Download The Phylogenetic Position of Entoprocta

INTEG.
AND
COMP. BIOL., 42:685–691 (2002)
The Phylogenetic Position of Entoprocta, Ectoprocta, Phoronida, and Brachiopoda1
CLAUS NIELSEN2
Zoological Museum (University of Copenhagen), Universitetsparken 15, DK-2100-Copenhagen, Denmark
SYNOPSIS. Ectoprocts, phoronids and brachiopods are often dealt with under the heading Tentaculata or
Lophophorata, sometimes with entoprocts discussed in the same chapter, for example in Ruppert and Barnes
(1994). The Lophophorata is purported to be held together by the presence of a ‘‘lophophore,’’ a mesosomal
tentacle crown with an upstream-collecting ciliary band. However, the mesosomal tentacle crown of pterobranchs has upstream-collecting ciliary bands with monociliate cells, similar to those of phoronids and
brachiopods, although its ontogeny is not well documented. On the contrary, the ectoproct tentacle crown
carries a ciliary sieving system with multiciliate cells and the body does not show archimery, neither during
ontogeny nor during budding, so the tentacles cannot be characterized as mesosomal. The entoprocts have
tentacles without coelomic canals and with a downstream-collecting ciliary system like that of trochophore
larvae and adult rotifers and serpulid and sabellid annelids. Planktotrophic phoronid and brachiopod larvae
develop tentacles at an early stage, but their ciliary system resembles those of echinoderm and enteropneust
larvae. Ectoproct larvae are generally non-feeding, but the planktotrophic cyphonautes larvae of certain
gymnolaemates have a ciliary band resembling that of the adult tentacles. The entoprocts have typical
trochophore larvae and many feed with downstream-collecting ciliary bands. Phoronids and brachiopods
are thus morphologically on the deuterostome line, probably as the sister group of the ‘‘Neorenalia’’ or
Deuterostomia sensu stricto. The entoprocts are clearly spiralians, although their more precise position has
not been determined. The position of the ectoprocts is uncertain, but nothing in their morphology indicates
deuterostome affinities. ‘‘Lophophorata’’ is thus a polyphyletic assemblage and the word should disappear
from the zoological vocabulary, just as ‘‘Vermes’’ disappeared many years ago.
INTRODUCTION
The four phyla discussed here have not found their
established positions in the zoological system (see Fig.
1). They are all sessile and use ciliated tentacles in
filter feeding. However, pterobranchs also show these
characteristics, and it is necessary to discuss the four
phyla more or less separately to assess their relationships (a more extensive discussion with detailed references can be found in Nielsen, 2001). Many recent
textbooks unite Ectoprocta (Bryozoa), Phoronida and
Brachiopoda under the name Lophophorata, a name
introduced by Hyman (1959), apparently because she
did not like the much older name Tentaculata. Her definition of the group was based on their common possession of a lophophore, i.e., a crown of ciliated mesosomal tentacles surrounding the mouth but not the
anus. Her definition logically includes the pterobranchs, but she (Hyman, 1959, p. 77) just stated that
‘‘The[ir] tentaculated arms are not to be regarded as a
lophophore although no doubt phylogenetically related
to that structure.’’ On the other hand, as pointed out
earlier (Nielsen, 2000, 2001), the tentacle crown of the
ectoprocts shows only superficial similarities with that
of phoronids and brachiopods; ectoproct tentacles have
lateral ciliary bands composed of multiciliate cells,
lack a longitudinal haemal vessel, and are probably not
mesosomal, whereas phoronid, brachiopod and pterobranch tentacles are monociliate, have a longitudinal
haemal vessel, and are probably mesosomal. Thus, it
appears that if the term lophophore is to be retained,
it should be used for the tentacle crowns of phoronids,
brachiopods and pterobranchs.
Morphology-based studies on metazoan phylogeny
do not agree on the position of the four phyla discussed here; the phylogeny which I favour and a phylogeny which most molecular biologists will probably
favour are shown in Figure 1. The main discrepancy
between the positions of the four phyla on the two
trees is the position of phoronids and brachiopods,
which are regarded as deuterostomes in the morphology-based tree, but as protostomes in the molecularbased tree.
