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PLoS One
2012 Jan 01;75:e37520. doi: 10.1371/journal.pone.0037520.
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Evolution of a novel muscle design in sea urchins (Echinodermata: Echinoidea).
Ziegler A
,
Schröder L
,
Ogurreck M
,
Faber C
,
Stach T
.
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The sea urchin (Echinodermata: Echinoidea) masticatory apparatus, or Aristotle''s lantern, is a complex structure composed of numerous hard and soft components. The lantern is powered by various paired and unpaired muscle groups. We describe how one set of these muscles, the lantern protractor muscles, has evolved a specialized morphology. This morphology is characterized by the formation of adaxially-facing lobes perpendicular to the main orientation of the muscle, giving the protractor a frilled aspect in horizontal section. Histological and ultrastructural analyses show that the microstructure of frilled muscles is largely identical to that of conventional, flat muscles. Measurements of muscle dimensions in equally-sized specimens demonstrate that the frilled muscle design, in comparison to that of the flat muscle type, considerably increases muscle volume as well as the muscle''s surface directed towards the interradial cavity, a compartment of the peripharyngeal coelom. Scanning electron microscopical observations reveal that the insertions of frilled and flat protractor muscles result in characteristic muscle scars on the stereom, reflecting the shapes of individual muscles. Our comparative study of 49 derived "regular" echinoid species using magnetic resonance imaging (MRI) shows that frilled protractor muscles are found only in taxa belonging to the families Toxopneustidae, Echinometridae, and Strongylocentrotidae. The onset of lobe formation during ontogenesis varies between species of these three families. Because frilled protractor muscles are best observed in situ, the application of a non-invasive imaging technique was crucial for the unequivocal identification of this morphological character on a large scale. Although it is currently possible only to speculate on the functional advantages which the frilled muscle morphology might confer, our study forms the anatomical and evolutionary framework for future analyses of this unusual muscle design among sea urchins.
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22624043
???displayArticle.pmcLink???PMC3356314 ???displayArticle.link???PLoS One
Figure 2. Gross morphology, histology, and ultrastructure of the frilled protractor muscle found in Echinometra mathaei.(A) Virtual horizontal section through a MRI dataset with 81 µm isotropic voxel resolution at the level of the retractor muscles. (B) Close-up view. In horizontal section, the protractor muscles appear as frilled bands. (C) Semi-thin section through a frilled protractor muscle. (D) Semi-thin section of a fascicle (indicated by the dotted line). (E) Semi-thin section of the protractor muscle epithelium directed towards the interradial cavity. (F) Semi-thin section of the protractor muscle epithelium directed towards the exterior cavity. (G) Ultra-thin section through the bordering area of four muscle fibers. (H) Ultra-thin section of the ciliated cuboidal epithelium directed towards the interradial cavity. (I) Ultra-thin section of the ciliated epithelium directed towards the exterior cavity. (J) Ultra-thin vertical section through a cilium. All epithelia found covering the protractor muscles are ciliated. (K) Ultra-thin vertical section through a collagen fibril. The presence of collagen fibrils varies between the adaxial and the abaxial connective tissue layers. au = auricle, bl = basal lamina, cc = central cavity, cf = collagen fibril, ci = cilium, ct = connective tissue, ec = exterior cavity, ep = epithelial cell, fa = fascicle, ic = interradial cavity, ip = interpyramidal muscle, lo = lobe, mf = muscle fiber, np = nerve process, nu = nucleus, ph = pharynx, po = postural muscle, pr = protractor muscle, pv = perivisceral coelom, py = pyramid, re = retractor muscle, to = tooth.
