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Abstract
Background
Myogenesis is currently investigated in a number of invertebrate taxa using combined
techniques, including fluorescence labeling, confocal microscopy, and 3D imaging,
in order to understand anatomical and functional issues and to contribute to evolutionary
questions. Although developmental studies on the gross morphology of bivalves have
been extensively pursued, organogenesis including muscle development has been scarcely
investigated so far.
Results
The present study describes in detail myogenesis in the scallop
Nodipecten nodosus (Linnaeus, 1758) during larval and postmetamorphic stages by means of light, electron,
and confocal microscopy. The veliger muscle system consists of an anterior adductor
muscle, as well as four branched pairs of striated velum retractors and two pairs
of striated ventral larval retractors. The pediveliger stage exhibits a considerably
elaborated musculature comprising the velum retractors, the future adult foot retractor,
mantle (pallial) muscles, and the anterior and posterior adductors, both composed
of smooth and striated portions. During metamorphosis, all larval retractors together
with the anterior adductor degenerate, resulting in the adult monomyarian condition,
whereby the posterior adductor retains both myofiber types. Three muscle groups, i.e.,
the posterior adductor, foot retractor, and pallial muscles, have their origin prior
to metamorphosis and are subsequently remodeled.
Conclusions
Our data suggest a dimyarian condition (i.e., the presence of an anterior and a posterior
adductor in the adult) as the basal condition for pectinids. Comparative analysis
of myogenesis across Bivalvia strongly argues for ontogenetic and evolutionary independence
of larval retractors from the adult musculature, as well as a complex set of larval
retractor muscles in the last common bivalve ancestor.
Electronic supplementary material
The online version of this article (doi:10.1186/s12983-015-0125-x) contains supplementary
material, which is available to authorized users.
Results and Discussion The Aculifera Hypothesis and Molluscan Ancestry The evolutionary origin of Mollusca has been a matter of long-standing debate. Thereby, reconstruction of the last common ancestor (LCA) to all mollusks, the so-called hypothetical ancestral mollusk, has been hampered by difficulties in recovering fossils of unambiguous molluscan stem species and by the lack of a general agreement concerning the relationships of the various molluscan class-level taxa to each other [2]. As a consequence, a broad consensus concerning the deep nodes in molluscan phylogeny is still lacking. Morphology-based analyses have suggested either one or the other of the sclerite-bearing but shell-less aplacophoran clades (Neomeniomorpha or Chaetodermomorpha, respectively) as the earliest molluscan offshoot [8, 9], a monophyletic Aplacophora as sister group to all remaining mollusks (the Testaria) [10], or a polyplacophoran-aplacophoran assemblage (Aculifera) as sister to all other mollusks with a primarily univalved shell (Conchifera) [11, 12]. This controversy may soon be settled, however, since two phylogenomic studies have independently confirmed the latter concept, whereby both recovered a monophyletic Aplacophora as sister group to Polyplacophora (chitons) within Aculifera [4, 5]. In the light of this phylogenetic framework, the recent description of a cylindrical (i.e., worm-shaped) sclerite- and shell-bearing Paleozoic mollusk [6] and the results of integrative molecular-paleontological studies [13, 14] have been considered as evidence for the presence of seven or eight shell plates in the LCA of crown-group aculiferans. If correct, this implies that the body plan of recent aplacophorans is the result of secondary simplification and thus a derived condition [6, 14]. Despite additional descriptions of fossils that exhibit a mixture of polyplacophoran- and aplacophoran-like features [15, 16], the morphology of the LCA of Aculifera remains elusive. This may be due to the overall paucity of well-preserved Paleozoic fossils that undoubtedly can be assigned to the aculiferan lineage, the uncertainty as to whether or not some early (Cambrian or Precambrian) fossils [17, 18] indeed represent crown- or stem-group mollusks, and the fact that solid morphological and developmental evidence from recent aplacophoran representatives is still largely lacking. The few reports of individual aplacophoran larvae and postlarvae have shown that these animals may bear six or seven rows of papillae, sclerites, or sclerite-secreting cells [19–21], but these studies found no further support by gross morphological developmental studies of two neomeniomorph representatives [22, 23]. Myogenesis Suggests that Aplacophorans Have a Secondarily Simplified Body Plan The muscular architecture of mollusks is intimately associated with the existence, number, and arrangement of shells in the respective taxa [24]. In polyplacophorans, the myoanatomy is highly complex [7, 25] (Figures 1A and 1C) and several components, such as a