, is seen in several species (e.g. Parascaris: see Muller, 1903). There is
no larval stage. In the adult the number of cells is fixed in many organs.
The nervous system has a ring with ganglia around the pharynx and
longitudinal nerves in the four epidermal cords. The large longitudinal muscle
cells cover the epithelium of the body wall except at the cords; the muscle cells
are connected directly with the dorsal or ventral nerve cord via a narrow
extension of the sarcoplasm. The gut has a triradiate pharynx of myoepithelial
cells (Reger, 1966) and an intestine without mesodermal lining.
Many species have hair- to hook-shaped spines on various regions of the body,
and the primitive, free-living Kinonchulus has a number of hooks and spines on
the pharynx, which may be everted, and the whole structure resembles the
proboscis of kinorhynchs, loriciferans, nematomorphs and priapulids (Riemann,
1972).
The nematodes have the aschelminth mesoderm and show many similarities
with the other phyla of this group.
Phylum NEMATOMORPHA:
The hair worms and the nematodes share many
characteristics, such as locomotory type, longitudinal muscles, epithelial cords
with only one or two nerves, and cuticle (Coomans, 1981b).
Cleavage is rather irregular and after the proliferation of some mesoderm cells
an invagination forms an archenteron; the blastopore becomes the anus (cloaca)
(Inoue, 1958). The parasitic larva has a protrusible proboscis with stylets and
hooks very similar to that of the primitive free-living nematode Kinonchulus
(Riemann, 1972). The adults do not feed; their gut is much reduced and the
pseudocoel is partially obliterated in most species.
Although the nematomorphs must be regarded as a separate phylum, they
are clearly related to the nematodes.
Phylum K I N o R H r N c H A : The cuticle of kinorhynchs is arthropod-like (Moritz & R.
Storch, 1972) and is divided into thick rings (zonites) connected with
membranes. The muscles are arranged in accordance with the ‘segmentation’.
There is an introvert with hooks and sometimes with more elaborate spines or
bristles (Cuteria; Higgins, 1968). The pharynx has an epithelial lining over the
mesodermal muscle cells (Merriman & Corwin, 1973).
The embryology of the kinorhynchs is unknown. Kozloff (1972) found the
eggs of Echinoderes and observed the hatching of the juvenile, which consisted of
11 zonites. Further development includes a series of moults and the adults have
13 zonites (Higgins, 1974).
The kinorhynchs thus share a number of characteristics with other phyla. The
cuticle and some of the sense organs (Moritz & R. Storch, 1972) resemble those
of arthropods. The arrangement of the muscles reflects the ‘segmentation’ of the
266
C. NIELSEN
cuticle, but they are not engaged in the movements of limbs and there is no
trace of coelomic compartments, so the similarities with the articulates are
superficial, The pharynx is quite different from the musculoepithelial pharynx of
nematodes and gastrotrichs, but similar to that of rotifers and polychaetes; there
are, however, so many detailed similarities both in general appearance and in
function of the proboscis of kinorhynchs, priapulids and loriciferens that their
close relationships can hardly be questioned.
Phylum LORICIFERA:
This newly described phylum (Kristensen, 1983) comprises
some minute interstitial animals which superficially resemble loricate rotifers.
The embryology of the only described genus, Nanaloricus, is unknown, but there
is a characteristic free-living juvenile (‘Higgins-larva’) with a pair of posterior
flippers and an ectoparasitic adult stage which is reached through two
moultings. Both stages have an eversible proboscis (introvert) with an intricate
array of spines, resembling those of priapulids, kinorhynchs, nematomorph
larvae, and certain nematodes. The proboscis can be retracted into the
abdomen, which is covered by six longitudinal cuticular plates (four in the
larva) which give the whole animal a considerable likeness to a priapulid larva.
The close relationship of Nanaloricus to priapulids and kinorhynchs can hardly
be doubted, and further investigations may well lead to the establishment of
nematodes, nematomorphs, priapulids, loriciferans and kinorhynchs as a welldefined taxon within the aschelminths.
Phylum PRIAPULIDA:
The development of the priapulids is only partially known.
In Priabulus caudatus, the cleavage is radial and there is a coeloblastula and an
embolic gastrula; mesoderm is formed as two bands from the blastopore lip
(Lang, 1953). The following stages are unknown, but a characteristic ‘loricate’
larva with a number of cuticular plates covering most of the body is known from
a number of species. The growth is accompanied by a series of moults. Both
larvae and adults have an introvert with hooks similar to the introvert of
kinorhynchs. The structure of the cuticle resembles that of the nematodes
(Moritz & V. Storch, 1970). The existence of a coelomic epithelium has been
claimed by some authors, but recent investigations by Malakhov (1980)
unequivocally show that there is no epithelium covering the muscles of body
wall and gut.
The priapulids are clearly an aschelminth group.
Phylum G A S r R O r R I C H A : The gastrotrichs share many characteristics with the
nematodes, but they move on a ventral, ciliated area, and their musculature is
therefore quite different.
The small eggs cleave totally; the cleavage pattern is not spiral (Table 3 ) , but
comparisons with other aschelminths have not been very successful (Teuchert,
1968). At the 30-cell stage, a ring of 10 cells which will give rise to mesoderm
and ectoderm surround the blastopore, which soon becomes divided into mouth
and anus through the usual gastroneuralian fusion of the lateral blastopore lips.
The mesoderm becomes arranged in two compact, lateral masses, which
differentiate into muscles, gonads, etc. There is no larval stage, and the growth
is continuous without moults. There is a bilobed ganglion at the dorsal and
lateral sides of the anterior part of the pharynx and a pair of ganglionated
lateroventral cords.
ANIMAL PHYLOGENY
267
Table 3. Cell lineage of Turbanella cornuta; based on Teuchert (1968)
f A
i
r
1
a”-right
anterior ectoderm
aa2-right anterior mesectoderm
a’
\
aI2-right lateral mesectoderm
left anterior mesectcderm
b”-left
lateral ectoderm
b’l-left lateral mesectoderm
dd’-right posterior ectoderm
ddz-right posterior mesectoderm
f d
d”-left
posterior ectoderm
dm2--leftposterior mesectoderm
E-entoderm
‘and I indicate anterior and lateral, respectively, and
and ’ indicate right and left, respectively.
The adults have an epithelium consisting of monociliate cells in some species
and multiciliate cells in other species. Each cilium is surrounded by a thin
cuticle except in the cirri, where the cuticle surrounds the whole structure. The
cuticular covering of the locomotory cilia appears to be a unique feature of the
gastrotrichs and the distribution of the mono/multiciliate condition of the
epithelial cells within the families as they are now understood does not permit
conclusions about which condition is the more primitive within the group
(Rieger, 1976).
The mesodermal muscles cover the body wall and the gut almost completely
and the two narrow lateral cavities can therefore be described as coelomic
(Teuchert, 1977).
The pharynx consists of myoepithelial cells as in nematodes and
nematomorphs, and the Y-shaped lumen has the same orientation in
Chaetonotoidea and Nematoda, but the orientation is opposite in the
Macrodasyoidea (Ruppert, 1982).
There are thus many important similarities between gastrotrichs and
nematodes (see also Coomans, 1981b), and I share the opinion of
Teuchert ( 1968) that Gastrotricha and Nematoda-Nematomorpha are closely
related.
PRO TORNAEOZOA
Protornaea, the hypothetical ancestor of ctenophores and notoneuralians
(Fig. 3), is envisaged as a holopelagic, tetraradial organism with four gastral
C. NIELSEN
268
canals and a ring of compound cilia, the archaeotroch, around the blastopore.
Mesoderm without coelomic cavities developed from the vegetal cells before or
just after gastrulation.
From this ancestor, the ctenophores evolved as biradial and still mostly
holopelagic organisms which retained the apical organ throughout life, whereas
the notoneuralians evolved as bilateral, primarily pelago-benthic organisms
which lost the apical organ at settling.
Phylum CTENOPHORA:
The comb jellies were for a long period united with the
cnidarians in the group Coelenterata, but this view is not favoured by most
modern authors. The oogenesis is highly specialized with a complicated system
of nurse cells which empty their cytoplasm into the oocyte (Pianka, 1974). The
cleavage is biradial and highly determined already at the two-cell stage. The
eight-cell stage is unusual in that it consists of two parallel, curved rows of cells;
the four median cells have been called M-cells and the four distal cells E-cells.
