Developmental dynamics of myogenesis in the shipworm Lyrodus pedicellatus (Mollusca: Bivalvia)

Abstract

BackgroundThe shipworm Lyrodus pedicellatus is a wood-boring bivalve with an unusual vermiform body. Although its larvae are brooded, they retain the general appearance of a typical bivalve veliger-type larva. Here, we describe myogenesis of L. pedicellatus revealed by filamentous actin labelling and discuss the data in a comparative framework in order to test for homologous structures that might be part of the bivalve (larval) muscular ground pattern.ResultsFive major muscle systems were identified: a velum retractor, foot retractor, larval retractor, a distinct mantle musculature and an adductor system. For a short period of larval life, an additional ventral larval retractor is present. Early in development, a velum muscle ring and an oral velum musculature emerge. In late stages the lateral and dorsal mantle musculature, paired finger-shaped muscles, an accessory adductor and a pedal plexus are formed. Similar to other bivalve larvae, L. pedicellatus exhibits three velum retractor muscles, but in contrast to other species, one of them disappears in early stages of L. pedicellatus. The remaining two velum retractors are considerably remodelled during late larval development and are most likely incorporated into the elaborate mantle musculature of the adult.ConclusionsTo our knowledge, this is the first account of any larval retractor system that might contribute to the adult bodyplan of a (conchiferan) mollusk. A comparative analysis shows that a pedal plexus, adductors, a larval velum ring, velum retractors and a ventral larval retractor are commonly found among bivalve larvae, and thus most likely belong to the ground pattern of the bivalve larval musculature.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-014-0090-9) contains supplementary material, which is available to authorized users.

Evolution of the molluscan body plan: the case of the anterior adductor muscle of bivalves

“…2B, B 0 ). This muscle topologically corresponds to the anlage of the pedal plexus in Lyrodus pedicellatus (Wurzinger-Mayer et al, 2014). At 48 hpf, another muscle is newly detected at the posterior end of the ventral larval retractor.…”

“…Since the description of the early development of Cerastoderma edule (Heterodonta: Cardiidae), the embryology of bivalves has been studied using microscopic observation and immunochemistry (Lov en, 1848;Hatschek, 1880;Meisenheimer, 1901;Cole, 1938;Creek, 1960;Allen, 1961;Cragg, 1985;Kakoi et al, 2008;Dyachuk & Odintsova, 2009;Wurzinger-Mayer et al, 2014). A classical microscopic study by Lillie (1895) reported that the adductor muscles, as well as the larval retractor muscles, of the freshwater clam Lasmigona complanata (Palaeoheterodonta: Unionidae) develop from ectomesoderm cells.…”

“…They did not examine the details of anterior adductor formation, however. Although Wurzinger-Mayer et al (2014) described myogenesis in Lyrodus pedicellatus (Heterodonta: Teredinidae), they began their observations at a stage when most larval retractor muscles and the anterior adductor muscle have already appeared. Therefore, the development of the anterior adductor muscle remains obscure.…”

Neuromuscular development in Patellogastropoda (Mollusca: Gastropoda) and its importance for reconstructing ancestral gastropod bodyplan features

“…kogamogai but also in other gastropods, bivalves, polyplacophorans, solenogastres, and caudofoveates as well as in annelids and entoprocts (e.g. Page 2002b; Wanninger and Haszprunar 2002a;Nielsen et al 2007;Wollesen et al 2008;Dyachuk and Odintsova 2009;Evans et al 2009;Wanninger 2009;Page and Ferguson 2013;Scherholz et al 2013;Wurzinger-Mayer et al 2014;Merkel et al 2015). The absence of such a prototrochal muscle ring in Scaphopoda suggests, once again, a secondary loss (Wanninger and Haszprunar 2002b).…”

“…Bivalve and gastropod larvae show striking similarities in their larval musculature such as the velum retractor muscles and the prototroch or velum muscle ring. In general, the larval retractor muscles are striated, insert posteriorly at the inner shell, project into the velum, foot or mantle, and in almost all cases degenerate during metamorphosis (Degnan et al 1997;Page 1998;Wanninger et al 1999a;Wollesen et al 2008;Dyachuk and Odintsova 2009;Kristof and Klussmann-Kolb 2010;Page and Ferguson 2013;Wurzinger-Mayer et al 2014). The muscle ring that underlies the prototroch or velum is not only found in the patellogastropod L. cf.…”