laterally positioned enrolling muscle and a dorsal rectus system that spans the longitudinal axis of the animal, have been widely considered as defining morphological features (autapomorphies) of this taxon [24]. In stark contrast to the sophisticated polyplacophoran myoanatomy, aplacophoran representatives have a much simpler muscular organization that, together with the body wall musculature, mainly comprises serially repeated dorsoventral muscles (Figures 1B and 1D). Accordingly, a scenario that suggests a shell plate-bearing aculiferan LCA with polyplacophoran-like musculature implies drastic secondary simplification of the muscular body plan of aplacophoran mollusks. Since ontogenetic data may provide important insights into the evolutionary history of a given taxon [26, 27], we investigated the development of a model neomeniomorph aplacophoran, Wirenia argentea, from hatching of the larvae until after metamorphosis. In comparing myogenesis in Wirenia with that of a polyplacophoran (Leptochiton asellus), we found striking similarities in the muscular organization of both species (see Table 1 for a summary of major larval and adult muscle systems known for the various molluscan lineages), including the presence of a rectus muscle (Figures 2A–2D), so far only known from polyplacophorans, and a laterally positioned enrolling muscle (Figures 2A–2H). Both systems are retained in adult polyplacophorans but are lost during Wirenia postlarval development (note that some neomeniomorphs do exhibit distinct enrolling muscles as adults [28, 29]). Although homology between the polyplacophoran and neomeniomorph enrolling muscles has been questioned [7], their similar position in the respective animals and, in particular, their identical mode of ontogenetic formation as independent muscle system (and not as a thickened derivative of the body wall musculature, as proposed earlier for the aplacophoran taxa [7]) argue strongly for their common evolutionary origin and thus for the presence of such a system in the LCA of both clades. Aside from these muscles, we found two additional muscular systems shared only by polyplacophorans and neomeniomorphs. These are a paired ventrolateral and a single ventromedian muscle (Figures 2E–2L). Both systems are only transiently present in advanced larvae, and neither has a counterpart in either the polyplacophoran or the neomeniomorph adult body plan. As with the rectus and the enrolling muscles, the identical positions of the ventrolateral and the ventromedian muscles in Wirenia and Leptochiton larvae, together with their identical positions relative to other muscles, clearly suggest that these respective muscles are homologous between the two species (see [30] for a recent overview on homology theory and assessment). Earlier, we had already found the ventrolateral system in larvae of another polyplacophoran, Mopalia muscosa [7], but had overlooked the ventromedian muscle. Reinvestigation of the original 3D data set, however, unambiguously revealed such a muscle also in Mopalia (data not shown; available on request). Accordingly, it appears highly likely that the ventrolateral and the ventromedian muscles together with the enrolling and the rectus muscle were all part of the muscular toolkit of the LCA of polyplacophorans and neomeniomorphs, and that the simple myoanatomy of adult Wirenia is a derived, secondary condition. Formation of the eight sets of dorsoventral muscles in polyplacophorans passes through a transitory stage of multiple individual myocytes that appear synchronously [7] (Figure 2E) and give rise to the first seven paired shell muscle units (while the eighth set forms considerably later, together with the most posterior shell plate [7]). In Wirenia, seven pairs of dorsoventral muscles develop simultaneously (Figures 3A–3E) and differentiate further in later stages (Figure 2F). A gradual numerical increase of the dorsoventral muscle sets was observed only after metamorphosis (Figure 3F). Accordingly, both neomeniomorphs and polyplacophorans exhibit a transient stage of seven-fold seriality in the arrangement of these muscles. Despite the different ontogenetic pathways that lead to this seven-fold seriality (fusion of multiple myocytes in polyplacophorans versus simultaneous formation in Wirenia), this seven-fold seriality appears to be a reoccurring pattern, at least in aculiferan mollusks (unfortunately, the ontogenetic sequence of the formation of the eight pairs of dorsoventral muscles in Monoplacophora is still unknown). This is well in line with the description of the seven-shelled fossil Kulindroplax [6], as well as with the serially arranged sclerites or papillae of some recent aplacophorans [19–21], and lends further support for an aculiferan LCA with a seven-fold seriality of epidermal hardparts and the associated musculature. This implies that the eighth set of dorsoventral muscles of recent polyplacophorans is a derived condition. The late formation of the most posterior shell plate and associated musculature in polyplacophorans [7, 31] may well be considered as ontogenetic testimony of such a