The cell lineage has been studied by a number of authors (see Table 4). T h e
3MI2-, 3MZ2-,4EI2-, and 4EZ2-cellsare micromeres given off from the oral side
of the macromeres during an embolic gastrulation; they have been interpreted
by some authors (e.g. Siewing, 1977) as ‘extra’ ectodermal cells given off by the
macromeres, but both the location and the fate of these cells indicate that they
must be interpreted as mesoderm. They may be homologous with the
micromeres of the sea-urchin embryo. When the gastrulation is completed the
mesodermal cells are situated at the apical side of the archenteron where they
Table 4. Cell lineage of ctenophores; based on Reverberi & Ortolani (1963),
Farfaglio (1963), Ortolani (1964) and Freeman & Reynolds ( 1973)
Number of blastomeres
4
8
16
32
64
I28
256
2e-cells of the comb rows
Seepidermis
2E
{
stomodaeurn
3E
rithe:;;
4E
1
4Ei I-entoderm
oft;
{4Ez
{
4E 2-mesoderm
4E2 -entoderm
(muscles)
4EZ2-mesoderm (muscles)
2m-cells of the balancer cilia of the statocyst
2M
stomodaeum
r-epith:;
3M i-entoderm
of;
3M’ 2-mesoderm (mesenchyme)
3M
{3M2
{
3M2I-entoderm
3M22-mesoderm (mesenchyme)
ANIMAL PHYLOGENY
269
proliferate and form a cross-shaped mass situated between the ectoderm and
entoderm (Metschnikoff, 1885). The two long arms of the cross are in the plane
of the tentacles, parallel to the long axis of the eight-cell stage, and the
observations of Ortolani (1964) suggest that the mesoderm from the E-cells
mainly becomes the muscles of the tentacles, while the mesoderm from the Mcells forms the mesenchyme.
The muscle cells of the cnidarians are epithelial whereas the ctenophores lack
musculo-epithelial cells (Brien, 1969) and the muscle cells of the so-called
mesogloea originate from the vegetal miromeres. The structure of the so-called
mesogloea of the ctenophores, with muscle and nerve cells in an intercellular
substance, is more reminiscent of that of the mesenchyme of a turbellarian than
of the mesogloea of the cnidarians (Hernandez-Nicaise, 1973). This is further
supported by the fact that the mesenchyme of regenerating ctenophores is
formed exclusively from mesenchyme cells (Franc, 1970). The colloblasts of the
ctenophores (Franc, 1978) are very different from the cnidoblasts of the
cnidarians, and the cnidoblasts reported from a number of ctenophores have
been shown to have originated from ingested medusae (Mills & Miller, 1984).
The combs superficially resemble the compound cilia that arise from single
cells in the other trochaeozoans, but each comb consists of cilia from a number
of multiciliate cells (Horridge & Mackay, 1964), and the cilia show
‘compartmenting lamellae’ and a dense midfilament not seen in other cilia
(Tamm & Tamm, 1981). A further difference is that the comb rows show
antiplectic metachrony (waves travelling parallel to the effective stroke of the
cilia) as opposed to the diaplectric metachrony characteristic of the ciliary
bands of other trochaeozoans. The ‘macrocilia’ found along the mouth of
Beroe each contain over a thousand axonemes (Horridge, 1965) and appear to
be unique in the animal kingdom.
Four small canals originate at the apical end of the archenteron; two of these
end as blind pockets, but the other two open near the apical sense organ and
have been observed to dilate and let undigested particles pass out (Main, 1928).
The multiciliate cells and the origin and structure of the mesenchyme render
the derivation of ctenophores from cnidarians very unlikely. Compound cilia
formed by multiciliate cells is a characteristic of the trochaeozoans, but the
combs are so different from the compound cilia of an archaeotroch-both in
structure and movement-that a homology is very uncertain. The origin of the
mesoderm from micromeres at the vegetal pole of the embryo indicates relations
with the notoneuralian line, and the presence of the four small canals from the
apical end of the archenteron (and the lack of a neotroch) is reminiscent of the
structure of the protornaea. The ctenophores are therefore regarded as an early
offshoot from the line leading from trochaea to the Notoneuralia.
NOTONEURALIA
The hypothetical ancestor of notoneuralians, notoneuron, is envisaged as a n
organism with a pelagic larval stage of the tornaria type and a creeping benthic
adult. The larva fed with the upstream collecting system of single cilia on
monociliate cells around the mouth and swam with the ring of compound cilia
(archaeotroch) around the anus (blastopore). The adult had a shape much like
that of the advanced larva of Cephalodiscus described by John (1932); it had an
intraepithelial nerve centre behind the apical area, an almost straight gut, a pair
270
C. NIELSEN
of small gill pores of unknown function but not specialized for particle
collecting, and ciliary feeding structures around the mouth. The side of the
adult facing the substratum is called the ventral side; it is an area between the
new mouth and the blastopore, and it is, therefore, not homologous with the
ventral side of the gastroneuralians, which is the area of the fused blastopore lips
(Fig. 5 ) .
Notoneuron probably had a coelomic sac which was derived from the dorsal
canal from the archenteron (the ventral and lateral canals leading to the mouth
and gill pores, respectively) and which became organized into the system of
proto-, meso- and metacoel found in living enteropneusts, pterobranchs,
echinoderms, phoronids and brachiopods. The presence at an early
embryological stage of a (dorsal) connection from the archenteron to the
exterior opposite the future mouth has been observed both in enteropneusts and
echinoderms (see below). The development of coelomic sacs from other areas of
the archenteron, as observed in some enteropneusts, brachiopods and
phoronids, is interpreted as a later deviation.
The larval apical organ is lost at metamorphosis in all notoneuralians. The
adult nerve centre develops in the mediodorsal region of the mesosome and
extends further posteriorly in the chordates.
Two evolutionary lines can be followed from notoneuron: in one line the
adults became sessile and elaborated the upstream collecting ciliary system of
the neotroch on a ring or horseshoe of tentacles. This line, called the Brachiata,
comprises pterobranchs, phoronids, brachiopods and echinoderms. In the
Gastroneuralia
a
t
Cnidaria
Notoneuralia
a
a
t
t
a
b
+b
*a
t
b
Figure 5. Comparison of axes and orientations of cnidarians, gastroneuralians and notoneuralians.
a-b denotes the apical-blastoporal axis; the area of the blastopore is indicated by a heavy line. I t is
seen that the ventral side of the gastroneuralians coincides with the blastopore area, whereas i t is
represented by an area between the blastopore and the new mouth in the notoneuralians. From
Nielsen & Nsrrevang (1985).
ANIMAL PHYLOGENY
271
second line the adults were primarily creeping and specialized the gill openings
for feeding and respiration instead of the ciliary system. This line, called the
Cyrtotreta, comprises enteropneusts and chordates.
BRACHIA TA
In the line leading primarily to sessility, the planktotrophic primary larvae
have been retained in representatives of most groups. In many types the
neotroch, which originally served only in feeding, became meandering and took
over locomotion, while the archaeotroch disappeared. In the sessile adults the
gut became U-shaped (as in many other sessile animals) and the two small gill
pores disappeared (except in Cephalodiscus and Ahbaria). The adults are
primarily filter-feeders with the larval neotroch expanded on a ring or horseshoe
of tentacles around the mouth (the name Brachiata-the armed-refers to these
tentacles. The pterobranchs, phoronids and brachiopods are sessile or
hemisessile and have somewhat diffuse nerve centres, whereas the highly
derived, pentamerous echinoderms have a number of nerve cords around the
mouth and along the arms.
The interpretation of the ‘lophenteropneust’ drawn by Lemche el al. (1976)
on the basis of photographs of hadal fauna comes close to a primitive brachiate
with a straight gut and a pair of arms with ciliated tentacles-even a small oval
gill pore is indicated in one of the drawings (Lemche et al., 1976: pl. 26C).
Phylum PTERORRA.,VCHIA:
The embryology of the pterobranchs is unfortunately
rather imperfectly known; Hyman (1959) suspected that Schepotieff (1909) had
ectoproct larvae mixed up in his material, and she outrightly rejected the
account of Gilchrist (1917). It appears, however, that there is a free-swimming
ciliated larva (at least in some species) with an apical organ, and that protocoel,
mesocoel and metacoel are formed from the archenteron. Advanced larvae are
elongate with a straight gut Uohn, 1932).
The adults have a long, narrow, U-shaped gut with the anus situated rather
close to the mouth; the dorsal side of the animal with the collar ganglion is quite
short. The ventral side is drawn out into a stalk from which budding occurs in
some species. One or more pairs of tentacles with an upstream collecting system
are found around the mouth. The ciliated cells of the tentacles are generally
monociliate with a distinct accessory centriole and the cilium surrounded by a
ring of microvilli, but some cells are said to have two or more cilia (Dilly, D72).
Gill pores are lacking in Rhabdopleura, but Cephalodiscus and Atubaria have a pair
of small gill openings, through which water transported to the oesophagus with
the food particles may seep out (Willey, 1894).
The nervous system shows a dorsal, epithelial concentration in the mesosomal
region (collar ganglion) with nerve cords to the tentacles, along the dorsal
midline, and around the oesophagus to the ventral midline all the way to the
stalk (Horst, 1939).
Cephalodiscus thus resembles notoneuron in having both an upstream collecting
ciliary system around the mouth and a pair of gill pores, but it clearly belongs to
the brachiate line, because it feeds by means of ciliated tentacles and
(consequently) lacks the specializations at the gill pores found in the cyrtotrete
line, and its nerve centre is not tube-shaped.
