- Open Access
Comparative larval myogenesis and adult myoanatomy of the rhynchonelliform (articulate) brachiopods Argyrotheca cordata, A. cistellula, and Terebratalia transversa
Frontiers in Zoology volume 6, Article number: 3 (2009)
Despite significant methodological progress, Brachiopoda remains one of the lophotrochozoan phyla for which no recent ontogenetic data employing modern methodologies such as fluorescence labelling and confocal microscopy are available. This is particularly astonishing given the ongoing controversy concerning its phylogenetic position. In order to contribute new morphogenetic data for phylogenetic and evolutionary inferences, we describe herein the ontogeny and myoanatomy of larvae and adults of the rhynchonelliform brachiopods Argyrotheca cordata, A. cistellula, and Terebratalia transversa using fluorescence F-actin labelling combined with confocal laserscanning microscopy.
Fully grown larvae of A. cordata and T. transversa consist of three distinct body regions, namely an apical lobe, a mantle lobe with four bundles of setae, and a pedicle lobe. Myogenesis is very similar in these two species. The first anlagen of the musculature develop in the pedicle lobe, followed by setae muscles and the mantle lobe musculature. Late-stage larvae show a network of strong pedicle muscles, central mantle muscles, longitudinal muscles running from the mantle to the pedicle lobe, setae pouch muscles, setae muscles, a U-shaped muscle, serial mantle muscles, and apical longitudinal as well as apical transversal muscles. Fully developed A. cistellula larvae differ from the former species in that they have only two visible body lobes and lack setae. Nevertheless, we found corresponding muscle systems to all muscles present in the former two species, except for the musculature associated with the setae, in larvae of A. cistellula. With our survey of the adult myoanatomy of A. cordata and A. cistellula and the juvenile muscular architecture of T. transversa we confirm the presence of adductors, diductors, dorsal and ventral pedicle adjustors, mantle margin muscles, a distinct musculature of the intestine, and striated muscle fibres in the tentacles for all three species.
Our data indicate that larvae of rhynchonelliform brachiopods share a common muscular bodyplan and are thus derived from a common ancestral larval type. Comparison of the muscular phenotype of rhynchonelliform larvae to that of the other two lophophorate phyla, Phoronida and Ectoprocta, does not indicate homology of individual larval muscles. This may be due to an early evolutionary split of the ontogenetic pathways of Brachiopoda, Phoronida, and Ectoprocta that gave rise to the morphological diversity of these phyla.
Brachiopoda is a small lophophorate phylum with a prominent fossil record since the Lower Cambrium . More than 12.000 fossil and approximately 380 recent species are known to date [2, 3]. The phylum is commonly divided into three taxa, the articulate Rhynchonelliformea and the two inarticulate clades Craniiformea and Linguliformea , and has traditionally been grouped together with Phoronida and Ectoprocta into the superphylum Lophophorata. However, this classification has recently been challenged by paleontological and molecular datasets. While some analyses employing morphological data assign Brachiopoda to Deuterostomia [e.g., [5, 6]], recent molecular data either propose sistergroup relationships to various spiralian phyla including Mollusca, Annelida, and Nemertea [7–11], or support the notion that Phoronida are an ingroup of Brachiopoda [12, 13].
Apart from some mainly gross morphological studies [14–21], detailed data using modern techniques such as fluorescence labelling and confocal laserscanning microscopy are not yet available. This is especially true with respect to the development of the musculature, despite the fact that myo-anatomical features may provide useful characters for reconstructing phylogenetic relationships [22, 23]. Recently, some data on larval muscle development for the proposed brachiopod sister groups Phoronida and Ectoprocta have become available [24–28]. Accordingly, larval myogenesis in Brachiopoda constitutes an important gap of knowledge in comparative developmental studies on Lophophorata. With the first thorough, comparative account of brachiopod larval myogenesis provided herein for the rhynchonelliform species Argyrotheca cordata (Risso, 1826), Argyrotheca cistellula (Searles-Wood, 1841), and Terebratalia transversa (Sowerby, 1846), we aim at stimulating the discussion concerning lophophorate bodyplan evolution, phylogeny, and development. Furthermore, we contribute to questions concerning the muscular ground pattern of rhynchonelliform brachiopod larvae. We supplement our ontogenetic data with a detailed description of the adult muscle systems of all three species.