ENTOPROCTA
Entoprocts are undoubtedly protostomes. They
show a number of characters which are found only in
spiralians, but their position within that group is difficult to assess.
The cleavage is spiral, and mesoderm is reported to
develop from the 4d-cell; the two first cleavages divide
the embryo into four quadrants, called A, B, C, and D
(Marcus, 1939; Malakhov, 1990; Fig. 2). Gastrulation
is described as embolic, but the funnel-shaped oesophagus (stomodaeum) is formed at about the same time,
and more detailed studies are needed to make the distinction between these two structures quite clear. The
larva is a typical trochophore with apical organ, prototroch and metatroch of compound cilia, adoral ciliary zone and gastrotroch of separate cilia, and a pair
of protonephridia; only the telotroch is missing (Nielsen, 1971, 1979). The apical organ resembles that of
other spiralians, with paired nerves and muscles to the
1 From the Symposium Lesser-Known Protostome Taxa: Evolution, Development, and Ecology presented at the Annual Meeting of
the Society for Integrative and Comparative Biology, 3–7 January
2001, at Chicago, Illinois.
2 E-mail: [email protected]
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CLAUS NIELSEN
FIG. 1. Comparison between a morphology-based phylogeny of the
Bilateria and a phylogeny based on HOX-genes and 18S rDNA. The
four phyla discussed here are underlined.
oesophagus/prototroch area and a pair of serotonergic
cells (Nielsen, 1971; Hay-Schmidt, 2000; Fig. 3).
There is a primary body cavity which functions as a
hydrostatic skeleton (Nielsen, 1971). Some species of
Loxosoma and Loxosomella have larvae with a long
planktotrophic stage, but the development of these larvae through the planktonic stage to metamorphosis has
not been followed. Particle collecting has not been de-
scribed in detail, but Jägersten (1964) observed particles being caught by cilia of the prototroch and carried
along the food groove to the mouth. So both structure
and function appear to conform to the general picture
of the downstream-collecting mechanism characteristic
of spiralian larvae (Riisgård et al., 2000). Most other
entoproct species have a short, free-swimming larval
stage and the larvae are apparently competent to settle
shortly after liberation (Nielsen, 1971).
Settling and metamorphosis show enormous variation between species (Nielsen, 1971). Settling with the
frontal organ appears to be the ancestral type, because
it involves the least morphogenetic change, whereas
the types with budding from a larval body which disintegrates appear highly derived. Larvae of the colonial forms settle with the ring of cells just apical to
the retracted prototroch, glued to the substratum by
secretions from three sets of glands in the foot (gastrotroch). The apical organ is lost after metamorphosis
and a new ‘‘brain’’ develops from the epithelium of
the ventral side of the atrium. Also the ciliary bands
disintegrate, and degenerating prototroch cells each
with a bundle of slowly beating cilia can often be seen
in the narrow primary body cavity of the newly settled
juveniles (Nielsen, 1971).
The adult loxosomatids are solitary, whereas the
other families comprise only colonial forms. The adult
feeding structures, i.e., tentacles with a downstreamcollecting ciliary system, develop anew after metamorphosis, but could possibly have been derived as
loops on the prototroch in the ancestor. Structure and
function of the ciliary bands are very similar to those
of the larvae, except that the two opposed bands of
compound cilia are of equal size (Riisgård et al.,
2000). There is a narrow primary body cavity with
protonephridia and few mesodermal elements (Nielsen
and Jespersen, 1997).
FIG. 2. Cleavage patterns in the major animal groups. The adult axes/planes are indicated: o-o, oral plane; t-t, tentacle plane; a/v-p/d, anterior/
ventral-posterior/dorsal axis; l-r, left-right axis. (From Nielsen, 2001.)