272
C . NIELSEN
Phylum PHOROMDA:
Most phoronids have planktotrophic actinotroch larvae in
which there is an upstream collecting system with monociliate cells on the
tentacles behind the mouth and a large archaeotroch around the anus. The
adults are benthic. Cleavage has been described as spiral by some authors, but it
now appears to be generally accepted that cleavage is biradial (Zimmer, 1964,
1980). The anterior part of the blastopore directly becomes the mouth while the
posterior part becomes obliterated by the fusion of the lateral lips. The anus
forms later, in an area well behind the region of the blastopore. Some authors
have claimed that the anus originates from the posterior part of the blastopore,
but this has not been substantiated. The mesoderm arises through ingression of
cells from the archenteron. The unpaired protocoel (hood coelom) is formed by
cells from a U-shaped area near the anterior part of the blastopore and soon
disappears. The mesocoel (collar coelom) is formed at a later stage, possibly
from the same group of cells. The metacoel (trunk coelom) is formed by cells
probably originating from the region at the junction of stomach and intestine.
The apical nervous concentration is lost at metamorphosis (Herrmann, 1979),
and the adult nervous system is mainly intraepithelial with a concentration in
the dorsal area between mouth and anus (Siltn, 1954a).
Although the blastopore does not become the anus of the adult, the three sets
of coelomic pouches and the ciliary systems of the larva clearly show that the
phoronids are notoneuralians. The adult phoronids have the tentacles typical of
brachiates.
Phylum BRACHIOPODA:
All recent brachiopods are characterized by a dorsal and a
ventral shell which enclose most of the soft parts. These shells may have evolved
independently in several lines which have been regarded as separate phyla
parallel with the phoronids (Wright, 1979). However, the presence in all
brachiopods of a dorsal and a ventral mantle-fold with mantle canals and setae
and the specialization of the protocoel into the ‘large lophophore canal’ clearly
characterize this group as monophyletic and separate it from the phoronids (see
also Rowell, 1982).
An unpublished study of Crania anomala by Stig Diding (Landskrona, Sweden)
throws new light on brachiopod embryology (a publication is in preparation).
Cleavage is radial and a coeloblastula is formed; gastrulation is embolic and the
larva swims by means of a uniform ciliation. The larva becomes elongated and
the blastopore now lies posteroventrally. The anterior and dorsal parts of the
internal cell layer consist of larger, lightly staining cells (entoderm) that develop
into an archenteron with a small cavity only in the anterior part. The posterior
and ventral parts of the cell layer (mesoderm) spread anterolaterally between
ectoderm and gut. The connection between the blastopore and the posterior
part of the coelom persists for some time, but the blastopore finally closes and
the mesoderm becomes arranged into four pairs of compartments: an anterior
pair, fused into a thin-walled narrow sac covering the anterior part of the gut,
and three pairs of conspicuous sacs lateral to the gut. The ectoderm laterodorsal
to the three posterior coelomic sacs forms invaginations from which setae
develop. The fully formed larva is uniformly ciliated with an anterior, somewhat
enlarged head and a short cylindrical body with three pairs of setal bundlesthe larva can quite easily be mistaken for that of a polychaete.
Metamorphosis has not been followed, but it appears probable that the anterior
ANIMAL PHYLOGENY
273
coelom gives rise to the (pre-oral) large arm canal and the second pair of
coelomic sacs becomes the (post-oral) small arm canal with the canals to the
tentacles. The third pair of coelomic sacs becomes the large body cavity and the
fourth pair becomes the small anal chamber.
In Lingula (Yatsu, 1902) the mesoderm is reported to be given off from the
archenteron as compact lateral masses, in which a cavity is subsequently
formed; the blastopore becomes slit-like and finally closes completely. In the
articulates (Long, 1964) a U-shaped, one-layered fold of gastrodermis divides
the archenteron into a median gut and a ring-shaped coelomic cavity; these
cavities are initially confluent at the posterior end of the embryo, but this
connection is soon closed, as is the posterior connection between the right and
left parts of the coelom; here also the blastopore closes laterally.
The articulate larvae (Long, 1964) are lecithotrophic and their bodies show
constrictions so that three body regions can be recognized: an anterior lobe with
an apical tuft and a ring of locomotory cilia, a ring-shaped mantle lobe on which
bundles of setae soon develop, and a posterior lobe which becomes the pedicle.
A crescentic pouch develops from each of the lateral coelomic compartments
and comes to occupy the mantle lobe. The stomodaeum develops a t the ventral
part of the anterior groove in the region of the anterior part of the closed
blastopore, but soon moves to the centre of the apical lobe. At metamorphosis
the larva settles with the pedicle, and the mantle lobe reverses to cover the
apical lobe and starts to secrete the shells. The first pair of tentacles develops
lateral to the stomadaeum, and further pairs of tentacles develop from the more
dorsal areas of the apical lobe.
The shelled larva of Lingula (Yatsu, 1902) and the initially shell-less larva of
Discinisca (Chuang, 1977) swim and feed by means of the ciliated tentacles
which form an upstream collecting system around the mouth.
The coelomic compartments and their derivation from the embryonic cavities
show much variation among the species (see, for example, Hyman, 1959; Long,
1964; Pross, 1980; and the unpublished study by Diding), but it is natural to
interpret the coelomic cavities of the Crania larva as protocoel, mesocoel and
metacoel plus a small extra compartment around the anus. This is supported by
the similarities between the coeloms of the Crania larva and of the actinotroch.
The structure of the shells is very similar to that of the calcified exoskeletons
of many gastroneuralians (see, for example, Nielsen & Pedersen, 1979), but the
terebratulids also have a calcified endoskeleton (in the lophophore) comparable
to that of the echinoderms (Schumann, 1973).
The poorly known nervous system comprises a subenteric ganglion on the
ventral side of a circumenteric nerve ring; a pair of small supraenteric ganglia
are found in certain articulates (Bemmelen, 1883).
The tentacles of both larvae and adults are ciliated and form an upstream
collecting system. Atkins (1958), Storch & Welsch (1976) and Reed & Cloney
(1977) stated that there is one cilium per cell in all the ciliary tracts, while
Gilmour (1978, 1981) reported that the lateral and frontal cells of Laqueus and
Glottidia are multiciliate. My transmission electron micrographs of tangential
sections of tentacles of Crania, Discinisca, Lingula and Terebratulina clearly show
that all cells are monociliate.
The phyiogenetic affinities of the brachiopods have been a matter of
discussion for many years. The shells and the setae may indicate relationship
13
274
C. NIELSEN
with the gastroneuralians (see Gustus & Cloney, 1972), other characteristics are
more reminiscent of the notoneuralians (e.g. ciliary apparatus, mesodermal
lophophore skeleton and coelom), and a whole number of characteristics are
open to people’s whims. I n accordance with the trochaea theory I emphasize
the presence of an upstream collecting system with monociliate cells around the
mouth and the development of the coelom of Crania, and accordingly regard the
brachiopods as notoneuralians.
Phylum ECHI.VODERMd%4: Most of the echinoderm classes comprise species which
have planktotrophic larvae with an upstream collecting band of single cilia on
monociliate cells around the mouth (Strathmann, 1971), as in the tornaria
larva, but none of the echinoderm larvae have an archaeotroch. The benthic
stages are not bilaterally symmetrical and are not easily compared to other
types. However, it seems possible to envisage the evolution of the ancestral
echinoderm from a tornaria-pterobranch-like ancestor which settled with the
apical/frontal pole (as in crinoids and some asteroids) and in which the anterior
left part of the body became greatly reduced and the posterior part of the body
became curved perpendicular to the original longitudinal axis of the body
(Grobben, 1923).
The blastopore becomes the anus in most species. I n some holothurians
(Labidoplax; see Selenka, 1883) the distal part of the archenteron bends dorsally
and forms a connection with the exterior (the hydropore); it later bends
ventrally, leaving a coelomic pouch in connection with the hydropore, and
forms a new opening to the exterior (the mouth). In most species three pairs of
coelomic sacs (protocoel, mesocoel, metacoel) can be recognized at some stage,
almost always formed as pockets from the archenteron. The nervous system of
the pentamerous adult is difficult to compare to that of the bilateral types, but,
for example, in echinoids the ectoneural nervous system forms as tube-shaped
infoldings like the neural tube of the enteropneusts (Ubisch, 1913).
C YH TO I R E TA
In this line only the enteropneusts have retained the planktotrophic tornaria
larva whereas all the chordates lack primary larvae. The ancestral adult was
benthic, creeping and elongated with an almost straight gut, and a
multiplication of the gill pores soon took place. Each gill pore became
specialized by the formation of the dorsal tongue bar, which makes the gill
openings U-shaped, and the development of supporting skeletal rods. The
homology of the gill structures of the recent enteropneusts and chordates is well
established (see, for example, Horst, 1939). (The name Cyrtotreta-arched
openings-refers to this characteristic shape of the gill slits).
The enteropneusts have a tube-shaped infolding (open at both ends) of the
nerve centre in the collar (mesosome), whereas the central nervous system of the
chordates develops as a tube-shaped infolding from the whole length of the
dorsal side of the embryo.
