Abstract

This work comprises detailed studies by scanning electron microscopy (SEM), transmission electron microscopy (TEM), fluorescence staining combined with confocal laser scanning microscopy (CLSM), as well as serial sectioning analyses and reconstruction techniques to elucidate the development of the larval and adult musculature of several basal representatives of the molluscan classes Polyplacophora, Bivalvia, Scaphopoda, and Gastropoda. Special reference is given to the shell musculature. In addition, aspects of the myo-anatomy of adult Solenogastres are reconsidered. A further part of this study deals with scaphopod shell morphogenesis and expression of the homeobox gene engrailed (en), in order to gain insights regarding the scaphopod-bivalve relationship. The results enable far reaching conclusions regarding the evolution and the phylogeny of the Mollusca. Solenogastres TEM analysis of adult Solenogastres revealed a mesenchymate body wall musculature which consists of outer ring, intermediate diagonal, and inner longitudinal muscles and resembles the condition of other worm-shaped taxa. The ventrally inter-crossing dorso-ventral musculature, which is diagnostic for the Mollusca, is arranged in multiple serial units along the anterior-posterior body axis. Polyplacophora During development, the chiton larva undergoes an intermediate stage in which the dorso-ventral musculature is serially arranged as in adult Solenogastres. The concentration into seven (and later eight) functional shell plate muscle units is a secondary condition which takes place after metamorphosis. Thus, assumptions of a primarily "segmented" (i.e. annelidlike) character of the polyplacophoran shell plate musculature are rejected. In addition, the anterior (i.e. pre-trochal) body region of chiton larvae shows a muscular grid which is lost at metamorphosis and resembles the body wall musculature of adult aplacophoran (Solenogastres + Caudofoveata) molluscs. Both, the multiple seriality of the dorso-ventral muscles and the apical muscle grid are regarded as ontogenetic recapitulation of the basal molluscan condition which is fully expressed in the adult body plan of Solenogastres. This infers a non-segmented, worm-shaped ancestor at the base of molluscan evolution. The existence of a larval ring-shaped muscle that underlies the prototroch cells (prototroch muscle ring) is a shared feature of polyplacophoran, gastropod, and bivalve larvae (see below) and suprataxic homology of this organ is proposed. Bivalvia Besides a rather complicated set of larval retractor muscles, the veligers of autobranchs (i.e. all Bivalvia except the Protobranchia, the latter with a test-cell larva) exhibit a distinct prototroch muscle ring similar to chitons and gastropods. Both systems are entirely larval and are resorbed during metamorphosis. Scaphopoda The general ontogeny and especially myogenesis in the dentaliid scaphopod Antalis entalis proceeds much more direct than in polyplacophorans or gastropods. Accordingly, distinct larval muscle systems are lacking. However, the paired cephalic and pedal retractors both form additional fibers which project into the region of the prototroch and are lost at metamorphosis. The existence of a distinct, paired cephalic retractor system, which is also found in the basal gastropod and cephalopod bauplan but not in the Bivalvia, suggests a clade comprising the Scaphopoda and Gastropoda + Cephalopoda. This is strengthened by expression data of the homeobox gene engrailed, which plays a significant role in molluscan shell formation. While two dorso-lateral centers of engrailed expression, which correspond to the two centers of initial shell calcification, are found in early bivalve veligers, engrailed is exclusively found in mantle margin cells surrounding the single anlage of the embryonic scaphopod shell. In contrast to bivalves, the scaphopod shell is thus formed from a single center of calcification, and a scaphopod-bivalve sistergroup relationship is therefore rejected. Gastropoda Primitive gastropods, such as the patellogastropods Patella vulgata and Patella caerulea, show one pair of asymmetrically positioned larval retractor muscles which have distinct insertion sites at the embryonic shell. Another strict larval muscle system is the prototrochal muscle ring. All these muscle are lost before, during, or shortly after metamorphosis. Parts of the adult mantle musculature as well as the muscles of the cephalic tentacles are formed prior to metamorphosis, while the buccal musculature is of entire postmetamorphic origin. The process of gastropod ontogenetic torsion is mainly caused by muscular activity of the larval retractors, while the adult shell musculature arises after the completion of torsion. Thus, ontogenetic torsion is regarded as an entirely larval process inferring that the arrangement of the adult shell musculature - which can often be reconstructed by muscle scars on fossilized shells - is not indicative for the question whether paleozoic univalved molluscs were torted or not.