Embryonic and larval development of Argyrotheca cordata
Embryos and larvae of Argyrotheca cordata are brooded by the mother animal and are released as late-stage larvae competent to undergo metamorphosis. Accordingly, larval development is entirely lecithotrophic. After cleavage and gastrulation (Fig. 1A), a three-lobed larva is established, which comprises an anterior apical lobe, a mantle lobe in the mid-body region, and a posterior pedicle lobe (Fig. 1B–F). In very early three-lobed stages, the blastopore is visible at the base of the apical lobe (Fig. 1B). This larval mouth closes during subsequent larval development (Fig. 1D).
The apical lobe is ciliated and bears, in early three lobed stages, an apical tuft which is lost in later stages (Fig. 1B, D). When the three lobes are fully established, four bundles of larval setae are formed at the posterior margin of the mantle lobe (Fig. 1E). Finally, in larvae competent to undergo metamorphosis, the anlage of the pedicle becomes visible as a distinct primordial hump at the posterior pole of the pedicle lobe (Fig. 1F).
Myogenesis and adult myoanatomy of Argyrotheca cordata
The larvae investigated were about 230–270 μm long and 210–240 μm wide. The first F-actin-positive signal is visible as distinct spots in the area that later forms the mantle lobe (Fig. 2A). These distinct spots are F-actin-positive microvilli which are situated in the lower part of the setal sacs where the setae are formed [cf. ]. The strong fluorescence signal of the microvilli disappears once setae formation is completed, due to the increasing predominance of the larval musculature (Fig. 2D–F).
The pedicle muscles start to form in three-lobed larvae that still lack setae (Fig. 2B). In older larvae with short setae (corresponding to the stage shown in Fig. 1E), setae muscles start to develop. These run from the setal pouches in anterior direction and connect to the apical longitudinal muscles at the border between apical and mantle lobe (lateral setae muscles) or to the central mantle muscles (dorsal setae muscles), respectively (Fig. 2C). The apical longitudinal muscles extend laterally within the apical lobe and terminate anteriorly at an apical transversal muscle (Fig. 2C). At this stage, longitudinal muscles are also found within the pedicle lobe. From there, they run into the mantle lobe, where they connect to longitudinal muscles which originate at the muscle interconnection point at the border between apical and mantle lobe. The larval gut rudiment is visible as a tube in the centre of the larvae (Fig. 2C).
In fully developed larvae, setae pouch muscles are established and interconnected by a circular mantle muscle (Fig. 2D). From this circular mantle muscle emerge serial mantle muscles, which are dorsolaterally closed by the central mantle muscles. The central mantle muscles are connected to the dorsal setae muscles and to the apical longitudinal muscles at the border of the apical and the mantle lobe (Fig. 2E–F). Anteroventrally, the serial mantle muscles are enclosed by a U-shaped muscle which extends ventrally from the pedicle muscles towards the circular mantle muscle (Fig. 2D–F; see also additional file 1). The primordial hump is devoid of any musculature (Fig. 2E–F).
Adult A. cordata studied were 0.8–1.3 mm wide and 0.9–1.4 mm long. We can confirm four pairs of muscles which have been described previously . These are one pair of adductors and one pair of diductors, which attach to both the dorsal and to the ventral valve. In addition, there are two pairs of pedicle adjustors, one of which being attached to the ventral valve and the pedicle, and one being attached to the dorsal valve and the pedicle (Fig. 3A–B). In addition, we found a distinct musculature in the tentacles of the lophophore and in the digestive system. Each tentacle contains several bands of striated muscle fibers (Fig. 3D–E), while the stomach and intestine are each lined by numerous delicate ring muscles (Fig. 3C). Moreover, minute muscles are distributed along the dorsal and ventral mantle margin, which probably function as mantle retractor muscles. These mantle retractors are abundant and are oriented perpendicularly to the mantle margin that lines the shell (Fig. 3A–B).
Myogenesis and adult myoanatomy of Argyrotheca cistellula
Similar to Argyrotheca cordata, larvae of A. cistellula are lecithotrophic and are brooded by the mother animal. A. cistellula larvae lack setae and the mantle lobe encloses the pedicle lobe during development. Thus, the fully developed larvae have only two visible lobes, namely the apical and the mantle lobe. The investigated larvae were around 117–139 μm long and 78–104 μm wide. The first muscles appear in larvae with all lobes fully differentiated. These are two dorsal mantle muscles which extend dorsally from anterior to posterior in the mantle lobe (Fig. 4A). Parallel and further lateral to these dorsal mantle muscles run the early lateral mantle muscles, and the first rudiments of the serial mantle muscles arise at this stage in the mantle lobe. These develop subsequently into a network of muscles that extends dorsally and ventrally from the two lateral mantle muscles (Fig. 4A–F). These lateral mantle muscles connect to the apical longitudinal muscles at the anterior pole and to the posterior muscle ring at the posterior pole of the larvae (Fig 4B–F). During subsequent development, the ventral mantle muscles and the pedicle muscles emerge (Fig. 4C). The pedicle muscles, situated in the centre of the mantle lobe, are the most prominent muscles in fully grown larvae (Fig. 4D). They connect to the apical longitudinal muscles, which in turn are in contact with the apical transversal muscles. The latter form a muscle ring in the apical lobe (Fig. 4E–F). The musculature of fully developed larvae includes the pedicle muscles, which are connected to the apical longitudinal muscles, the ventral mantle muscles, and the dorsal mantle muscles that connect to the pedicle muscles. Furthermore, serial mantle muscles, which extend dorsally and ventrally from the lateral mantle muscles, are present. Ventrally, the serial mantle muscles terminate at the ventral mantle muscles (Fig. 4F).