Phylum E . N r E R O P . v E L ~ s 7 ; i : Some of the enteropneusts have a typical notoneuralian
life cycle with a planktotrophic tornaria larva and a creeping, benthic adult.
The tornaria has a neotroch of single cilia on monociliate cells functioning as an
upstream collecting system around the mouth and an archaeotroch of
compound cilia around the anus (Strathmann & Bonar, 1976). The lining of the
ANIMAL PHYLOGENY
2 75
secondary body cavities is formed probably exclusively from the archenteron,
and three sets of cavities can be recognized: protocoel, mesocoel and metacoel.
In some enteropneusts the protocoel is formed from the apical part of the
archenteron at an early stage and soon connects with the exterior via the
hydropore (Heider, 1909). The mesocoelic and metacoelic cavities may be
formed in a number of ways: as pouches from the protocoel, as hollow or solid
evaginations from the archenteron, or from isolated (?ento)mesodermal cells
(Korschelt, 1936). The gill slits originate from a series of outpocketings from the
oesophagus of the late tornariae (Ritter & Davis, 1904) or in later stages
(Hyman, 1959).
The larval nervous system comprises an apical organ, in some species with a
pair of eyes; the apical organ is lost at metamorphosis. The adults have a
longitudinal, dorsal main nerve which is epithelial and has a tube-shaped
portion at the mesosome. The tube is formed at metamorphosis through an
infolding of the ectoderm exactly as in Brunchiostomu (Morgan, 1894), and
Bullock (1945: 75) described the structure as “simply a submerged strip of
epidermis”.
In the adults feeding is mainly through collection of deposited particles by
mucus secreted by the proboscis and transported to the mouth by cilia, while
the capture of suspended particles by the gill apparatus is of minor importance
(Thomas, 1972). It is not known whether this type of feeding represents a
primitive condition or a specialization from the filter-feeding type of the
chordates, as suggested by Knight-Jones (1953).
Chordata
Similarities between the Urochordata, Cephalochordata and Vertebrata have
been documented in so many papers that the discussion can be restricted to
some of the embryological information which makes it possible to relate the
chordates to the other notoneuralians.
None of the chordates have primary larvae which feed. In most forms the eggs
are provided with a large amount of yolk or the embryo is nourished by the
mother. The formation of a blastopore can, however, be recognized in many
forms and the anus is formed in the blastopore region. The most characteristic
features of the chordates are the formation of neural folds, which fuse in the
dorsal midline so that the central nervous system becomes tube-shaped, and the
formation of a notochord from the archenteron underlying the neural tube. The
posterior parts of the neural folds extend backwards along the sides of the
blastopore, and at their fusion they enclose the blastopore so that the
neurenteric canal is formed. Both mouth and anus are formed at a later stage.
Phylum UROCHORDA
TA.- Adult tunicates are highly specialized, sessile or pelagic,
filter-feeding organisms whose structure can only be related to that of other
animals in connection with their ontogeny.
In the ascidians, gastrulation, formation of the notochord, neural tube and the
neurenteric canal resemble those ofBrunchiostornu,especially in the molguilds which
have larvae without a tail (Berrill, 1931). In ascidians with the more usual
tadpole larvae the notochord moves to the tail region of the embryo (Conklin,
1905). The mesoderm originates from a pair of dorsolateral areas of the
archenteron, but there is no metamerism and secondary body cavities are not
276
C. NIELSEN
formed. Mouth, anus, atrium and gill slits develop at a later stage. The
notochord degenerates in connection with settling.
The lack of metamerism in tunicates may indicate that the ancestor of the
chordates was unsegmented, and that cephalochordates and vertebrates
represent a monophyletic line.
Phylum CEPHALOCHORDATA:
Amphioxus (Branchiostoma) has had a central position
in discussions on deuterostome evolution for more than a century, and its
affinities with both tunicates and vertebrates are well established. Here it must
therefore suffice to make a few comments on its embryology to emphasize some
of the characteristics of the chordate line.
The embryology has been described by Hatschek (1881) and Conklin (1932)
and their descriptions agree in all important details. The gastrula is somewhat
oblique, in later stages with the blastopore closest to the somewhat flattened
presumptive dorsal side. A pair of dorsolateral ectodermal folds fuse along the
dorsal midline and a neural tube is formed; this tube is open posteriorly only for
a short time and then the folds overgrow the blastopore and the neurenteric
canal is formed. The notochord is formed from the archenteron underlying the
neural tube. A series of coelomic pouches are formed from the archenteron on
each side of the notochord. Mouth, anus and gill slits form later.
The adult lancelet uses the gill slits as a particle-collecting filter with a slime
net, as do the tunicates, and this appears to be the primitive condition within
the chordates.
Phylum VERTEBRATA:
The vertebrates are the most complicated of the
chordates, but the embryology of the amphibians shows detailed similarities
with that of Brunchiostoma, and the many well-documented homologies, for
example of the thyroid with the endostyle of cephalochordates and tunicates,
underline the common ancestry of the chordates.
DISCUSSION OF CHARACTERS USED IN THE CLASSIFICATION OF PHYLA
In principle, all heritable characters can be of phylogenetic importance,
but only few have turned out to be useful in elucidating the evolution of the
major animal groups. Early phylogenies were based solely on morphology and
embryology, but nevertheless we still lack important information, especially
about embryology of several phyla. Newer studies on ultrastructure and
biochemistry are even more fragmentary in their coverage, but have provided
important information, especially on the early evolution of animals.
Palaeontology has so far not contributed to our understanding of early animal
radiation. Most of the phyla can be traced back to the Cambrian, and traces of
metazoan activity have been identified in the form of burrows and traces of
various forms as far back as the Mid-Riphean about 1000 million years ago
(Brasier, 1979). This only shows that the small, soft-bodied early metazoans
evolved in the Mid-Riphean or perhaps even in the Lower Riphean, but tells us
nothing about their characters.
Most of the characters used in the classification presented in the section above
are discussed in the following. References to literature are, in this section, mostly
restricted to papers of comparative type, whereas the more specific references
are generally to be found in the sections about the respective phyla.
ANIMAL PHYLOGENY
277
The trochaea theory is based on a series of assumptions about evolutionary
changes in structures and functions in relation to the whole life cycles of the
ancestral forms. These assumptions are based on observations on four sets of
intimately connected characters, namely the pelago-benthic life cycle, the fate of
the blastopore/origin of the definitive mouth, the larval ciliary bands, and the
ontogeny and location of the nervous system. For practical reasons these
characteristics are discussed separately below but it must be emphasized that
they are mutually dependent in the theory.
Pelago-benthic l$e cycles
Many authors, but especially Jagersten (1972), have emphasized the
importance of dealing with whole life cycles in phylogenetic considerations. A
crucial question is, therefore, whether direct development or life cycles
comprising lecithotrophic larvae are derived from life cycles comprising
planktotrophic larvae or vice versa. Jagersten ( 1972) considered the pelagobenthic life cycle with a planktotrophic larva as the ancestral condition for all
metazoans. Strathmann ( 1978) discussed the larval stages of marine
invertebrates and concluded that planktotrophy is the original condition and
that it is easily lost but not easily reacquired. I agree completely with these
views, and the ancestral character of the pelago-benthic life cycle with
planktotrophic larvae is one of the founding stones of the trochaea theory.
Living larval and adult forms reflect adaptations to the pelagic and benthic
environments, and a number of parallel specializations can be observed in
various groups, for example a posterior extension of the prototroch area in
larvae of sipunculans, protobranch bivalves and ectoproct bryozoans-the SOcalled pericalymma larvae (see Salvini-Plawen, 1980).
Profound changes in structure take place at the metamorphosis of most
present-day organisms when organs used for swimming and/or suspension
feeding lose their functions and new structures become engaged in feeding and
locomotion. Equally important changes in structure and function must have
been involved when organisms with pelago-benthic life cycles evolved from
holoplanktonic ancestral forms: gastroneuron from trochaea and notoneuron
from tornaea.
Trochaea and the trochophore larva of gastroneuron were suspension feeders
which strained particles from the water (and swam) by means of a downstream
collecting band of compound cilia. When the earliest gastroneuralians took up a
creeping, benthic adult life the following changes occurred (see Fig. 4): the
compound cilia retained their function in the larvae but not in the adults, where
they disappeared; the zone of single cilia around the blastopore became
specialized to form a particle-transporting area around the mouth (an area
corresponding to the adoral ciliary zone in the trochophore) and a locomotory
band along the line of fusion of the blastoporal lips (corresponding in the
trochophore to the gastrotroch, which transports rejected particles backwards so
that they can be swept away by the telotroch). The road was then open for all
sorts of specializations both in the pelagic, planktotrophic larvae and the
benthic, deposit-feeding adults.