ENTOPROCTA, ECTOPROCTA, PHORONIDA,
AND
BRACHIOPODA
687
FIG. 3. Serotonergic nerve cells (black dots) in apical organs of protostome and deuterostome larvae. Protostomia: Mollusca (Phestilla),
Annelida (Polygordius), Entoprocta (Loxosoma), Ectoprocta (Membranipora), Platyhelminthes (Stylostomum). Deuterostomia: Phoronida (Phoronis), Brachiopoda (Lingula), Echinodermata (Strongylocentrotus), Enteropneusta (tornaria larva). (From Nielsen, 2001.)
The only character which is deuterostome-like is the
loss of the apical organ at metamorphosis; this is typically seen in all non-chordate deuterostomes. However, the structure of the apical organ is of the protostome type and sessile organisms often show highly
modified nervous systems, so this character probably
represents a convergence.
No entoproct character indicates a close relationship
with any specific spiralian phylum, so until further
knowledge has been gathered it seems practical to
place them at the base of the spiralian tree in a polytomy with Schizocoelia, Parenchymia and Gnathifera
(Nielsen, 2001; Fig. 1).
ECTOPROCTA
The ectoproct bryozoans are perhaps the most puzzling phylum in phylogenetic studies of the Bilateria.
The strong influence from the treatise of Hyman
(1959), where they are classified as ‘‘lophophorates,’’
seems more or less to have stifled discussions of alternative phylogenetic positions. Even some quite recent authors have regarded the lophophorates as
‘‘placed between protostomes and deuterostomes,’’
which is not in agreement with modern phylogenetic
systematics.
Early ectoproct development is poorly known. Cyclostomes and phylactolaemates have very peculiar
embryologies, which must be considered highly derived. Gymnolaemates show more usual developmental types, with a few species having planktotrophic cyphonautes larvae (in genera such as Membranipora,
Electra and Alcyonidium) whereas most other species
have more or less modified lecithotrophic larvae (Hayward and Ryland, 1998; Cadman and Ryland, 1996).
The early cleavage shows an unusual, biradial pattern,
which could perhaps be considered as modified spir-
alian, but the planes of the cleavage have not been
related to the planes of the larva. The origin of the
mesoderm is uncertain, but there is no sign of mesothelia or coelomic sacs. The fully formed cyphonautes
is laterally compressed with a pair of shells; it swims
with the corona, a ring of multiciliate cells with separate cilia situated along the lower edge of the shells,
surrounding a concave ‘‘ventral side’’ or vestibule.
The corona could perhaps be interpreted as a modified
prototroch; its situation and normal direction of beat
corresponds to that of a trochophore, but the cilia are
not compound and the direction of the beat can be
reversed, a feature which is apparently not known
from bands of compound cilia in spiralians (Nielsen,
1987). The vestibule is divided into a larger, anterior
inhalant chamber and a smaller, posterior exhalant
chamber by a U-shaped ciliated ridge, which carries
three rows of cilia: Lateral cilia at the lateroposterior
side of the ridge create a water current across the ridge
from the anterior to the posterior chamber; laterofrontal cilia apparently function as a mechanical filter
which intercepts the particles carried by the water flow
and in some unknown way transfers them to frontal
cilia at the anterior side of the ridge; the particles are
then in some way transported to the mouth (Strathmann and McEdward, 1986). This filter-feeding structure resembles one side of the tentacle of the adult (see
below). The apical organ is of the protostome type
with nerves and muscles leading to the prototroch and
a pair of serotonergic cells (Stricker et al., 1988a; HaySchmidt, 2000; Fig. 3). A pair of ciliated tubes have
been observed in each side of the larval body (Stricker
et al., 1988b); they could possibly be derived protonephridia, but more detailed studies are needed.
Settling and metamorphosis show much variation.