Similar to the condition found in Argyrotheca cordata, four pairs of shell muscles are found in adult A. cistellula (Fig. 5). One pair of shell adductors attaches medially to the dorsal and to the ventral valve (Fig. 5). Two pairs of pedicle adjustors extend posterior into the pedicle, whereby one attaches to the dorsal and one to the ventral valve. Finally, one pair of diductors attaches at the posterior end of the ventral valve and runs to the dorsal valve.
Each tentacle of the lophophore contains a number of striated muscle fibres. Mantle margin muscles are arranged perpendicularly to the shell periphery along the edge of the dorsal and the ventral valve (Fig. 5A–B).
Myogenesis, metamorphosis, and juvenile myoanatomy of Terebratalia transversa
Larvae of Terebratalia transversa are lecithotrophic and develop for approximately four days at 11°C in the water column until they are competent to undergo metamorphosis. The investigated larvae were three-lobed, 120–178 μm long and 94–141 μm wide, whereby the pedicle lobe was partly overgrown by the mantle lobe. The first developing muscles are the pedicle muscles and early rudiments of the serial mantle muscles (Fig. 6A). Thereafter, the musculature of the four setae pouches forms (Fig. 6B). In later stages, the setae pouch muscles interconnect with the circular mantle muscle (Fig. 6C). A U-shaped muscle extends on the ventral side of the larvae from the pedicle muscles towards the circular mantle muscle. The serial mantle muscles and the setae muscles span between the circular mantle muscle and the U-shaped muscle strand. The latter run from the setae pouches to the central mantle muscles (Fig. 6D). The central mantle muscles extend from the dorsal setae muscles, which run from the dorsal setae pouches towards the apical lobe. They connect to the apical longitudinal muscles at the border of the apical and the mantle lobe (Fig. 6D). Subsequently, the apical musculature develops, which consists of an apical transversal muscle and two lateral apical longitudinal muscles that are connected to the serial mantle muscles (Fig. 6E). In late three-lobed larvae, the pedicle muscles are, together with the central mantle muscles, the most prominent muscular structures. The central mantle muscles connect to the serial mantle muscles, the setae pouch muscles, the setae muscles, and the apical musculature (Fig. 6F).
During metamorphosis, parts of the larval musculature appear to get resorbed and juvenile muscles develop (Fig. 7A). We were, however, unable to clarify whether or not certain components of the larval musculature are incorporated into the juvenile muscular bodyplan.
The juvenile musculature comprises early rudiments of the tentacle muscles, early rudiments of the mantle margin musculature, the musculature of the intestine, adductors, ventral pedicle adjustors which are connected to the diductors, and dorsal pedicle adjustors (Fig. 7B–D).
Comparison of larval and adult rhynchonelliform myoanatomy
The gross morphology of Argyrotheca cistellula differs considerably from that of A. cordata and Terebratalia transversa in that the pedicle lobe gets enclosed by the mantle lobe during development . Thus, A. cistellula appears two-lobed and lacks setae, while the other two species express three distinct body lobes and setae. Despite these differences, myogenesis follows a similar pattern in all three species (Table 1). When fully developed, prominent pedicle muscles, apical longitudinal as well as apical transversal muscles, and serial mantle muscles are present in all three species. In addition, A. cordata and T. transversa show a circular mantle muscle which we consider homologous to the posterior muscle ring in A. cistellula. This homology is based on the similar position of this muscle in the mantle lobe and the fact that the U-shaped muscle of A. cordata and T. transversa and the ventral mantle muscles of A. cistellula all insert at this muscle. The central mantle muscles of A. cordata and T. transversa are in our opinion homologous to the dorsal mantle muscles of A. cistellula due to the similar position of these muscles and their connection to the apical and the serial mantle muscles in all three species. The U-shaped muscle of A. cordata and T. transversa corresponds to the ventral mantle muscles in A. cistellula due to their similar position and the fact that these muscles enclose the serial mantle muscles antero-ventrally.
