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Comparative larval myogenesis and adult myoanatomy of the rhynchonelliform (articulate) brachiopods Argyrotheca cordata, A. cistellula, and Terebratalia transversa
© Altenburger and Wanninger; licensee BioMed Central Ltd. 2009
Received: 05 November 2008
Accepted: 03 February 2009
Published: 03 February 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
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 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).
Myogenesis and adult myoanatomy of Argyrotheca cistellula
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
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
Comparative larval myoanatomy of the rhynchonelliform brachiopods Argyrotheca cordata, Terebratalia transversa, and A. cistellula
Symbol in figures
apical longitudinal muscles
apical transversal muscle
+ (apical muscle ring)
central mantle muscles
+ (dorsal mantle muscles)
circular mantle muscle
+ (posterior muscle ring)
lateral mantle muscle
mantle and pedicle lobe
serial mantle muscles
setae pouch musculature
+ (ventral mantle muscle)
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).
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).
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