Tornaea and the tornaria larva of notoneuron were suspension feeders which
strained particles from the water by means of an upstream collecting system of
C. NIELSEN
278
single cilia, the neotroch, around the mouth and swam by means of the
compound cilia of the archaeotroch. The adult notoneuron probably resembled
Cephalodiscus in having the neotroch elaborated to form small tentacles and in
having a pair of small gill pores. From there one evolutionary line led to the
mainly sessile forms with large tentacle crowns (Cephalodiscus and Atubaria with a
pair of small gill pores, and Rhabdopleura, brachiopods and phoronids without
gill pores), and another line to creeping types as the enteropneusts without
tentacles but with many gill slits. The echinoderms probably evolved from the
first-mentioned line; the three chordate phyla are more likely descendants from
the enteropneust line, as indicated, for example, by the detailed similarities of
the gill slits.
It is thus assumed that radial symmetry characterized the early pelagic
organisms and the early cnidarians, whereas bilaterality evolved in connection
with the evolution of creeping habits. The various types of sessile descendants of
the bilateral creeping organisms show many parallel specializations: a U-shaped
gut with mouth and anus rather close to each other and a correspondingly short
ventral (bryozoans) or dorsal (sipunculans, pterobranchs, phoronids) side, and a
comparatively small and usually rather concentrated nervous system.
Fate of blastoporelorigin of deJinitive mouth
The widely accepted division of the ‘Bilateria’ into Protostomia and
Deuterostomia indicates the phylogenetic importance generally attributed to the
fate of the blastopore. In the Protostomia the blastopore should become the
definitive mouth (later modified to indicate that the blastopore should become
mouth anus) while it should become the anus in the Deuterostomia. Several
recent authors (e.g. Siewing, 1981) have spoken in favour of abandoning this
character, and from the discussions of the various phyla it can be seen that it is
highly variable within several phyla and it definitely cannot be used alone (see
also Fioroni, 1980).
The fate of the blastopore is an integral part of the trochaea theory. Most
gastroneuralian phyla comprise examples of the condition considered ancestral
of the group, namely that the lateral lips of the blastopore fuse along a
midventral line leaving only an anterior mouth and a posterior anus. But much
variation occurs, and both in annelids and molluscs almost every conceivable
modification has been realized. I n the notoneuralians the blastopore should
persist as the anus whereas the definitive mouth should be a new structure
formed in the anterior (more apical) part of the body; here also a number of
different ways of forming the definitive mouth and anus have been observed,
but two rather distinct types can be recognized: (1) in many enteropneusts and
echinoderms the blastopore directly becomes the anus, and in some brachiopods
(Crania) the anus breaks through in the area of the closed blastopore; (2) in the
chordates the blastopore almost always closes completely and a new anus breaks
through in the same region of the larva. The blastopore closure is, however,
highly characteristic in this group: the neural folds, which fuse dorsally to form
the neural tube, extend posteriorly around the blastopore so that at their fusion
the blastopore becomes enclosed and the neurenteric canal is formed. This is
positively a larval specialization (caenogenesis) and the primary larva must be
considered as lost, the only trace being the ciliation of the early developmental
+
ANIMAL PHYLOGENY
279
stages. The secondary larva developed a tail, with notochord and neural tube
extending behind the anus.
Larval ciliary bands
Most planktotrophic larvae swim and feed by means of cilia around the
mouth, and in almost all species these cilia are arranged in bands which move
the water across the band. Most of these bands show diaplectic metachronal
waves (Knight-Jones, 1954). The cilia may strain particles in two different
ways: (1) in downstream collecting systems the cilia usually work together as
compound cilia and move the particles to the downstream side of the band; (2)
in upstream collecting systems the single cilia move the particles to the upstream
side of the band (Strathmann el al., 1972; Nielsen & Rostgaard, 1976). The
particles are usually transported to the mouth by bands of small single cilia that
move the particles along the band and often show orthoplectic (antiplectic)
waves (Knight-Jones, 1954). Planktonic lecithotrophic larvae swim by means of
ciliary bands which in most cases are easily identified with some of the bands of
the planktotrophic larvae. Many planktonic larvae have a prominent ring of
locomotory compound cilia around the anus, and additional rings of cilia occur
in several larvae, e.g. polychaete larvae.
The typical gastroneuralian pattern of prototroch, metatroch and telotroch of
compound cilia, with prototroch and metatroch forming a downstream
collecting system, and an adoral ciliary zone (plus gastrotroch) of single cilia is
found in trochophore larvae of polychaetes (Fig. 6A) and echiurans.
Many mollusc larvae (veligers) feed with the ciliary bands of the velum, and
prototroch, metatroch and adoral ciliary zone can easily be identified (Fig. 6B).
A telotroch is only found in solenogaster larvae, and the gastrotroch is perhaps
represented by the ciliation of the foot. Planktotrophic entoproct larvae exhibit
the same system as that of the veligers (Fig. 6C), while sipunculan larvae are
more difficult to interpret.
The pilidium larvae of most nemerteans have one ring of conspicuous cilia
(perhaps the prototroch), which at least in some species are arranged in
compound cilia forming a downstream collecting system. Some of the polyclad
turbellarians have planktotrophic larvae with a ring of cilia resembling that of
some of the pilidium larvae,
Rotifers have direct development and some adults feed and swim by means of a
ciliary system comparable to that of the trochophore, with prototroch and
metatroch consisting of compound cilia and an adoral ciliary zone consisting of
single cilia (Fig. 6D).
The typical notoneuralian pattern of a neotroch of single cilia on monociliate
cells forming an upstream collecting system and an archaeotroch of compound
cilia around the posterior part of the body (usually called telotroch, but
homologous with the whole archaeotroch of the trochaea) is found in the
tornaria larvae of the enteropneusts (Fig. 7A).
The young planktotrophic echinoderm larvae have a neotroch very similar to
that of the tornaria, but all echinoderm larvae lack the archaeotroch (Fig. 7B).
The neotroch is drawn out into delicate loops in the various types of larvae, and
these loops are arranged in such patterns that their cilia can also be used for
locomotion (Strathmann, 1971).
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C. NIELSEN
Figure 6. Ciliary bands of selected gastroneuralians. A, Annelid trochophore (based on a pectinariid
larva from Friday Harbor, Washington). B, Mollusc veliger (Crepidula, based on drawings in
Werner, 1955). C, Entoproct larva (based on Loxosorna pectinaricola from Denmark). D, Adult rotifer
(Meliferla,modified from Beauchamp 1965). a, adoral ciliary zone; g, gastrotroch; m, metatroch; p,
prototroch; t, telotroch.
The actinotroch larvae of Phoronis have an archaeotroch of compound cilia
and the row of tentacles behind the mouth carries a continuous band of single
cilia on monociliate cells, forming an upstream collecting system (Fig. 7C). This
ciliary band can be interpreted as the posterior part of the neotroch. The larvae
of the brachiopods Lingula (Fig. 7D) and Discinisca swim by means of a ring of
tentacles with an upstream collecting system of single cilia on monociliate cells
behind the mouth (as indicated by the swimming direction), and these cilia
must be interpreted as a neotroch.
All larvae of ectoproct bryozoans swim by means of single cilia arising from
an area which in some species is a narrow ring but which in other species covers
the whole surface of the larva; these cilia are not used in feeding but the general
morphology of the ciliated area (with many cilia per cell) resembles the 'serosa'
of sipunculans and solenogasters. I n the cyphonautes larva a U-shaped band of
single cilia on multiciliate cells forming an upstream collecting system occurs
behind the mouth. The ontogeny, location and structure of this band (one row
of cilia per cell) make it difficult to compare with other ciliary bands.
It is thus possible to interpret the ciliary bands of almost all planktotrophic
ANIMAL PHYLOGENY
28 1
Figure 7. Ciliary bands of selertrd notoneuralians. A, Enteropneust tornaria (based on a larva from
Fort Pciercc, Florida). B, Echinoderm plutcus (based on Dcndraster from Friday Harbor,
Washington). C, Phoronid actinotroch (based on drawings in SilPn, 1954b). D, Brachiopod larva
(based on Glollidza from Fort Pierce, Florida). a, archaeotroch; 11, neotroch; o, oral ciliary field.
larvae and also the ciliary bands of the adult rotifers in accordance with the
trochaea theory.
T h e structure of a number of ciliary bands will be the topic of a coming
paper.
Nervous pstems
The communication between the cells of the earliest blastaea must have been
directly between neighbouring cells. In connection with the establishment of a
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C. NIELSEN
preferred direction of swimming, special sensory cells must have become
concentrated at the apical pole, and this nerve centre was probably connected
with other areas through special nervous cells.
These early nervous systems were almost certainly diffuse, intra-epithelial
nerve nets with only little specialization. Early synapses may have been
symmetrical, i.e. capable of transmitting in both directions as in some living
cnidarians Uha & Mackie, 1967), but only polarized synapses are known from
living trochaeozoans. Other types of differentiation involved concentration of
specialized nerve cells into ganglia and neurons into nerve trunks surrounded by
mesoderm.
An apical organ is well developed in cnidarian gastrulaelplanulae.