Figure 3. Comparison of muscle scars created by flat (A–H, Paracentrotus lividus) and frilled (I–P, Echinometra mathaei) protractor muscles on skeletal elements.(A, I) Volume-rendered models of the lantern based on μCT datasets with 27 µm isotropic voxel resolution. The boxes indicate the areas shown in C, D and K, L. (B, J) Virtual horizontal section through MRI datasets with 78×78×500 µm resolution showing the flat and frilled protractor muscles prior to their insertion on the epiphysis. (C, D, K, L) SEM micrographs of the muscle scars created by flat and frilled protractor muscles on the epiphysis and upper pyramid. The dotted lines indicate the outline of the protractor muscle. (K, L, E, M) Volume-rendered models of lantern and perignathic girdle based on μCT datasets with 27 µm isotropic voxel resolution. The boxes indicate the location of the interambulacral insertion site of the protractor muscle on the perignathic girdle. (F, N) Virtual horizontal section through MRI datasets with 78×78×500 µm resolution showing the protractor muscles prior to their insertion on the perignathic girdle. (G, H, O, P) SEM micrograph of the muscle scars created by flat and frilled protractor muscles on the perignathic girdle. The dotted lines indicate the outline of the protractor muscle. au = auricle, bn = buccal notch, ep = epiphysis, lo = lobe, pg = perignathic girdle, pr = protractor muscle, py = pyramid, to = tooth, ts = tooth support.
Figure 4. Illustration of the close interrelationship between lantern protractor muscles and buccal sacs in derived “regular†sea urchins, exemplified by Strongylocentrotus purpuratus.(A) Photograph of the oral part of the interambulacrum showing the location of the paired buccal sacs. (B) Volume-rendered model of a μCT dataset with 27 µm isotropic voxel resolution showing the same view as in (A), but soft tissues are inapparent due to the type of analysis employed (i.e., X-ray). The dotted line indicates the location of a single buccal sac. (C) Virtual vertical section through a MRI dataset with 42 µm isotropic voxel resolution. The lumen of the buccal sacs is continuous with the interradial cavity. The labels marked (D–I) indicate the location of the horizontal sections shown hereafter. (D–I) Virtual horizontal sections through a MRI dataset with 78×78×500 µm resolution. The protractor muscles are located directly above the buccal notches. am = ambulacrum, bn = buccal notch, bp = buccal plate, bs = buccal sac, ce = compass elevator muscle, es = exterior septum, ic = interradial cavity, im = interambulacrum, in = intestine, lo = lobe, pe = peristome, pm = peristomial membrane, pr = protractor muscle, pv = perivisceral coelom, py = pyramid, sp = spine, st = stomach, tf = tube foot, to = tooth.
Figure 5. Comparison of protractor muscle shape in selected derived “regular†sea urchin species.Frilled protractor muscles can only be found in sea urchin species of the families Toxopneustidae, Echinometridae, and Strongylocentrotidae (K–P). See Fig. 6 for a phylogeny of the Echinoidea, while Table 3 lists character distribution in all 49 echinacean species analyzed in this study. (A) Stomopneustes variolaris (Stomopneustidae). (B) Arbacia dufresnii (Arbaciidae). (C) Parasalenia gratiosa (Parasaleniidae). (D) Temnopleurus toreumaticus and (E) Pseudechinus magellanicus (Temnopleuridae). (F) Trigonocidaris albida (Trigonocidaridae). (G) Polyechinus agulhensis and (H) Sterechinus neumayeri (Echinidae). (I) Parechinus angulosus and (J) Psammechinus microtuberculatus (Parechinidae). (K) Toxopneustes pileolus and (L) Sphaerechinus granularis (Toxopneustidae). (M) Echinometra lucunter and (N) Heterocentrotus mammilatus (Echinometridae). (O) Pseudocentrotus depressus and (P) Hemicentrotus pulcherrimus (Strongylocentrotidae). (A–E), (G–K), and (N–P) based on MRI datasets with 50×50×200 µm resolution. (F) based on a MRI dataset with 32 µm isotropic voxel resolution. (L, M) based on MRI datasets with 78×78×500 µm resolution. lo = lobe.
Figure 7. Schematic illustration of general differences in lantern protractor muscle morphology and resulting changes in the relation of muscle volume to muscle surface.An increase in volume of the flat and thin protractor muscle (A) can either result in a flat and thick (B) or a frilled and thin (C) muscle design. However, only the frilled protractor muscle design considerably increases muscle volume (dark grey) as well as the muscle surface directed towards the interradial cavity (light grey). These values are based on measurements provided in Table 2.
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