Despite these similarities, we found distinct differences in the myoanatomy of the three species investigated. As such, the setae pouch muscles, the setae muscles, and the longitudinal muscles, which run from the mantle lobe to the pedicle lobe, are only present in A. cordata and T. transversa, while the lateral mantle muscles are only present in larvae of A. cistellula. These differences between A. cistellula on the one hand and A. cordata and T. transversa on the other correspond to the gross morphological observation that A. cistellula lacks setae.
Larval setae in brachiopods have been proposed to function as a defence device and to control buoyancy . The setae of A. cistellula larvae have probably been secondarily lost, as these larvae are brooded and may settle shortly after release from the mother animal. However, A. cordata larvae have retained their setae despite being brooded, which may hint towards an extended planktonic period of these larvae.
The muscles in the pedicle lobe have been proposed earlier to be of functional use during metamorphosis [32, 33]. When larvae settle, a glandular region at the tip of the primordial hump functions as site of attachment to the substrate . Subsequently, the primordial hump forms the first rudiment of the juvenile pedicle. After larval settlement, the mantle lobe is inverted over the apical lobe and eventually forms the juvenile mantle. The apical lobe gets enclosed by the valves and forms the lophophore and all anterior adult structures [32, 35]. At the onset of metamorphosis, the U-shaped muscle may, due to its connection to the pedicle muscles and the circular mantle muscle, aid in inverting the mantle lobe. During metamorphosis, the larval pedicle muscles are still present at the time of ventral pedicle adjustor and diductor formation. However, whether the larval pedicle muscles are resorbed or are (partly) incorporated into the juvenile diductor and/or pedal adjustor muscles could not be clarified by the present study.
Argyrotheca cordata is the sole species from this study for which data on the larval myoanatomy had previously been available. In the first descriptions from 1873 and 1883, "muscles abdominaux", that run from the pedicle lobe into the mantle lobe, had been identified [14, 30]. A different description was given slightly later, when a network of muscles in the fully developed larva was described. The muscles were denoted "Muskel des lateralen Borstenbündels", "Muskel des medialen Borstenbündels", "musculus contractor", "musculus rotator dorsalis", and "musculus abductor" . Our findings confirm the results of the first papers with respect to the pedicle muscles and the setae muscles. However, in our specimens, the pedicle muscles were not directly connected to the setae muscles as depicted in the first descriptions, but were instead connected to the U-shaped muscle.
In adult Argyrotheca cordata, four pairs of muscles had been identified previously . The pair of adductor muscles has two insertion sites, one anterior to the other at the dorsal valve, and an additional one at the ventral valve. The pair of diductor muscles inserts at the posterior part of both the ventral and the dorsal valve. One of the two pairs of adjustors inserts at the ventral valve and the pedicle, while the other pair inserts at the dorsal valve and the pedicle .
The muscular systems of adult A. cordata and A. cistellula are similar to each other and comprise one pair of adductors, two pairs of pedicle adjustors and one pair of diductors. The tentacles contain several fibres of striated musculature which have previously been described as "rows of striated fusiform myoepithelial cells" in the lophophore of T. transversa .
For the juvenile musculature of Terebratalia transversa we followed the nomenclature used by Eshleman and Wilkens . The juvenile musculature, five days after metamorphosis, comprises rudiments of the tentacle muscles, rudiments of the mantle margin musculature, one pair of adductors, one pair of diductors, one pair of dorsal, and one pair of ventral pedicle adjustors. The ventral pedicle adjustors are connected to the diductors in the juvenile.
Comparative myogenesis of Lophophorata
For the Phoronida, data on muscle development are currently available for three species, namely Phoronis pallida, P. harmeri, and P. architecta [24, 26, 27]. The larvae of these species are of the actinotroch-type and differ considerably from brachiopod larvae in both their gross anatomy and in their lifestyle, because these phoronid larvae are planktotrophic, while the brachiopod larvae investigated herein are of the typical three-lobed, lecithotrophic type. Accordingly, a considerable part of the larval phoronid musculature is linked to the digestive system (e.g., the oesophageal ring muscles) and to the maintenance of a cylindrical body shape (e.g., a meshwork of circular and longitudinal muscles in the bodywall). In addition, trunk retractor muscles, that originate from the posterior collar ring muscles and insert in the telotrochal region, are present in phoronid larvae . The collar region contains mainly ring muscles and few longitudinal muscles. The subumbrellar and exumbrellar layers of the hood contain circular muscles and a series of longitudinal muscles, which, in the exumbrellar layer, function as hood elevators . Furthermore, the tentacles of phoronid actinotroch larvae contain elevator and depressor muscles which consist of two loops in the elevators and a single loop in the depressors. These tentacle muscles are interconnected by the ring muscle of the collar . We did not identify any muscles in the larvae of the three brachiopod species described herein that could potentially correspond to the actinotroch muscle systems known so far.