Concentrations of nerves can be expected to develop in connection with bands
of locomotory cilia (single or compound) and this is very conspicuous in presentday ctenophores (where concentrations of nerves inhibit the movements of the
comb plates; see Horridge, 1974). A ring nerve was probably found along the
archaeotroch (at the edges of the mouth) in the trochaea, and this ring nerve
along the locomotory organ must have been connected to the apical sensory
organ by a number of nerves.
In gastroneuralian larvae (trochophores) the nervous system characteristically
comprises an apical brain connected to a nerve along the edges of the
blastopore, which has been partially closed by the fusion of the lateral lips so
that the ring nerve has been transformed into nerves along prototroch,
metatroch, ventral midline and telotroch. The main parts of the larval nervous
system can be recognized in the adults of most gastroneuralians: the brain
develops from the apical organ (sometimes a frontal organ is also involved) and
the main pair of ventral nerves originates along the ventral midline. There are
exceptions to this. In the parenchymians and the aschelminths the nervous
system is of the orthogonal type (see Reisinger, 1972) in which the main pair of
ventral nerves can usually not be recognized, but in the few types which have
primary larvae, for example some turbellarians, the development of the brain in
connection with the apical organ has been ascertained (see Kato, 1940). The
sessile entoprocts have larvae with apical and frontal organs which are lost at
the metamorphosis, when a new, ventral ganglion is formed from an epithelial
invagination. This is unusual in the gastroneuralians where the ventral nerves
and ganglia are generally formed through epithelial proliferation, whereas
infolding is the rule among notoneuralians. There are, however, other types of
gastroneuralians which form the ventral ganglia through invagination, for
example pseudoscorpions, in which Weygoldt (1964, 1965) observed a pair of
longitudinal ectodermal infoldings which divide to form the double row of
ventral ganglia, and millipedes where Dohle (1964) observed the formation of
ventral ganglia from a series of separate ectodermal invaginations.
Notoneuralian larvae have apical organs which are only slightly differentiated
in echinoderm and brachiopod larvae, whereas the actinotrochs of phoronids
and the tornaria larvae of enteropneusts have a more complicated organ, in
some tornariae even with a pair of eyes. There is no trace of an apical organ in
the chordates, but this is probably due to the lack of primary larvae. Although
the trochaea theory predicts the presence of a ringe nerve along the
archaeotroch and nerves connecting it with the apical organ, these nerves could
not be found in actinotrochs by Zimmer (l964), and I am not aware of any
ANIMAL PHYLOGENY
283
reports from tornaria larvae either. At metamorphosis the apical organ is shed
in actinotrochs and echinoderm larvae, and it degenerates in tornaria larvae
and brachiopod larvae. The adult nerve centre of phoronids and pterobranchs is
a basiepithelial concentration in the very short dorsal area between epistome
and anus. In the brachiopods the nerve centres are basiepithelial and the main
centre appears to be ventral, but further investigations are badly needed. The
echinoderms show a pentameric, likewise basiepithelial ectodermal nervous
system (and additional nerve concentrations in the walls of the coelomic canals).
In enteropneusts the nerve centre is a tube-shaped infolding of the dorsal
ectoderm of the mesosome. The central nervous system of the chordates arises as
an epithelial infolding of the dorsal side of the embryo as in the enteropneusts,
but in the chordates the neural tube extends posteriorly all the way to the anus.
It thus appears that there are two distinct types of adult nerve centres among
bilateral animals (Fig. 8): the gastroneuralian type which comprises a brain
notoneuralian central nervous system
gastroneuralian
apical brain
gastroneuralian ventral main nerves
FigurE 8. A comparison of central nervous systems of gastroneuralians and notoneuralians.
derived at least partially from the apical organ of the larva and a pair of
longitudinal ventral main nerves, and the notoneuralian type in which the
larval apical brain is lost at metamorphosis and the whole adult nerve centre is
derived from a dorsal, longitudinal area.
Cleavage patterns
Cleavage patterns show much variation throughout the animal kingdom, and
most authors agree that the regular, holoblastic cleavage of rather small eggs
represents the primitive condition. Large, yolk-rich eggs, sometimes with
discoidal or superficial cleavage, irregular cleavage of placentally nourished eggs
and other deviations from the primitive pattern have evolved independently
within a number of phyla and are therefore of minor value in phylogenetic
considerations at the interphyletic level.
Three types of holoblastic cleavage are commonly recognized: radial, bilateral
and spiral cleavage (Siewing, 1969), but for several phyla there is no general
agreement about the interpretation of the cleavage patterns observed.
The most easily recognized cleavage type is spiral cleavage, which is
characterized by a series of highly specialized traits. (1) The cleavage is
determined, i.e. the fate of the various parts of the embryo is fixed, already at
the time of the first cleavage; only in some nemerteans is each blastomere of the
two-cell stage capable of developing into a complete larva (Horstadius, 1971).
(2) At the four-cell stage one of the blastomeres (D) is usually larger than the
others and this quadrant marks the posterior-dorsal part of the embryo. As the
polar bodies mark the apical pole of the embryo, the axes of the embryo can be
recognized at this early stage. (3) At the early cleavages the mitotic spindles are
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C. NIELSEN
inclined alternatingly to left and right with respect to the main axis of the
embryo, so that a spiral arrangement of the blastomeres ensues. (4) At the 64-cell
stage each of the blastomeres can be identified and their fates are identical in
annelids and molluscs; the 4d-cell, for example, becomes the main source of the
mesoderm (see, for example, Sewing, 1969: 65). Deviations from this scheme
occur within both phyla, but the pattern must be considered basic for spiral
cleavage.
The spiral cleavage pattern has been found in a number of gastroneuralian
phyla: Annelida, Mollusca, Echiura, Sipuncula, Gnathostomulida, Nemertini,
Plathyhelminthes and Entoprocta, and it appears beyond doubt that these
phyla have evolved from a common ancestor with spiral cleavage. A few
arthropods show spiralian tendencies in their cleavage patterns, but their
development is generally much modified and primary larvae are lacking.
A number of other phyla, for example rotifers and nematodes, have been
claimed to have ‘modified spiral cleavage’ (see, for example, Costello & Henley,
1976), but their fate maps cannot be compared with the spiralian types and to
me it appears that the only characteristic shared with the spiral type is the high
degree of determination.
Given the restrictive definition of spiral cleavage outlined above, most other
cleavage types appear less characteristic. Radial cleavage, with a low degree of
determination, observed for example in cnidarians and echinoderms, appears
primitive, while the bilateral types and other types with a high determination
occur scattered among the phyla and have probably evolved a number of times.
Since all recent trochaeozoans are bilateral it is not unexpected that bilaterality
is often expressed in early embryological stages. The ctenophores have a
characteristic biradial cleavage, reflecting the biradial structure of the adults.
Mesoderm and coelom
A coelom is here defined as a body cavity surrounded by mesoderm, and the
discussion of mesoderm and coelom must therefore begin with the origin and
definition of the mesoderm.
Ectoderm and entoderm, the two primary germ layers, are defined
embryologically as the outer and the inner cell layer of the gastrula stage, and
the two terms can almost without problems be applied to the epidermis and the
gut epithelium of the adults. Mesoderm, the secondary germ layer, can be
defined as the cells situated between ectoderm and entoderm and-at least in
the adults-isolated from these by a basal lamina (exceptions discussed below in
the section on ultrastructure and special cell types). Cell junctions of the septate
and tight types are of course found between ectodermal cells and between
entodermal cells, but they should not be found between mesodermal cells and
cells of the primary germ layers. Cell junctions and basal lamina should
therefore be of use in distinguishing ecto-, meso- and entodermal elements in
organs of supposedly composite origin. The mesodermal cells originate from
ectoderm or entoderm by ingression or invagination.
From the above definition it follows that only gastraeozoans possess the three
germ layers. Sponges and placozoans have protective and digestive epithelia
with other cell types between them, but the two epithelia cannot be
homologized with ectoderm and entoderm, and a basal lamina is not present.
ANIMAL PHYLOGENY
285
Mesoderm may be classified according to its origin: from the ectoderm, from
the rim of the blastopore, or from the entoderm.
( 1 ) Mesoderm of ectodermal origin (ectomesoderm, mesectoderm) occurs in
many animal phyla, but has in most cases been studied only poorly. This type of
mesoderm is apparently formed by more-or-less diffuse ingression, not by
invagination. It does not usually form epithelia (see below).
Ectomesoderm is the dominant type, perhaps even the only type, of
mesoderm in the cnidarians.
In the spiralians, ectomesoderm (ectomesenchyme) is reported to originate
from the second and third micromere quartet (Sewing, 1969). I t has been
claimed that the muscles crossing the blastocoel of annelid trochophores develop
from ectomesodermal cells of the third micromere quartet, and that
ectomesoderm is involved in the development of prostomium and proboscis in
certain polychaete species, but further investigations are needed (Anderson,
1973). In Echiurus, cells of the second and third micromere quartet give rise to
the larval mesoderm, including muscles of body cavity and oesophagus, and to a
lining of the ectoderm of the larva resembling a coelomic lining (Baltzer, 1917 ) .
