INTEGR. COMP. BIOL., 43:47–54 (2003)
The Significance of Muscle Cells for the Origin of Mesoderm in Bilateria1
REINHARD M. RIEGER2
AND
PETER LADURNER
Institute of Zoology and Limnology, University of Innsbruck, Technikerstraße 25, A-6020 Innsbruck, Austria
INTRODUCTION
The transition from diploblastic to triploblastic body
plans hinges on the origin of mesoderm. The nature
and development of mesoderm, therefore, have been
at the crux of questions of metazoan evolution for over
a hundred years (Ruppert, 1991; Nielsen, 2001). Recent studies in developmental genetics have revealed
a number of mesoderm-specific genes in a wide variety
of bilaterians, including vertebrates, insects, nematodes, echinoderms, and hemichordates (e.g., see Peterson et al., 1999; Davidson, 2001; Furlong et al.,
2001; Gross and McClay, 2001; Kumano et al., 2001;
Smith, 2001; Tagawa et al., 2001; Technau, 2001). Expression of mesodermal genes is often coupled with
axis formation in Bilateria (e.g., Holland, 2000), and
so correlation with axis determination in ancestral diploblasts is also important (e.g., Müller et al., 1999;
Spring et al., 2000; Yanze et al., 1999). It has been
concluded that the common ancestor of diploblasts and
triploblasts not only featured genes regulating myogenesis but used them also in muscle cell differentiation similar to triploblasts (Spring et al., 2002).
The nature of the original mesodermal cells in triploblasts is also emerging from studies of the cytology
and embryology of lower bilaterians. For example,
Ladurner and Rieger (2000) and Rieger and Ladurner
(2001) have shown how muscle cells arise in embryos
of acoels and other lower worms and become positioned between ecto- and endoderm. Cell-lineage studies of ctenophores (Martindale and Henry, 1999; Henry and Martindale, 2001), polyclad flatworms (Boyer
et al., 1996, 1998), nemertines (Henry and Martindale,
1998) and acoelomorph flatworms (Henry et al., 2000)
reveal important distinctions between mesodermal
cells arising from ectoderm and those from endoderm.
And studies of the arrangement of body-wall muscles
in platyhelminths (Tyler and Rieger, 1999; Tyler, 2001;
Hooge, 2001) and their embryonic development (Ladurner and Rieger, 2000) show a spectrum of function
and position that provide models for the ancestral bilaterian.
Many hypotheses on the origin of the Bilateria postulate that the ancestor was a small vermiform organism, in the millimeter or centimeter size range, that
moved by ciliary locomotion. Depending on the hypothesis, this ancestor could have been acoelomate,
pseudocoelomate or coelomate and it may have had
either direct development or a biphasic life cycle. The
biphasic life cycle would involve alternation between
a pseudocoelomate larva and a benthic adult of acoelomate protostome or of coelomate deuterostome organization (see literature in Nielsen, 2001; Rieger and
Ladurner, 2001; Collins and Valentine, 2001).
Alternative hypotheses postulate that the ancestor
was a large colonial organism, centimeters or decimeters in size. For example, Dewel (2000) has proposed that colonies similar to pennatulacean anthozoans were transformed to triploblasts by integrating
their zooids into a large, solitary, modular triploblast
with a segmented body plan (see also Collins and Valentine, 2001). Rieger (1986, 1994) proposed that colonial coelomates with microscopic zooids similar to
bryozoans gave rise to microscopic adult acoelomates
and pseudocoelomates through progenesis of the larva
and gave rise to macroscopic ancestors of solitary protostome and deuterostome coelomates from single zooids. The mesoderm played a critical role in this evo-
1 From the Symposium New Perspectives on the Origin of Metazoan Complexity presented at the Annual Meeting of the Society for
Integrative and Comparative Biology, 3–6 January 2002, at Anaheim, California.
2 E-mail: [email protected]
47
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SYNOPSIS.
