Myoanatomy of Myzostoma cirriferum (Annelida, Myzostomida): Implications for the evolution of the myzostomid body plan

Abstract

Studies of rare genomic marker systems suggest that Myzostomida are a subgroup of Annelida and phylogenomic analyses indicate an early divergence of this taxon within annelids. However, adult myzostomids show a highly specialized body plan, which lacks typical annelid features, such as external body annulation, coelomic cavities with metanephridia, and segmental ganglia of the nervous system. The putative loss of these features might be due to the parasitic/symbiotic lifestyle of myzostomids associated with echinoderms. In contrast, the larval anatomy and adult locomotory system resemble those of annelids. To clarify whether the myoanatomy of myzostomids reflects their relationship to annelids, we analyzed the distribution of f-actin, a common component of muscle fibers, in specimens of Myzostoma cirriferum using phalloidin-rhodamine labeling in conjunction with confocal laser-scanning microscopy. Our data reveal that the musculature of the myzostomid body comprises an outer circular layer, an inner longitudinal layer, numerous dorsoventral muscles, and prominent muscles of the parapodial complex. These features correspond well with the common organization of the muscular system in Annelida. In contrast to other annelids, however, several elements of the muscular system in M. cirriferum, including the musculature of the body wall, and the parapodial flexor muscles, exhibit radial symmetry overlaying a bilateral body plan. These findings are in line with the annelid affinity of myzostomids and suggest that the apparent partial radial symmetry of M. cirriferum arose secondarily in this species. Based on our data, we provide a scenario on the rearrangements of muscle fibers that might have taken place in the lineage leading to this species.

Myoanatomy and anterior muscle regeneration of the fireworm Eurythoe cf. complanata (Annelida: Amphinomidae)

“…cf. complanata is in concordance with investigations by Gustafson () and Storch (), and comparable to conditions known from biramous Errantia, such as Glyceridae, Aphroditidae, and Nereididae, but can be also observed in the uniramous Sphaerodoridae, Phyllodocidae, Syllidae, and Myzostomida (Storch, ; Tzetlin and Filippova, ; Filippova et al, ; Helm et al, ; Aguado et al, ; Helm and Capa, ). A prominent acicular flexor muscle is present in the notopodial branch of E .…”

Comparative analyses of morphological characters in Sphaerodoridae and allies (Annelida) revealed by an integrative microscopical approach

“…Sphaerodoridae typically possess uniramous parapodia supported by a single straight aciculum. Similar parapodial muscle patterns showing prominent sets of protractor and flexor muscles can be found within the biramous Glyceridae, Aphroditidae, and Nereididae, and are shown herein for the uniramous phyllodocids and syllids, and the putatively errant Myzostomida as well (Storch, 1968;Tzetlin and Filippova, 2005;Helm et al, 2013). Notably, within Glyceriformia, several taxa are uniramous as well and others bear both uni-and biramous conditions (e.g., Storch, 1968).…”

“…Therefore, the arrangement of longitudinal and transverse muscle fibers in long-bodied sphaerodorids is similar to the conditions known for most annelids, and thus has to be regarded as an ancestral character. A division of the dorsalmost longitudinal bundles into smaller bundles as described for the long-bodied sphaerodorids is also known for several members of the Errantia, e.g., Syllidae, Polynoidae, Chrysopetalidae, Aphroditidae, and Myzostomida (Tzetlin and Filippova, 2005;Purschke and Müller, 2006;Helm et al, 2013). Due to the high variability concerning the arrangement of longitudinal muscle bundles in different taxa, usability of this character for evolutionary questions remains unclear (see also Tzetlin and Filippova, 2005).…”

“…Thus, four distinct longitudinal bundles are present in most Errantia (Tzetlin and Filippova, 2005), and the presence of two additional dorsal longitudinal muscle fibers in long-bodied Sphaerodoridae and four additional fibers in short-bodied forms has to be assumed as a secondary condition. A dorsal outer muscle layer of transverse muscle fibers is also known for Hesionidae, Nereidididae, Syllidae, Myzostomida and Phyllodocidae (Tzetlin and Filippova, 2005;Purschke and Müller, 2006;Filippova et al, 2010;Helm et al, 2013). Being also present in taxa outside the phyllodocid radiation, like e.g., in most Eunicida and Sedentaria, and members of the Amphinomidae and Sipuncula (see Weigert et al, 2014 for phylogenetic details, Gustafson, 1930;Wanninger et al, 2005;Purschke and Müller, 2006;Filippova et al, 2010) a plesiomorphic condition has to be assumed for the presence of transverse muscle fibers.…”

A correlative approach for combining microCT, light and transmission electron microscopy in a single 3D scenario

“…The use of specific markers and fluorescent dyes in combination with conventional fluorescence microscopy or confocal laser scanning microscopy (CLSM) allows for assessment of specific tissues or cellular components (e.g. [5]), and microscopic X-ray computed tomography (microCT) allows imaging of the X-ray dense structures of entire specimens (e.g. [6]).…”