The amount of ectomesoderm in molluscs is highly variable. In the prosobranch
Paludinu it has even been reported that the entire mesoderm originates through
ingression of ectodermal cells from the ventral area of the embryo, and that the
mesodermal organs have the same morphology as those of species in which the
mesoderm originates from the 4d-cell (Dautert, 1929). Also, nemerteans show
considerable variation in the development of ectomesoderm, and Hammarsten
( 19 18) reported that the entire mesoderm of Mulucobdellu originates from the
cells 2a1 I-2d' I . In turbellarians, cells originating from the second (and
perhaps also the third) micromere quartet (or duet) contribute to the formation
of the mesenchyme (Bresslau, 1928-1933). Some of the mesodermal cells of the
nematode embryo have been interpreted as ectomesoderm, but the drawings of
the embryos and the diagram of the cell lineage (see Table 2) make it more
natural to regard the three areas of mesoderm-forming cells as belonging to the
blastopore lips.
There is to my knowledge no indication of ectomesoderm in the brachiates
except for small areas associated with the hydropore, where the entomesodermal
pocket from the archenteron contacts the ectoderm.
The mesodermal cell types originating from the neural crests in the
vertebrates (see, for example, Sewing, 1969) represent a specialization
connected with the evolution of the neural tube of the chordates, and are
perhaps best regarded as representing a fourth type of mesoderm.
(2) Mesoderm originating from the blastopore lips is characteristic of the
gastroneuralians. In spiral cleavage the 4d-cell typically gives rise to all the
mesoderm and this pattern can be recognized even when cleavage has been
somewhat modified (Sewing, 1969). As can be seen from the above,
ectomesoderm partially (or in some cases even completely) replaced 4dmesoderm in several species, but this is not reflected in the morphology of the
mesodermal structures.
The origin of the mesoderm of the aschelminths is poorly known. In some
nematodes (Table 2) the mesodermal cells form a horseshoe-shaped row along
the anterior and lateral blastopore lips, and in some gastrotrichs (Table 3) the
cells which give rise to entoderm and mesoderm form a ring around the
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C. NIELSEN
blastopore. The origin of the mesoderm in the other aschelminth phyla is
unknown except in the chaetognaths, which are discussed below.
(3) Mesoderm originating from the entoderm or the cells at the vegetal pole
of the blastula is characteristic of the protornaeozoans and is also found in
chaetognaths. In ctenophores the mesodermal cells are first situated at the
vegetal pole and then move to the apical part of the archenteron at gastrulation
(Table 4). The micromeres that give rise to the primary mesenchyme in
echinoderm embryos are likewise situated at the vegetal pole, but they usually
move into the blastocoel before gastrulation.
The notoneuralians generally have the ‘archimeric’ pattern of coelomic
pouches: protocoel, mesocoel and metacoel; these coelomic compartments are
formed after gastrulation. The archimeric coelomic pouches originate from
various areas of the archenteron through invagination, ingression of cells or a
combination of these methods. It is not possible a priori to identify one of these
conditions as the more primitive, but it is possible to arrange the different modes
of mesoderm-sac formation in a morphological series which is in agreement with
the trochaea theory. This theory predicts that the coelom of the notoneuralians
originated from the walls of a canal leading from the apical part of the
archenteron to the exterior. In some holothurians such a canal actually occurs
at an early embryological stage; it soon loses connection with the archenteron
and develops into the protocoel, with the hydropore, while mesocoel and
metacoel are budded off later on. In many other echinoderms and in many
enteropneusts the apical part of the archenteron is pinched off and becomes the
protocoel, while mesocoel and metacoel and coelomoducts subsequently bud off
from the protocoel. Other enteropneusts exhibit a series of modifications with
protocoel formed from the apical part of the archenteron but with mesocoel and
metacoel formed as hollow or solid buds from other parts of the archenteron or
from isolated cells of unknown origin. Finally, in the brachiopod Crania the
mesoderm is formed from the posterior part of the archenteron as pockets that
extend forwards to form protocoel, mesocoel, metacoel and a fourth pair of
coelomic sacs (opisthocoel) . In phoronids the mesoderm cells separate from the
archenteron and become rearranged in the archimeric pattern. This pattern
cannot be recognized in the chordates, but in Branchiostoma the mesoderm
originates as pouches from the archenteron.
The chaetognaths have an enterocoelic mode of coelom formation, but other
characters point to a close relationship with some of the aschelminths. I have
chosen to put emphasis on these characters and thus to regard the mode of
coelom formation as a special feature of the chaetognaths.
The coelom of the notoneuralians thus has an origin which can be interpreted
as intimately coupled with the origin of the mesoderm. A number of authors,
especially Sewing (1980) have stressed the relationship of the phyla having
proto-, meso- and metacoel, at least in some stages of their development, by
uniting them as archicoelomates. The archimeric condition has been
demonstrated unequivocally only in pterobranchs, phoronids, brachiopods,
echinoderms and enteropneusts, which here together with the chordates are
classified as the notoneuralians. The structure of the gill apparatus clearly unites
the enteropneusts and the chordates, and it must be assumed that the chordate
ancestors had primary larvae with archimeric coelomic pouches and that this
basal feature was lost when the chordates lost the primary larva.
ANIMAL PHYLOGENY
287
Gastroneuralian coeloms show much variation, and it appears reasonable to
believe that coeloms have evolved several times within this group. Enterocoely
occurs in the chaetognaths (discussed above) and has been reported from
tardigrades (Marcus, 1929), but this latter may be based on a misinterpretation
(R. M. Kristensen, Copenhagen, pers. comm.). In all other coelomate
gastroneuralians the embryos have one or more pairs of compact masses of
mesoderm in which a cavity develops (schizocoely). T h e arthropod mixocoel is
interpreted as a confluent coelom and blastocoel formed by secondary partial
dissolution of the coelomic walls.
Among the spiralians the parenchymians are of a compact construction and
there is no trace of a coelom, except for the proboscis coelom of the nemerteans.
The bryozoans have a fluid skeleton which functions in the protrusion of
the hyposphere of the larva in entoprocts and of the polypide in the adult
ectoprocts. T h e entoproct larvae have a rather spacious primary body cavity
(blastocoel) traversed by muscle cells, whereas the adults have a very narrow
body cavity. In the ectoprocts the larvae are compact but the adults have a
spacious body cavity lined by mesoderm which arises after metamorphosis of the
larva. The origin of both mesoderm and coelomic cavity is much debated, but
since the origin of the mesoderm is unknown and the coelom is not developed in
the larva, the interpretation of ectoprocts as archimeric can best be
characterized as wishful thinking. The entoproct larva has a thin layer of
ectoderm surrounding a cavity functioning as a hydrostatic skeleton; I believe
that the coelomic lining of the ectoprocts is a mesodermal strengthening of the
wall of this hydrostatic skeleton. This implies that the coelom must have evolved
independently within the bryozoans.
Articulates are generally thought of as gastroneuralians with serially arranged
mesoderm sacs. It is widely accepted that the coelomic cavities may become
reduced, as for example in the hirudineans, or confluent, as for example in the
polychaetes Polyphysia and Pectinaria, but the origin and homology of the
coelomic spaces are much debated. With regard to the phyla included here
within the articulate group, it appears that segmentation is not necessarily a
basic articulate character. T h e early articulates probably had muscles both at
the body wall and the gut and one or perhaps rather a lateral pair of cavities
lined by mesothelium (coeloms). A compartmentalization of these primary
coelomic cavities has occurred in sipunculans (tentacle and body coeloms),
annelids, arthropods and perhaps in molluscs, while the teloblastic addition of
paired coelomic sacs can be interpreted as a later specialization. A detailed
discussion of the molluscan segmentation is given by Wingstrand (1985).
T h e mesoderm and body cavities of aschelminths show much variation. I n
nematodes, nematomorphs and gastrotrichs there are only longitudinal muscles
in the body wall, and these muscles form a continuous layer only interrupted by
some longitudinal epidermal thickenings with nerves. T h e gut is naked in
nematodes and nematomorphs, but in some gastrotrichs the longitudinal muscle
cells completely surround a pair of narrow, longitudinal cavities so that the gut
is covered by mesoderm. According to the definition used here these cavities
must be called coeloms. T h e chaetognaths have a similar layer of longitudinal
muscles, but the other aschelminth groups have both longitudinal and circular
muscles, which in some phyla, for example rotifers and kinorhynchs, are
individual muscles rather than continuous layers. This variation indicates that
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C. NIELSEN
the discussions about the significance of coeloms in aschelminths are rather
futile, at least at this stage of knowledge.
The importance of fluid-filled body cavities for the movements of the
organisms has been stressed by several authors (see, for example, Clark, 1964).
Here it should only be pointed out that both primary (blastocoelic) and
secondary (coelomic) cavities may function as fluid skeletons. Even intracellular
structures, such as the vacuoles in the pharyngeal cells of the gymnolaematous
bryozoans (Bullivant & Bils, 1968), may have this function, clearly showing that
hydrostatic skeletons have evolved many times. Also, the hydrostatic skeletons
formed by coelomic cavities appear to have evolved a couple of times, and from
the above discussion it should be clear that the coeloms of articulates and
notoneuralians are not homologous, although they have the same general
situation and function. Therefore, the existence of a common coelomate
ancestor, sometimes postulated for the bilateral metazoans, appears highly
unlikely.