Muscle tissue may have played a central role in the early evolution of mesoderm. The first
function of myocytes could have been to control swimming and gliding motion in ciliated vermiform organisms, as it still is in such present-day basal Bilateria as the Nemertodermatida. The only mesodermal cells
between epidermis and gastrodermis in Nemertodermatida are myocytes, and conceivably the myocyte was,
in fact, the original mesodermal cell type. In Nemertodermatida as well as the Acoela, myocytes are subepithelial fiber-type muscle cells and appear to originate from the gastrodermal epithelium by emigration
of single cells. Other mesodermal cells in the acoels are the peripheral parenchyma (connective tissue) and
tunica cells of the gonads, and these also arise from the gastrodermis. Musculature in many of the coelomate
protostomes and deuterostomes, on the other hand, is in the form of epitheliomuscular (myoepithelial) cells,
and this cell type may also have been an early form of the mesodermal myocyte. The mesodermal bands in
the small annelid Polygordius and in juvenile enteropneusts have cells intermediate between mesenchymal
and epithelial in their histological organization as they develop into myoepithelia. If acoelomates were derived from coelomates by progenesis, then the fiber-type muscles of acoelomates could be products of foreshortened differentiation of such tissue. The precise serial patterning of circular muscle cells along the
anterior-posterior axis during embryonic development in the acoel Convoluta pulchra provides a model for
early steps in the gradual evolution of segmentation from iterated organ systems.
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R. M. RIEGER
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lution by forming the coelom for protruding and retracting the zooids.
Yet another hypothesis for the origin of the mesoderm from the subumbrellar epithelium of a hydrozoan
medusa buds has been recently advanced (Boero et al.,
1998).
THE MYOCYTE AND THE ORIGINAL FUNCTION OF
MESODERMAL TISSUES
Why was it advantageous to the ancestral bilaterian
to develop mesoderm? In the case of a small (mm–
cm) vermiform ancestor, it could be to control the direction of ciliary locomotion and, at the same time, to
provide flexible skeletal support (Clark, 1964; SalviniPlawen and Splechtna, 1979, p. 18). Such improvements could have been made by muscles. They would
allow more accurate changes in direction of movement
and contractions and extensions of the body and so
would have been useful for improving prey capture,
defence, or more complex reproductive behaviour.
This, in turn, would have been a factor in the evolution
of cephalization.
Small free-living platyhelminths (acoelomorphs, catenulids, macrostomids) illustrate this function of the
body-wall musculature. These animals accomplish forward motion with the epidermal cilia and use their
muscles for turning and steering movements, thus directing the currents created by the virtually constantly
moving cilia (Tyler and Rieger, 1999).
It is significant that the only mesodermal cells between the gastrodermal and epidermal epithelium in
the acoelomorph nemertodermatids like Flagellophora
apelti are myocytes (Fig. 1; see also Smith and Tyler,
1985; Rieger et al., 1991). Cell-lineage studies in the
closely related Acoela have established that their entire
muscle tissue (as well as their peripheral parenchyma)
is derived solely from endodermal cell lines (Henry et
al., 2000); no ectomesodermal (ectomesenchymal) tissues seem to exist.
Other mesodermal tissues, such as connective tissue,
likely originated after muscle. Such appears to be the
case in the acoels (Fig. 1) where the peripheral paren-
chyma develops from endodermal sources after the
formation of mesodermal musculature (Smith and Tyler, 1985). The same may apply to the mesodermal
connective tissue in other bilaterians.
Germ cells in the ancestral bilaterian probably resided in the gastrodermis. The nemertodermatid Flagellophora apelti illustrates this, having modified gut
cells that form specialized tunica cells around male
and female gametes (Rieger et al., 1991). These cells,
usually seen as being mesodermal, apparently represent another cell line originating from endoderm.
Other functions of tissues and organs derived from
the mesoderm in bilaterians—for example, excretion
and osmoregulation, or the hydrostat function of the
coelom—also must have influenced early evolution of
mesodermal tissues.
MESODERMAL MUSCULATURE—EPITHELIAL OR
MESENCHYMAL ORIGIN
Basically, mesoderm forms either by direct transformation of portions of the epithelium of the archenteron into the mesothelial mesoderm or by immigration of individual cells from the endodermal blastoporal region or other regions of the archenteron (Fioroni, 1992; Gilbert and Raunio, 1997).
In the case of mesothelial mesoderm, the forerunners of the mesoderm would be gastral pockets in an
organism at the coelenterate level of organization (Rieger, 1986; Balavoine, 1998; Tyler, 2001). By this concept, the mesothelium was originally organized as a
simple or stratified myoepithelium with epitheliomuscular cells (Rieger, 1986; Rieger and Lombardi, 1987;
Ruppert and Barnes, 1994; Tyler, 2001). Ultrastructural investigations of somatic and visceral mesoderm of
many adult coelomate bilaterians—particularly annelids, chaetognaths, echinoderms, and cephalochordates—point to such a primary mesothelial nature of
the mesoderm: A continuous histological sequence has
been discovered in annelids and echinoderms, from
simple myoepithelial organization with epitheliomuscular cells to a subperitoneal musculature of fiber-type
muscle cells covered by a non-muscular squamous
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FIG. 1. Diagrams of cross-sections through representatives of the Acoelomorpha illustrating derivation of mesodermal connective tissue from
gastrodermis. A. Hypothetical ancestor to the Acoelomorpha, with epithelial gastrodermis of ciliated phagocytes and digestive gland cells. B.