The cyphonautes larva settles with an everted adhesive
688
CLAUS NIELSEN
sac which develops into the epithelium of the underside of the ancestrula, whereas the upper epithelium
derives from the ectoderm carrying the shells. Other
types, such as Bowerbankia and Tanganella (Reed,
1991) have metamorphoses resembling that of the colonial entoprocts, with a glandular adhesive sac secreting the adhesive which glues the ancestrula to the
substratum after retraction of the hyposphere. Larval
organs such as apical organ and gut degenerate, the
first polypide is formed from a blastema of varying
origin (Zimmer, 1997), and further zooids in the colony develop through budding. This makes it impossible to infer a dorsoventral orientation of any zooid in
a colony. In the zooids, the mesoderm becomes organized as a coelomic epithelium surrounding a large
body compartment and a smaller compartment surrounding the mouth and sending canals into the tentacles, but the two compartments are in open connection in an area behind the mouth (Nielsen, 2000). This
origin and adult organization of the body cavity bears
no resemblance to the archimery of the deuterostomes,
including phoronids and brachiopods. The zooids have
no nephridia.
The ciliary bands show some variation between the
main groups, but particle capture by the ‘‘ciliary sieving method’’ has been observed in cyclostomes and
gymnolaemates. Cyclostomes have the most simple
tentacles with only lateral and laterofrontal cilia. The
lateral cilia create a water current towards the mouth
and out of the tentacular funnel between the tentacles,
and particles are strained from the water by the filter
formed by the stiff laterofrontal cilia. The drag on the
captured particle elicits a tentacle flick, which pushes
the particle to the central current carrying the particle
to the mouth (Nielsen and Riisgård, 1998). Gymnolaemates have tentacles with lateral, laterofrontal and
frontal ciliary bands; they use the same ciliary sieving
method as the cyclostomes, but have a more varied
behavioural repertoire (Riisgård and Manrı́quez,
1997). The phylactolaemates are in need of further
study. The ciliary sieving method of the ectoprocts
(gymnolaemates and stenolaemates) seems to be
unique in the animal kingdom.
Neither ontogeny nor adult structure of ectoprocts
shows any specific similarities (synapomorphies) with
phoronids and brachiopods, so the traditional classification of these three phyla as ‘‘lophophorates’’ finds
no support in morphology, and it is not supported by
molecular analyses either.
PHORONIDA AND BRACHIOPODA
Phoronids and brachiopods are undoubtedly closely
related. As mentioned above, the two phyla are regarded as deuterostomes by some morphologists,
whereas most molecular biologists regard them as protostomes.
The two phyla are usually regarded as sister groups
when morphological data are analysed (e.g., Carlson,
1995; Giribet et al., 2000; Nielsen, 2001), but many
molecular analyses resolve the phylogeny with pho-
ronids as an ingroup of the brachiopods, grouping variously with Craniida, Articulata and ‘‘Inarticulata’’
(Cohen and Gawthrop, 1997; Zrzavý et al., 1998; Giribet et al., 2000); this finds no support in morphology.
Brachiopods have a number of characters which are
not shared with the phoronids and which must be regarded as autapomorphies: Two shells, a brachial and
a pedicle valve, secreted by characteristic mantle folds,
which are extensions of the metasome and contain metacoelomic mantle canals; rows of setae, each secreted
by one cell, along the mantle edges; a short ventral
side, as shown by the ontogeny (Nielsen, 1991); and
two coelomic systems in the lophophore, a large brachial canal which is restricted to the base of the lophophore and a small brachial canal which sends a canal
into each tentacle and which represents the mesocoel
(at least in Neocrania, as demonstrated by its ontogeny, see Nielsen, 1991). On the contrary, phoronids
lack mantle folds with setae and valves, have a short
dorsal side (as shown by their ontogeny), and have
only one (mesosomal) cavity in the lophophore.
On the other hand, two characters indicate a sistergroup relationship of the two phyla. Their planktotrophic larvae have long, ciliated tentacles similar in
structure and function to those of the adults and forming a postoral horseshoe which is almost closed near
the apical organ in the area where new tentacles develop; these tentacles directly become the juvenile tentacles at metamorphosis in most species. The adults
have one (or two) pair(s) of metanephridia with a large
ciliated funnel; these also serve as gonoducts. These
characters are not seen in the Neorenalia (5Deuterostomia sensu stricto), although this can of course not
be stated categorically for the larval tentacles, because
all pterobranchs studied so far have direct development.