The muscular architecture in ectoproct larvae is very diverse, thus following the high plasticity of larval gross morphology and the notion that lecithotrophic larvae might have evolved up to six times within Ectoprocta . To date, the larval muscular systems have been described for Membranipora membranacea (cyphonautes larva), Flustrellidra hispida (pseudocyphonautes larva), Celleporaria sherryae and Schizoporella floridana (both coronate larva), Bowerbankia gracilis (vesiculariform larva), Bugula stolonium and B. fulva (both buguliform larva), Sundanella sibogae, Nolella stipata, Amathia vidovici, Aeverrillia setigera, and Alcyonidium gelatinosum (all ctenostome larva), and Crisia elongata (cyclostome larva) [25, 28]. Recently, a number of homologies have been proposed for various larval ectoproct muscle systems . These are the coronal ring muscle, which underlies the ciliated, ring-shaped swimming organ of most larval types, the anterior median muscle, which runs anteriorly from ventral to dorsal in most species, lateral muscles, which project laterally in dorso-ventral direction in most larvae, longitudinal muscles along the posterior body axis, and transversal muscles, which are situated transversally in the central body region of F. hispida, M. membranacea, and A. gelatinosum. Besides these proposed homologous muscles, each larval type shows unique muscles in the body wall and/or inside the larval body, reflecting at least partly the functional adaptations to a planktotrophic versus a lecithotrophic lifestyle. No muscles corresponding to any of the ectoproct muscle types were found in the brachiopod species investigated in this study (and noticeably no homologous muscles between the lecithotrophic ectoproct and brachiopod larval types could be identified), again demonstrating the high plasticity of lophophorate larval anatomy.
All rhynchonelliform brachiopod larvae studied to date are three-lobed with four bundles of setae , except for the larva of Argyrotheca cistellula, which is externally bilobed and lacks setae, and the three-lobed thecideid larvae, which likewise lack setae . Despite these gross morphological differences, myogenesis in the three brachiopod species investigated is very similar. Thus, we propose a larval muscular groundpattern for rhynchonelliform brachiopods comprising apical longitudinal muscles, apical transversal muscles, circular mantle muscles, central mantle muscles, longitudinal muscles, serial mantle muscles, pedicle muscles, setae pouch muscles, setae muscles, and a U-shaped muscle. However, a final statement can only be made once data on the musculature of theceid and rhynchonellid larvae become available.
Comparing this proposed larval muscular groundpattern to the hitherto investigated phoronids, ectoprocts, and spiralian taxa such as polychaetes, molluscs, plathelminths or entoprocts does not reveal any homologies of larval brachiopod muscles and the muscles of other lophotrochozoan larvae, regardless of whether the respective larvae are lecithotrophic or planktotrophic [23, 41–47]. From these data we conclude that the ontogenetic pathways of the individual lophophorate phyla have split early in evolution from that of other Lophotrochozoa, which then resulted in the wide morphological diversity of larval and adult lophophorate bodyplans.
Animal collection and fixation
Argyrotheca cordata and A. cistellula
Adults were obtained from encrusting coralline red algae (coralligène), which was collected in the vicinity of the Observatoire Océanologique de Banyuls-sur-mer, France (42°29'27.51" N; 3°08'07.67" E), by SCUBA from 30–40 m depth in July 2002 and June 2007. All developmental stages from unfertilized eggs to fully differentiated larvae were obtained by dissection from the adults. The specimens were relaxed at room temperature in 7.14% MgCl2, fixed in 4% paraformaldehyde (PFA) in 0.1 M phosphate buffer (PB) for 2 hours or for 3–5 hours, and subsequently washed thrice with 0.1 M PB for 15 min each. The samples were stored in 0.1 M PB with 0.1% NaN3 at 4°C. Material fixed for 2 hours was used for immunocytochemistry (ICC) and material fixed for 3–5 hours was used for scanning electron microscopy (SEM).