Nemertodermatid, showing obliteration of gut lumen; the gastrodermis is still epithelial. C. The acoel Paratomella rubra, showing breakdown
of the gastrodermal epithelium into parenchymal digestive cells around a gut lumen. D. The acoel Diopisthoporus or Hesiolicium, showing
separation of a layer of peripheral parenchymal cells (mesodermal connective tissue) and a central, multinucleated digestive parenchyma.
Mesodermal body-wall musculature indicated as a gray layer between epidermis and gastrodermis; actually, the body wall musculature is an
open meshwork of muscle fibers that allows direct contact of epidermal and gastrodermal cells. (After Smith and Tyler, 1985, modified.)
EVOLUTION
ORIGIN OF BODY WALL MUSCULATURE OF VERMIFORM
BILATERIANS FROM DIPLOBLASTIC CONDITIONS
We (Rieger and Ladurner, 2001) have presented two
models for the origin of the body wall musculature in
MESODERM
49
vermiform bilaterians. The cnidarian model portrays
the outer circular muscle layer as originating from the
ectoderm (ectomesenchymal). In later evolutionary
steps, these muscles are gradually replaced by muscle
tissue derived from endomesoderm. This model rests
on the observation that the body of cnidarian polyps
generally has epidermal epitheliomuscular cells with
longitudinal orientation of myofilaments and a gastrodermal system of epitheliomuscular cells with primarily circular myofilament arrangements. Among bilaterians, the Müllers larva of the polyclad Hoploplana
inquilina, for example, also shows a dual origin: outer
circular muscles are derived from the ectodermal lineage of the 2b micromeres; inner longitudinal muscles
are derived from endoderm (Reiter et al., 1996; Boyer
et al., 1998). We point out that this may be solely a
larval feature; data on the origin of the circular musculature in adult polyclads are lacking. At least for
certain sipunculids, however, circular muscles are reportedly derived from the ectomesenchyme (Rice,
1967).
Our second model (ctenophore model) portrays
body-wall musculature as having solely an endodermal
origin. The organization and development of musculature in ctenophores and acoelomorphs supports this
model (Martindale and Henry, 1999; Henry et al.,
2000). However, the body-wall muscle system of pelagic ctenophores is less complex than that of vermiform Bilateria. Without more intermediate stages it is,
therefore, difficult to see how it can be ancestral to the
body wall of acoelomorphs and other bilaterians. Benthic ctenophores such as Coeloplana would be interesting to study to resolve this question.
Another puzzle in ctenophore musculature is the parietal musculature. Ultrastructure clearly identifies parietal muscle cells to be intraepithelial in the epidermis
and pharyngeal epithelium (Hernandez-Nicaise, 1991).
They do appear to be regular myoepithelial cells as
defined by Rieger and Lombardi (1987). Muscle tissue
of Ctenophora otherwise is subepithelial and consists
of complex fiber-type muscle cells (Hernandez-Nicaise, 1991). A better understanding of the origin and
three-dimensional organization of this epithelial musculature is needed to clarify its relation to cnidarian
musculature.
ENDO- AND ECTODERMAL MYOCYTES AND
MESODERMAL ‘‘STEM CELLS’’ IN BASAL BILATERIA
While circular and longitudinal muscles arise from
different cell lines (ecto- and endodermal, respectively) in spiralians like the polyclad Hoploplana inquilina
and sipunculans, as mentioned above, muscles in other
groups of lower bilaterians may have other origins.
Several ecto- and endodermal cell lines contribute to
the musculature of the nematode Caenorhabditis elegans, for example (Sulston et al., 1983), but only endodermal cell lines provide muscle cells in the acoel
Neochildia fusca (see Henry et al., 2000).
Just which of these different developmental strategies may be ancestral is difficult to decide, although
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peritoneum (Rieger, 1986; Rieger and Lombardi, 1987;
Fransen, 1988; Stauber, 1993; Bartolomaeus, 1994).