A whole series of characters distinguish the Deuterostomia (sensu lato, i.e., including phoronids and brachiopods) from the Protostomia (Nielsen, 2001).
The first two cleavages are generally median and
transverse, whereas they form a cross dividing the embryo into right, anteroventral, left, and posterodorsal
cells in most spiralians (Fig. 2). Among neorenalians,
only few exceptions are known, the best example being the sea urchin Strongylocentrotus (Davidson et al.,
1998). Phoronids have a somewhat labile pattern, but
the first cleavage is transverse and the second one median in most of the embryos (Freeman, 1991). Brachiopods show considerable variation: Terebratalia
and Neocrania show no fixed relationship between
early cleavage planes and adult body symmetry (Freeman, 1993, 2000), whereas in Glottidia and Discinisca, the first cleavage is median in almost all embryos
(Freeman, 1995, 1999). The third cleavage separates
apical and blastoporal regions in all species.
Regulative powers are generally considerable in
deuterostome embryos and very limited in protostomes, which are generally incapable of regulating,
with a few being able to regulate at the 2-cell stage.
Phoronid embryos are generally able to regulate when
ENTOPROCTA, ECTOPROCTA, PHORONIDA,
TABLE 1.
AND
BRACHIOPODA
689
The occurrence of phylogenetically important characters among bilaterian phyla: v character present (based on Nielsen, 2001).*
Sipuncula
Mollusca
Annelida
Onychophora
Arthropoda
Tardigrada
Entoprocta
Ectoprocta
Platyhelminthes
Nemertini
Rotifera
Gnathostomulida
Chaetognatha
CYCLONEURALIA
Phoronida
Brachiopoda
Pterobranchia
Echinodermata
Enteropneusta
CHORDATA
Downstreamcollecting
ciliary bands
Spiral cleavage
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2-3 apical
serotonergic cells
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Upstreamcollecting
ciliary bands
Archimery
Many apical
serotonergic
cells
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* Ciliary bands of both larvae and adults are included. Supraphyletic taxa in capital letters. The four phyla discussed here are underlined.
1 Ectoprocts have ciliary sieving bands (see the text).
2 Rotifer and chaetognath cleavage can possibly be interpreted as spiral (see Nielsen, 2001).
bisected along the primary axis between the 2-cell
stage and the gastrula stage; apical halves of 8-cell to
late blastula stages develop into ciliated spheres,
whereas the blastoporal halves develop almost normally (Freeman, 1991). Studies of the brachiopods
Terebratalia, Neocrania, Glottidia, and Discinisca
(Freeman, 1993, 1995, 1999, 2000) have demonstrated
some variations, but the general pattern is that isolated
blastomeres of the 2-cell stages and halves of the 4cell stage show complete regulation. Apical halves of
blastulae develop into ciliated vesicles, whereas the
blastoporal halves developed into miniature larvae
with small apical lobes. Experiments with halving
blastulae along the primary axis showed that the bilaterality becomes established during this stage and
that the power of regeneration becomes lost. The regulative powers of phoronids and brachiopods resemble
those of the sea urchins (Hörstadius, 1939) in very
many details.
The mesoderm of protostomes and deuterostomes
typically originates from different sources, with protostomes having mesoderm developing from the blastopore lip/4d-cell (and ectomesoderm) whereas deuterostomes have the mesoderm originating from the
archenteron (in some cases in the shape of mesodermal
pouches, i.e., by enterocoely, but this is not essential).
Mesoderm formation is not well known in phoronids,
but Zimmer (1980, 1991), Emig (1977) and Herrmann
(1986) agree that mesoderm proliferates from the dorsal and lateral sides of the anterior archenteron and
forms the protocoel; meso- and metacoel become organized at later stages from cells of uncertain origin.