Adults were collected in the San Juan Archipelago, USA, in the vicinity of the Friday Harbor Laboratories, and were kept in running seawater tables. To obtain larvae, females were dissected and their eggs transferred into beaker glasses with filtered seawater. The seawater was changed several times in order to wash off follicle cells, and the eggs were left overnight for germinal vesicle breakdown. Males were opened and left in filtered seawater overnight. Thereafter, their testes were scraped out, macerated, and diluted with filtered seawater to obtain a sperm suspension. Prior to fertilization, sperm cells were activated by adding three drops of a 1 M Tris buffer solution (Sigma-Aldrich, St. Louis, MO, USA) to approximately 50 ml of sperm suspension. Larvae were maintained in embryo dishes at around 11°C and the filtered seawater was changed twice daily. Free swimming larvae, metamorphic stages, and juveniles five days after metamorphosis were relaxed in 7.14% MgCl2 and fixed in 4% PFA in 0.1 M PB for 30 min at room temperature. Larvae were washed thrice for 15 min in 0.1 M PB and stored in 0.1 M PB with 0.1% NaN3 at 4°C.
Scanning electron microscopy
For scanning electron microscopy (SEM), the specimens were postfixed in 1% OsO4, dehydrated in a graded acetone series, critical point dried, and sputter coated with gold. Digital images were acquired using a LEO 1430 VP SEM (Zeiss, Jena, Germany).
F-actin labelling, confocal laserscanning microscopy (CLSM), and 3D reconstruction
Prior to staining, larvae were washed thrice for 15 min in PB and incubated for 1 h in PB containing 0.1% Triton X-100 (Sigma-Aldrich) to permeabilize the tissue. Then, the specimens were incubated in 1:40 diluted Alexa Fluor 488 phalloidin (Invitrogen, Molecular Probes, Eugene, OR, USA) and 3 μg/ml DAPI (Invitrogen) in the permeabilization solution overnight at 4°C. Subsequently, specimens were washed thrice for 15 min in 0.1 M PB and embedded in Fluoromount G (Southern Biotech, Birmingham, AL, USA) on glass slides. The same procedure was used for juveniles and adults, with the addition of a decalcifying step using 0.05 M EGTA (Sigma-Aldrich) at room temperature overnight prior to permeabilization and staining. Negative controls omitting the phalloidin dye were performed on all species in order to avoid potential misinterpretations caused by autofluorescence.
The samples were analysed with a Leica DM RXE 6 TL fluorescence microscope equipped with a TCS SP2 AOBS laserscanning device (Leica Microsystems, Wetzlar, Germany). Animals were scanned at intervals of 0.49 μm or 0.64 μm, respectively, and the resulting image stacks were merged into maximum projection images. Photoshop CS3 (Adobe, San Jose, CA, USA) was used to create overlay images of CLSM and light micrographs and for assembling the figure plates. 3D reconstruction was performed on CLSM datasets using volume rendering algorithms of the graphics software Imaris 5.7.2 (Bitplane, Zurich, Switzerland).
Williams A, Rowell AJ: Evolution and Phylogeny. Treatise on Invertebrate Paleontology, Part H, Brachiopoda. Edited by: Moore RC. 1965, Lawrence, Kansas: The Geological Society of America and The University of Kansas, 1: 164-199.
Logan A: Geographic distribution of extant articulated brachiopods. Treatise on Invertebrate Paleontology, Part H, Brachiopoda, Revised. Edited by: Selden PA. 2007, Boulder, Colorado, and Lawrence, Kansas: The Geological Society of America, Inc. and The University of Kansas, 6: 3082-3115.
Stechmann A, Schlegel M: Analysis of the complete mitochondrial DNA sequence of the brachiopod Terebratulina retusa places Brachiopoda within the protostomes. Proc R Soc Lond B Biol Sci. 1999, 266: 2043-2052.
Williams A, Carlson SJ, Brunton CHC, Holmer LE, Popov L: A supra-ordinal classification of the Brachiopoda. Proc R Soc Lond B Biol Sci. 1996, 351: 1171-1193.
Nielsen C: The phylogenetic position of Entoprocta, Ectoprocta, Phoronida, and Brachiopoda. Integr Comp Biol. 2002, 42: 685-691.
Lüter C, Bartolomaeus T: The phylogenetic position of Brachiopoda – a comparison of morphological and molecular data. Zool Scr. 1997, 26: 245-253.
Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD: Broad phylogenomic sampling improves resolution of the animal tree of life. Nature. 2008, 452: 745-749.
Helmkampf M, Bruchhaus I, Hausdorf B: Multigene analysis of lophophorate and chaetognath phylogenetic relationships. Mol Phylogenet Evol. 2008, 46: 206-214.
Mallatt J, Winchell CJ: Testing the new animal phylogeny: First use of combined large-subunit and small-subunit rRNA gene sequences to classify the protostomes. Mol Biol Evol. 2002, 19: 289-301.