The plesiomorphic nature of myoepithelial organization of the body wall musculature is evident in adult
annelids, echiurans, and sipunculids (Bartolomaeus,
1994). From these data an epithelial organization of
the mesodermal musculature can be deduced as being
the ancestral histological organization for all Bilateria,
fiber-type subepithelial myocytes as being a derived
condition. The same process of epithelial muscle cells
migrating to a subepithelial position is already well
known among certain cnidarians (Werner, 1984).
On the other hand, immigration of individual cells
(or small groups of cells) can conceivably lead directly
to a mesodermal muscle grid of fiber-type muscles.
This mode of establishing the mesodermal musculature
likely has occurred in small vermiform organisms
(Rieger and Ladurner, 2001). Such early microscopic
bilaterians were not necessarily direct developers; they
could equally well have been derived by progenesis
from ciliated acoelomate or pseudocoelomate larvae of
larger coelomates.
Schizocoelous mesoderm formation in coelomate
spiralians also makes use of individual cell immigration during its early phase. However, mesodermal cells
form bands soon thereafter; in several cases, such as
in Owenia (Fig. 2) or in Magelona, these mesodermal
bands have an epithelial organization already very early on (Rieger, 1986; Turbeville, 1986). An intermediate epithelial/mesenchymal tissue organization of the
mesodermal bands exists, e.g., in Polygordius (Fig. 3).
From such an intermediate configuration, subepithelial, fiber-type muscle cells in an acoelomate tissue
grade, just as occurs in small interstitial annelids (see
literature in Fransen, 1988), could arise in microscopic
adult organisms by progenesis (Rieger, 1986).
By contrast with the Annelida, the Mollusca have
muscle tissue (consisting of fiber-type muscle cells)
developing independently of the mesothelial lining of
the gonocoel and pericardium (Salvini-Plawen and
Bartolomaeus, 1995). Ancestral molluscs may have
been vermiform organisms similar to larger flatworms.
A body-wall musculature with fiber type muscle cells
and serially arranged dorso-ventral muscles must have
been early features of their musculature (Wanninger
and Haszprunar, 2002).
Muscle is known to arise from both ectodermal (ectomesenchyme) and endodermal (endomesoderm)
sources in the Spiralia (see literature in Boyer et al.,
1998; Gilbert and Raunio, 1997; Henry and Martindale, 1998). The exact contribution of ectomesenchymal muscle to the muscle tissue of adults is not resolved in many cases, however. In general, most of the
mesodermal tissues in adults are endomesodermal
(Henry and Martindale, 1999, p. 258).
OF
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P. LADURNER
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FIG. 2. Ultrastructure of early mesodermal bands in a young mitraria larva of Owenia fusiformis in sagittal section showing their epithelial
nature. A. Diagram of larva to show location of sections (modified from Wilson [1932]). B. Origin of mesodermal bands in anal region
between gut and worm-trunk invagination. Note individual cells (*) near origin of mesodermal band and series of three mesodermal cells (1,
2, 3) forming part of a small coelomic cavity. Anus at lower left, epidermis of worm-trunk invagination to right. Scale bar 5 mm. C. Enlargement
of the numbered mesodermal cells from B. Lumen of the coelom is only a narrow space between the three cells (large arrowheads), and they
are joined by zonulae adhaerentes (small arrowheads). Every coelomic sac has its own basal lamina (inset), separate from the basal laminae
of the epidermal trunk invagination and gut epithelium. Scale bar 2.5 mm.
EVOLUTION
OF
MESODERM
51
we think that an endodermal origin is the most likely
candidate given the nature of other mesodermal tissues
in the key model acoelomorphs.
Also critical for understanding muscle differentiation is the role stem cells play in growth, maintenance,
and regeneration of muscles in the adult organism. The
unique postembryonic stem cells of platyhelminths,
known as neoblasts, presumably arise from embryonic
stem cells, and they appear to be totipotent, capable of
giving rise to any differentiated cell type in the adult,
although it is still unclear whether specific subpopu-
lations are responsible for different cell types (Ladurner et al., 2000).
