© 2003 by The Society for Integrative and Comparative Biology
The Significance of Muscle Cells for the Origin of Mesoderm in Bilateria1
1 Institute of Zoology and Limnology, University of Innsbruck, Technikerstraße 25, A-6020 Innsbruck, Austria
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SYNOPSIS |
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 SYNOPSIS INTRODUCTIONTHE MYOCYTE AND THE...MESODERMAL MUSCULATURE...ORIGIN OF BODY WALL...ENDO- AND ECTODERMAL MYOCYTES...SERIAL ARRANGEMENT OF MESODERMAL...FUTURE STUDIESReferences |
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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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INTRODUCTION |
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SYNOPSISINTRODUCTIONTHE MYOCYTE AND THE...MESODERMAL MUSCULATURE...ORIGIN OF BODY WALL...ENDO- AND ECTODERMAL MYOCYTES...SERIAL ARRANGEMENT OF MESODERMAL...FUTURE STUDIESReferences |
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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 evolution 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).
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THE MYOCYTE AND THE ORIGINAL FUNCTION OF MESODERMAL TISSUES |
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SYNOPSISINTRODUCTIONTHE MYOCYTE AND THE...MESODERMAL MUSCULATURE...ORIGIN OF BODY WALL...ENDO- AND ECTODERMAL MYOCYTES...SERIAL ARRANGEMENT OF MESODERMAL...FUTURE STUDIESReferences |
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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
; Salvini-Plawen 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.
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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 parenchyma 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.
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MESODERMAL MUSCULATURE—EPITHELIAL OR MESENCHYMAL ORIGIN |
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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 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).
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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).
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ORIGIN OF BODY WALL MUSCULATURE OF VERMIFORM BILATERIANS FROM DIPLOBLASTIC CONDITIONS |
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SYNOPSISINTRODUCTIONTHE MYOCYTE AND THE...MESODERMAL MUSCULATURE...ORIGIN OF BODY WALL...ENDO- AND ECTODERMAL MYOCYTES...SERIAL ARRANGEMENT OF MESODERMAL...FUTURE STUDIESReferences |
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We (Rieger and Ladurner, 2001
) have presented two models for the origin of the body wall musculature in 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 Müller's 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.
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ENDO- AND ECTODERMAL MYOCYTES AND MESODERMAL "STEM CELLS" IN BASAL BILATERIA |
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SYNOPSISINTRODUCTIONTHE MYOCYTE AND THE...MESODERMAL MUSCULATURE...ORIGIN OF BODY WALL...ENDO- AND ECTODERMAL MYOCYTES...SERIAL ARRANGEMENT OF MESODERMAL...FUTURE STUDIESReferences |
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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 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 subpopulations 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 protosomes 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.
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SERIAL ARRANGEMENT OF MESODERMAL MUSCLE TISSUE AND SEGMENTATION |
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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 |
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SYNOPSISINTRODUCTIONTHE MYOCYTE AND THE...MESODERMAL MUSCULATURE...ORIGIN OF BODY WALL...ENDO- AND ECTODERMAL MYOCYTES...SERIAL ARRANGEMENT OF MESODERMAL...FUTURE STUDIESReferences |
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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 cytodifferentiation 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.
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ACKNOWLEDGMENTS |
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This work was supported by FWF-grant P15204 [GenBank] 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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FOOTNOTES |
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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: reinhard.rieger{at}uibk.ac.at
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