Passamaneck Y, Halanych KM: Lophotrochozoan phylogeny assessed with LSU and SSU data: Evidence of lophophorate polyphyly. Mol Phylogenet Evol. 2006, 40: 20-28.
Peterson KJ, Eernisse DJ: Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences. Evol Dev. 2001, 3: 170-205.
Cohen BL: Monophyly of brachiopods and phoronids: reconciliation of molecular evidence with Linnaean classification (the subphylum Phoroniformea nov.). Proc R Soc Lond B Biol Sci. 2000, 267: 225-231.
Cohen BL, Weydmann A: Molecular evidence that phoronids are a subtaxon of brachiopods (Brachiopoda: Phoronata) and that genetic divergence of metazoan phyla began long before the early Cambrian. Org Divers Evol. 2005, 5: 253-273.
Kowalevski AO: Observations sur le développement des brachiopodes (Analyse par Oehlert et Deniker). Arch Zool Exp Gen. 1883, Series 2: 57-76.
Plenk H: Die Entwicklung von Cistella (Argiope) neapolitana. Ein Beitrag zur Entwicklungsgeschichte der Brachiopoden (1. Mitteilung). Arb zool Inst Univ Wien. 1913, 20: 93-108.
Chuang SH: The embryonic, larval and early postlarval development of the terebratellid brachiopod Calloria inconspicua (Sowerby). J R Soc NZ. 1996, 26: 119-137.
Long JA: The embryology of three species representing three superfamilies of articulate Brachiopoda. 1964, University of Washington, PhD Thesis
Lüter C: Embryonic and larval development of Calloria inconspicua (Brachiopoda, Terebratellidae). J R Soc NZ. 1998, 28: 165-167.
Grobe P, Lüter C: Reproductive cycles and larval morphology of three Recent species of Argyrotheca (Terebratellacea: Brachiopoda) from Mediterranean submarine caves. Mar Biol. 1999, 134: 595-600.
Lüter C: Anatomy. Treatise on Invertebrate Paleontology, Part H, Brachiopoda, Revised. Edited by: Selden PA. 2007, Boulder, Colorado, and Lawrence, Kansas: The Geological Society of America, Inc. and The University of Kansas, 6: 2321-2355.
Williams A, Rowell AJ: Brachiopod Anatomy. Treatise on Invertebrate Paleontology, Part H, Brachiopoda. Edited by: Moore RC. 1965, Lawrence, Kansas: Geological Society of America and University of Kansas Press, 1: 6-57.
Hooge MD, Tyler S: Concordance of molecular and morphological data: The example of the Acoela. Integr Comp Biol. 2006, 46: 118-124.
Wanninger A: Myo-anatomy of juvenile and adult loxosomatid entoprocta and the use of muscular body plans for phylogenetic inferences. J Morphol. 2004, 261: 249-257.
Santagata S: Structure and metamorphic remodeling of the larval nervous system and musculature of Phoronis pallida (Phoronida). Evol Dev. 2002, 4: 28-42.
Gruhl A: Muscular systems in gymnolaemate bryozoan larvae (Bryozoa: Gymnolaemata). Zoomorphology. 2008, 127: 143-159.
Santagata S: Larval development of Phoronis pallida (Phoronida): Implications for morphological convergence and divergence among larval body plans. J Morphol. 2004, 259: 347-358.
Santagata S, Zimmer RL: Comparison of the neuromuscular systems among actinotroch larvae: systematic and evolutionary implications. Evol Dev. 2002, 4: 43-54.
Santagata S: The morphology and evolutionary significance of the ciliary fields and musculature among marine bryozoan larvae. J Morphol. 2008, 269: 349-364.
Lüter C: Ultrastructure of larval and adult setae of Brachiopoda. Zool Anz. 2000, 239: 75-90.
Shipley AE: On the structure and development of Argiope. Mitt zool Stat Neapel. 1883, 4: 494-520.
Chuang SH: Larval development in Discinisca (inarticulate brachiopod). Am Zool. 1977, 17: 39-53.
Stricker SA, Reed CG: The ontogeny of shell secretion in Terebratalia transversa (Brachiopoda, Articulata). 1. Development of the mantle. J Morphol. 1985, 183: 233-250.
Lüter C: Zur Ultrastruktur, Ontogenese und Phylogenie der Brachiopoda. 1998, Göttingen: Cuvillier Verlag
James MA, Ansell AD, Collins MJ, Curry GB, Peck LS, Rhodes MC: Biology of living brachiopods. Adv Mar Biol. 1992, 28: 175-387.