The neoblast system is best characterized in planarians and macrostomids (Newmark and Sanchez-Alvarado, 2000; Ladurner et al., 2000). Modern labeling
techniques have revealed the neoblast system also in
acoels (Gschwentner et al., 2001) and in the nemertodermadid Sterreria psammicola (P.L., unpublished
data). Molecular studies now suggest that nemertodermatids and acoels occupy the basal most phylogenetic
position in the Bilateria, prior to the split into proto-
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FIG. 3. Mesodermal bands showing both epithelial and mesenchymal characters in young larva of Polygordius sp. I. A. Overview of larva
in Epon-Araldite block before serial sectioning. B. Diagram of cross section through caudal-most portion of the developing young worm with
two ventrolateral mesodermal bands. C. Series of 250 ultrathin sections through the caudal end of the mesodermal band projected onto a
diagram of a section in the middle of the series. Cells have an intracellular, rudimentary, diplosomal cilium and only one point of contact with
the basal matrix (epithelial characters). Contact between cell Nr. 6 and basal matrix lies in front of the section (arrows). A lumen is lacking;
only spot desmosomes are present (mesenchymal characters). Numbers next to rudimentary cilia with Golgi complexes are those of sections
in which they were found. Rudimentary cilia in cells Nr. 1, 3, 5, 7, 8 not shown because they were close (1, 8) or beyond sectioned area.
Modified after Rieger (1986; English translation at http://www.umesci.maine.edu/biology/labs/origin/).
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somes and deuterostomes (Jondelius et al., 2002).
Should this position be corroborated, the neoblast system would appear as the basal most mechanism in the
Bilateria for postembryonic cell renewal also of mesodermal cell lines including the myocytes. Because
neoblasts are likely derived from embryonic stem
cells, a stem cell system may be even the original
mode of mesoderm formation in the embryo.
By labeling cells in S-phase with nuclear markers,
stem cells can be identified (Fig. 4A) and their fates
in differentiation of muscle cells can be monitored
through secondary labeling with monoclonal antibodies for specific muscle components (Fig. 4B, C). Antibodies for other mesodermal cell types could also be
fruitfully applied.
SERIAL ARRANGEMENT OF MESODERMAL MUSCLE
TISSUE AND SEGMENTATION
Several phylogentic studies have proposed that the
ancestor to all Bilateria was segmented, especially because of similarities in the genetic mechanisms specifying segmentation in insects and vertebrates (see literature in Dewel [2000] and Budd [2001]). However,
if segmentation were derived gradually from iterated
organ systems, as suggested by Budd (2001), the bilaterian stem group need not have been fully segmented. Such iteration appears in circular muscles of
basal bilaterians, for example Convoluta pulchra. During differentiation of the body-wall musculature in this
acoelomorph, the circular fibers distinctly appear before the longitudinal fibers, and they show precise serial patterning of rings, each formed by several muscle
cells, oriented perpendicular to the anterior-posterior
axis (Ladurner and Rieger, 2000). Such a process
could have been involved in early stages of the evolution of segmentation; that is, it could be under control of genes comparable to those acting early on for
segment formation in metameric animals.
FUTURE STUDIES
Further understanding of the evolution of mesoderm
in the Bilateria will depend on studies of developmental genetics, cell differentiation, and embryonic cell
lineage. In particular, we emphasize the need for these
points to be addressed:
In conjunction with studies on mesodermal genes,
comparative histological investigations of the developing body-wall musculature of various vermiform bilaterians are needed to better understand the variability
of this development. The lower metazoan groups Gastrotricha and Gnathostomulida, but also Onychophora,
Annelida, Mollusca, and Enteropneusta would be the
most relevant taxa.
Similarly, comparative studies on myocyte cytodif-
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FIG. 4. Components of body-wall musculature and underlying stem-cell system producing it in the microturbellarian Macrostomum sp. (A)
BrdU-labeled S-phase stem cells (neoblasts) in the lateral midbody region, left side, within the mesodermal tissue compartment close to
musculature. (B) Same body region stained with monoclonal antibody against entire body wall musculature; note thin outer circular fibers,
sporadic diagonal fibers, and thick inner longitudinal fibers. (C) Same body region stained with monoclonal antibody for longitudinal muscle
fibers only. Scale bar 30 mm.
EVOLUTION
ferentiation and its genetic control in non-vermiform
taxa, including basal deuterostomes, lophotrochozoans, and ecdysozoans need to be carried out.
The contribution of ectomesodermal musculature to
the total mesodermal musculature especially in the
spiralians warrants further investigation.
ACKNOWLEDGMENTS
This work was supported by FWF-grant P15204 to
R. Rieger, P. Ladurner, Innsbruck and R. Peter, Salzburg. We thank Gunde Rieger and Seth Tyler for critical comments. P.L. is supported by an APART-fellowship (APART Nr. 10841).
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