Ultrastructure and special cell bpes
Electron-microscopical techniques have added new dimensions to the study of
animal structure, and their importance for the understanding of animal
evolution has been emphasized by several authors (e.g. Storch, 1979).
Among extracellular structures, basal laminae appear to be of phylogenetic
significance. They have not been observed in sponges and placozoans, but have
been found in almost all gastraeozoans, which points to a special, uniform
structure of the gastraeozoan epithelia. Only acoelous turbellarians are reported
to lack a basal lamina (Pedersen, 1983), but the extracellular membrane
surrounding the statocyst in Convoluta (Ferrero, 1973) may be interpreted as one.
Many reports of basal laminae are based on light-microscopical investigations
and there has been considerable inconsistency in terminology (basement
membrane, subepidermal membrane etc.) , New investigations using modern
methods, such as immunohistochemistry, appear necessary for a full
understanding of the significance of the basal lamina (see Pedersen, 1983).
Cuticular structures may also contribute to our understanding of animal
evolution. The intracellular (‘internal’) cuticle of rotifers, acanthocephalans and
perhaps also of chaetognaths is a unique structure which must be considered of
high phylogenetic significance. The normal, extracellular cuticles have been
used in several discussions (see, for example, Rieger & Rieger, 1976; Coomans,
1981b) and are included in the discussions of some phyla, but it appears rather
premature to draw wide-ranging conclusions from the still rather scattered
information.
Structures of the plasma membrane including cell junctions may also be
drawn into the discussion. The plasma membrane of ciliary (flagellar) bases
shows intermembranous particles in a 3 (-5)-stringed ‘necklace’ pattern in all the
metazoans investigated, while a series of other patterns are found in ‘protozoans’
(including choanoflagellates: Bardele, 1983; pers. comm.) . Investigations of the
cilia of placozoans, dicyemids and orthonectids could perhaps contribute to our
understanding of the relationships of these groups.
Cell junctions are another characteristic of metazoans. Septate or tight
junctions occur along the distal cell contact areas of the epithelia of all
ANIMAL PHYLOGENY
289
metazoans where they seal off the extracellular space inside the organisms so
that molecules in this region are not lost to the surroundings (Staehelin, 1974).
Gap junctions (arrays of membrane particles forming cylinders which connect
cells through canals with a diameter of about 1.5 nm; see Unwin & Zampighi,
1980) appear to be characteristic of the gastraeozoans, indicating a more
intimate contact and coordination between the cells (Mackie & Singla, 1983).
The presence of mitochondria with flattened cristae unites the choanoflagellates and the metazoans and isolates them from almost all the
heterotrophic protist groups (including the ciliates), which have tubular cristae;
flat cristae are also found in the kingdom Chlorophyta, in the Rhodophyta and
in the non-flagellate Fungi (Taylor, 1978).
The structure of cilia (flagella) is of high importance in protist phylogeny
(see, for example, Moestrup, 1982). T h e vane observed on the cilia of
choanoflagellates and sponge choanocytes is a unique feature, and the
similarities of the whole collared unit underlines the relationships of the two
phyla. Not all sponge cilia have a vane; the short cilia of the larvae lack a vane
and, moreover, resemble those of, for example, larvae of cyclostome bryozoans
and certain turbellarians also in their coordinated movements with metachronal
waves.
The structure of gastraeozoan locomotory cilia is rather uniform, but cilia arc
important organelles of several special cell types or organs which have been used
in phylogenetic discussions, for example photoreceptors, spermatozoa and
protonephridia.
Photoreceptor cells were at one time thought to be of two distinct types: the
ciliary type characteristic of coelenterates and deuterostomians and the
rhabdomeric type characteristic of protostomians. As can be seen from the
excellent review by Coomans (1981a) both types have now been found in
several phyla, and in some cases even in the same animal, and the various types
of photoreceptor cell occur in a number of obviously non-homologous eyes. One
can only agree with Coomans (1981a: 59) that “the photoreceptor type could
indeed be more linked with ecology and behaviour than with phylogeny.”
Also, protonephrida and other cyrtocytes (Kiimmel, 1962) are still in need of
further investigation both with respect to structure and to function, and so far
the cyrtocytes have contributed only little to our knowledge of metazoan
evolution (Wilson & Webster, 1974).
The morphology of the spermatozoa may be a characteristic of the
metazoans, but since sexual processes have not been observed in choanoflagellates we do not know whether spermatozoa are also present in this group.
The spermatozoan type considered primitive has a round head with the
chromosomes, a short midpiece with mitochondria1 material surrounding two
centrioles, and a long flagellar tail, and has been found in most of the metazoan
phyla (Bacetti & Afzelius, 1976). Only detailed similarities between highly
specialized spermatozoa can therefore be used as indicators of close relationships
(e.g. the spermatozoa of pentastomids and certain crustaceans).
Biochemistry
Various types of biochemical information have been used in discussions of
phylogeny, but so far with only limited success. An exception is collagen, which
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290
is now believed to be restricted to metazoans (Adams, 1978), but it is unknown
whether the choanoflagellates can synthesize collagen. Also, acetylcholine
/cholinesterase appears to be restricted to metazoans.
Sialic acids have been searched for in a large number of eukaryotes and
appear to be restricted to echinoderms, enteropneusts, cephalochordates and
vertebrates (Warren, 1963; Segler et al., 1978). Chitin has now been critically
searched for in most phyla and has turned out to be absent in sponges,
parenchymians, sipunculans, ctenophores, echinoderms, cephalochordates and
vertebrates (Jeuniaux, 1982). The distribution of sialic acids and chitin suggests
that the echinoderms are closer to the cyrtotretes (enteropneusts chordates)
than to the other phyla here classified as brachiates; this is not excluded by
morphological or embryological facts, but more information must be gathered
before a firm conclusion can be reached.
In most cases the investigations have not dealt with a sufficient number of
phyla, and only general trends have been suggested. Studies of amino-acid
sequences of cytochrome c and other proteins are still too scattered to be of
independent value (Dayhoff & Schwartz, 1981).
+
CONCLUSION
The phylogenetic tree outlined in Fig. 2 is based on the trochaea theory
and the discussion of phyla and types of characters above have revealed that a
number of additional characters can be added to important ramifications of the
tree (Fig. 9).
BRACH IATA
CYRTOTRETA
ciliated tentacles
SPlRALlA
ASCHELMINTHES
spiral cleavage
4d-mesoderm
mesoderm from vegetal cells
multiciliate cells
cnidoblasts
Porifera
basal lamina nerve cells synapses
gap lunctions loss of ciliary vane
septateltight )unctions collagen Spermatozoa
acetylcholinelcholinesterase ciliary necklace
Figure 9. A cladogram of the main animal groups showing characters which are independent of the
rrochaca theory; compare with Fig. 1.
ANIMAL PHYLOGENY
29 1
The diagrams comprise a series of hypothetical ancestors, and all these as well
as the intermediate forms between them are believed to have been viable in the
environments where they are supposed to have lived. This must be an
indispensible condition of any phylogenetic theory.
The phylogenetic tree presented in Fig. 2 implies only few examples of
convergent evolution of fundamental ground-plan characters, and I believe that
i t has a higher probability than those presented previously.
The several theories about the evolution of the early metazoan types were
discussed in the paper describing the trochaea theory (Nielsen & Narrevang,
1985) and the classification of the phyla presented here has been discussed in the
two main sections above. However, one special feature of the trochaea theory
deserves mentioning here: the theory proposes that both bilaterality and coelom
evolved independently in gastroneuralians and notoneuralians. This makes it
meaningless to derive the schizocoelic body cavities of the gastroneuralians from
the enterocoelic body cavities of notoneuralians, the tornaea larva from the
trochophore, the upstream collecting ciliary systems from the downstream
collecting ciliary systems, and the notoneuralian central nervous system from the
gastroneuralian central nervous system and vice versa.
Finally, I express my hope that this analysis will provoke not only new
discussions of existing information but also investigations in areas where
important knowledge has been shown to be lacking.
ACKNOWLEDGEMENTS
The first draft of this paper was written in collaboration with Dr Arne
Narrevang (Copenhagen) and I wish to thank him and his students for much
important information and inspiration. Drs H.-E. Gruner (Berlin), R.
Strathmann (Friday Harbor) and R. Eakin (Berkeley) have seen early versions
of the manuscript and are thanked for valuable comments. The final version has
been scrutinized by Drs R. D. Barnes (Gettysburg), K. G. Wingstrand
(Copenhagen) and 0. Tendal (Copenhagen) whom I thank heartily for much
constructive criticism. Thanks are due to Oxford University Press and
Systematics Association for permission to reproduce Figs 3-5 and to M r R. Nielsen
for drafting Figs 7 & 8.
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