Stricker SA, Reed CG: The ontogeny of shell secretion in Terebratalia transversa (Brachiopoda, Articulata). 2. Formation of the protegulum and juvenile shell. J Morphol. 1985, 183: 251-271.
Reed CG, Cloney RA: Brachiopod tentacles – ultrastructure and functional significance of connective-tissue and myoepithelial cells in Terebratalia. Cell Tissue Res. 1977, 185: 17-42.
Eshleman WP, Wilkens JL: Actomyosin ATPase activities in the brachiopod Terebratalia transversa. Can J Zool. 1979, 57: 1944-1949.
Strathmann RR: Evolution and loss of feeding larval stages of marine invertebrates. Evolution. 1978, 32: 894-906.
Pennington JT, Stricker SA: Phylum Brachiopoda. Atlas of Marine Invertebrate Larvae. Edited by: Young CM. 2002, San Diego: Academic Press, 441-461.
de Lacaze-Duthiers FJH: Histoire naturelle des brachiopodes vivants de la Mediterranée. I. Histoire naturelle de la Thecidie (Thecidium mediterraneum). Ann Sci Nat Zool (serie 4). 1861, 15: 259-330.
Hill SD, Boyer BC: Phalloidin labeling of developing muscle in embryos of the polychaete Capitella sp. I. Biol Bull. 2001, 201: 257-258.
Reiter D, Boyer B, Ladurner P, Mair G, Salvenmoser W, Rieger R: Differentiation of the body wall musculature in Macrostomum hystricinum marinum and Hoploplana inquilina (Plathelminthes) as models for muscle development in lower Spiralia. Dev Genes Evol. 1996, 205: 410-423.
Fuchs J, Bright M, Funch P, Wanninger A: Immunocytochemistry of the neuromuscular systems of Loxosomella vivipara and Loxosomella parguerensis (Entoprocta: Loxosomatidae). J Morphol. 2006, 267: 866-883.
McDougall C, Chen W-C, Shimeld S, Ferrier D: The development of the larval nervous system, musculature and ciliary bands of Pomatoceros lamarckii (Annelida): heterochrony in polychaetes. Front Zool. 2006, 3: 16-
Nielsen C, Haszprunar G, Ruthensteiner B, Wanninger A: Early development of the aplacophoran mollusc Chaetoderma. Acta Zool. 2007, 88: 231-247.
Wanninger A, Haszprunar G: Chiton myogenesis: Perspectives for the development and evolution of larval and adult muscle systems in molluscs. J Morphol. 2002, 251: 103-113.
Wanninger A, Ruthensteiner B, Lobenwein S, Salvenmoser W, Dictus WJAG, Haszprunar G: Development of the musculature in the limpet Patella (Mollusca, Patellogastropoda). Dev Genes Evol. 1999, 209: 226-238.
We are grateful to Henrike Semmler (Copenhagen) for rearing and fixing Terebratalia larvae during the Comparative Invertebrate Embryology class 2006 at the Friday Harbor Laboratories and for comments on an early draft of the manuscript. We further thank the divers and the staff of the Marine Biological Station Banyuls-sur-mer for collecting the coralligène and for providing laboratory space. Scott Santagata (Brookville, New York) is thanked for comments on the manuscript and Jana Hoffmann (Berlin, Germany) for providing access to some of the classic literature. The valuable comments of an anonymous reviewer helped to improve the manuscript. This study was funded by the Danish Agency for Science, Technology and Innovation (grant no. 645-06-0294 to AW) and the Danish Research Agency (grant no. 21-04-0356 to AW). Research in the lab of A. Wanninger is further supported by the EU-funded Marie Curie Network MOLMORPH (contract grant number MEST-CT-2005-020542).
The authors declare that they have no competing interests.
AA performed research and drafted the manuscript. AW designed and coordinated research, performed the SEM analysis, and contributed significantly to the writing of the manuscript. Both authors read and approved the final version of the manuscript.
Electronic supplementary material
Additional file 1: Larval musculature of Argyrotheca cordata . Movie of a confocal scan through a fully developed larva of Argyrotheca cordata to illustrate the three-dimensional arrangement of the larval musculature. (MPG 12 MB)
Authors’ original submitted files for images
Below are the links to the authors’ original submitted files for images.
About this article
Cite this article
Altenburger, A., Wanninger, A. Comparative larval myogenesis and adult myoanatomy of the rhynchonelliform (articulate) brachiopods Argyrotheca cordata, A. cistellula, and Terebratalia transversa. Front Zool 6, 3 (2009). https://doi.org/10.1186/1742-9994-6-3
- Longitudinal Muscle
- Ventral Valve
- Dorsal Valve
- Larval Musculature
- Ring Muscle