This is very similar to the formation of the mesoder-
mal sacs in the enteropneust Ptychodera flava (Peterson et al., 1999). In brachiopods, the mesoderm develops from the archenteron, through differentiation of
particular regions of the archenteron in Crania, Discinisca, Glottidia, and articulates (Nielsen, 1991; Freeman, 1995, 1999; Long and Stricker, 1991), although
Freeman (2000) described a quite deviant type of differentiation in Crania. Thus, the origin of the mesoderm is clearly of the deuterostome type in phoronids
and brachiopods.
The larval apical organ contains a kidney-shaped
group of many serotonergic cells in Phoronis and an
elongate group on the median tentacle of the brachiopods Glottidia and Lingula, whereas the protostome
larvae have only 2–3 serotonergic cells (Hay-Schmidt,
1990, 1992; Fig. 3).
Archimery, the organization of the body in three
regions each with characteristic coelomic compartments, is clearly recognized during ontogeny and in
the full-grown larvae of Crania (Nielsen, 1991), but
the protocoel is not well developed in phoronids and
has not been identified with certainty in adult brachiopods. However, both meso- and metacoels have been
followed from the larval stages through metamorphosis to the adults, so their identity cannot be doubted.
The ciliary bands on the phoronid and brachiopod
tentacles are upstream-collecting bands with separate
cilia on monociliate cells just like those of larvae or
adults of pterobranchs, echinoderms and enteropneusts
(Nielsen, 1987). The particle-collecting method is generally believed to involve a reversal of the ciliary beat
(Strathmann, 1973), but further investigations are
needed.
690
CLAUS NIELSEN
All these characters indicate that phoronids and brachiopods belong to the deuterostome line. I cannot
identify any unequivocal protostome character, but
blastopore fate and protonephridia of phoronids are
among the characters which could indicate protostomian affinities (or be ancestral).
DISCUSSION
The above summaries have concentrated on morphological characters, and it appears that entoprocts
and ectoprocts are protostomes (and possibly closely
related), whereas phoronids and brachiopods share a
number of key characters with the other deuterostomes
(Figs. 2–3; Table 1).
Molecular studies support the monophyly of Phoronida 1 Brachiopoda but almost invariably place
them within the ‘‘Lophotrochozoa,’’ which in most
studies comprising many species appear as a complete
hotchpotch of ciliated protostomes (Winnepenninckx
et al., 1998; Halanych, 1998; Giribet et al., 2000).
However, it should be stressed that whereas the Deuterostomia sensu stricto is recognized as a monophyletic group with a number of well defined phyla in a
rather constant phylogenetic pattern, the protostomes
do not show a clear or consistent pattern. Analyses
including a variety of annelids and molluscs do not
show Annelida and Mollusca as monophyletic (e.g.,
Giribet et al., 2000; Peterson and Eernisse, 2001), and
the Ectoprocta are usually polyphyletic too. To me this
indicates that the 18S rDNA molecule does not contain
enough information to resolve the old speciation
events at the base of the Bilateria, and that only the
branch leading to Deuterostomia sensu stricto has been
isolated (i.e., given off no surviving groups) for so
long that it can be recognized in the analyses.
Morphologically it is rather easy to define both the
Deuterostomia sensu lato and the Deuterostomia sensu
stricto (5Neorenalia), whereas I find it impossible to
identify any synapomorphies of a Protostomia sensu
lato, i.e., including phoronids and brachiopods; all
characters that can be listed are symplesiomorphies,
viz. deuterostome synapomorphies which are absent,
and this supports the impression of a paraphyletic
‘‘Protostomia sensu lato.’’ The only logical position of
the Protostomia-Deuterostomia split therefore places
Phoronida 1 Brachiopoda in the Deuterostomia (sensu
lato).
Although no firm conclusion can be drawn about
the phylogenetic position of the ectoprocts, it can be
stated that there is no indication from morphology or
molecules in favour of uniting them with phoronids
and brachiopods. In consequence, the word Lophophorata must be removed from the phylogenetic vocabulary, just as the word Vermes was abandoned several decades ago.
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