Evolution of a Novel Muscle Design in Sea Urchins (Echinodermata: Echinoidea)


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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