scenario. The rudimentary data on myogenesis (and development in general) [21] of the second aplacophoran taxon, the Chaetodermomorpha, does not allow for definite conclusions concerning the presence of neomeniomorph- and/or polyplacophoran-like features such as the rectus or the ventromedian muscles in the LCA of this taxon. However, the ring musculature in the body wall of both aplacophoran clades, which is also rudimentarily present in the apical region of polyplacophoran larvae [7] (Figure 2), may constitute an aculiferan apomorphy uniting Polyplacophora, Neomeniomorpha, and Chaetodermomorpha (Table 1). This, together with the cylindrical shape of the aplacophorans and the polyplacophoran larva as well as the fossil Kulindroplax, argues for a worm-like body shape of the LCA of Aculifera, rendering the dorsoventrally flattened appearance of recent polyplacophorans a derived condition. The paired lateral longitudinal muscle in the larva of the chaetodermomorph Chaetoderma [21] may correspond to either the enrolling or the ventrolateral muscle of larval polyplacophorans and neomeniomorphs (Table 1), which would further support the inclusion of Chaetodermomorpha within Aculifera. The fact that Kulindroplax shares morphological features not only with polyplacophorans but also with recent chaetodermomorphs, including the absence of a pedal pit and the position of the gills [6], likewise supports such a scenario. Whether or not a monophyletic Aculifera will stand the test of future phylogenetic analyses or whether Chaetodermomorpha, despite these shared morphological characters, will be proven to have different affinities [32] remains to be seen. The transient expression of typical polyplacophoran-like muscles in the Wirenia larva, however, strongly suggests that at least neomeniomorph aplacophorans stem from an ancestor with polyplacophoran-like features that most likely also included seven shell plates.
We investigated muscle development in two chiton species, Mopalia muscosa and Chiton olivaceus, from embryo hatching until 10 days after metamorphosis. The anlagen of the dorsal longitudinal rectus muscle and a larval prototroch muscle ring are the first detectable muscle structures in the early trochophore-like larva. Slightly later, a ventrolaterally situated pair of longitudinal muscles appears, which persists through metamorphosis. In addition, the anlagen of the putative dorsoventral shell musculature and the first fibers of a muscular grid, which is restricted to the pretrochal region and consists of outer ring and inner diagonal muscle fibers, are generated. Subsequently, transversal muscle fibers form underneath each future shell plate and the ventrolateral enrolling muscle is established. At metamorphic competence, the dorsoventral shell musculature consists of numerous serially repeated, intercrossing muscle fibers. Their concentration into seven (and later eight) functional shell plate muscle bundles starts after the completion of metamorphosis. The larval prototroch ring and the pretrochal muscle grid are lost at metamorphosis. The structure of the apical grid and its atrophy during metamorphosis suggests ontogenetic repetition of (parts of) the original body-wall musculature of a proposed worm-shaped molluscan ancestor. Moreover, our data show that the "segmented" character of the polyplacophoran shell musculature is a secondary condition, thus contradicting earlier theories that regarded the Polyplacophora (and thus the entire phylum Mollusca) as primarily eumetameric (annelid-like). Instead, we propose an unsegmented trochozoan ancestor at the base of molluscan evolution. Copyright 2002 Wiley-Liss, Inc.
The Mollusca is one of the most diverse, important and well-studied invertebrate phyla; however, relationships among major molluscan taxa have long been a subject of controversy. In particular, the position of the shell-less vermiform Aplacophora and its relationship to the better-known Polyplacophora (chitons) have been problematic: Aplacophora has been treated as a paraphyletic or monophyletic group at the base of the Mollusca, proximate to other derived clades such as Cephalopoda, or as sister group to the Polyplacophora, forming the clade Aculifera. Resolution of this debate is required to allow the evolutionary origins of Mollusca to be reconstructed with confidence. Recent fossil finds support the Aculifera hypothesis, demonstrating that the Palaeozoic-era palaeoloricate 'chitons' included taxa combining certain polyplacophoran and aplacophoran characteristics. However, fossils combining an unambiguously aplacophoran-like body with chiton-like valves have remained elusive. Here we describe such a fossil, Kulindroplax perissokomos gen. et sp. nov., from the Herefordshire Lagerstätte (about 425 million years bp), a Silurian deposit preserving a marine biota in unusual three-dimensional detail. The specimen is reconstructed three-dimensionally through physical-optical tomography. Phylogenetic analysis indicates that this and many other palaeoloricate chitons are crown-group aplacophorans.
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