Nervous and muscle system development in Phascolion strombus (Sipuncula)

Abstract

Recent interpretations of developmental gene expression patterns propose that the last common metazoan ancestor was segmented, although most animal phyla show no obvious signs of segmentation. Developmental studies of non-model system trochozoan taxa may shed light on this hypothesis by assessing possible cryptic segmentation patterns. In this paper, we present the first immunocytochemical data on the ontogeny of the nervous system and the musculature in the sipunculan Phascolion strombus. Myogenesis of the first anlagen of the body wall ring muscles occurs synchronously and not subsequently from anterior to posterior as in segmented spiralian taxa (i.e. annelids). The number of ring muscles remains constant during the initial stages of body axis elongation. In the anterior-posteriorly elongated larva, newly formed ring muscles originate along the entire body axis between existing myocytes, indicating that repeated muscle bands do not form from a posterior growth zone. During neurogenesis, the Phascolion larva expresses a non-metameric, paired, ventral nerve cord that fuses in the mid-body region in the late-stage elongated larva. Contrary to other trochozoans, Phascolion lacks any larval serotonergic structures. However, two to three FMRFamide-positive cells are found in the apical organ. In addition, late larvae show commissure-like neurones interconnecting the two ventral nerve cords, while early juveniles exhibit a third, medially placed FMRFamidergic ventral nerve. Although we did not find any indications for cryptic segmentation, certain neuro-developmental traits in Phascolion resemble the conditions found in polychaetes (including echiurans) and myzostomids and support a close relationship of Sipuncula and Annelida.

Is Diurodrilus an annelid?

“…The configuration of the widely separated main, lateral, and paramedian longitudinal ventral nerves of the trunk largely resembles what is found in many small elongated taxa and larvae (Mü ller and Sterrer, 2002;Mü ller and Westheide, 2002;Voronezhskaya et al, 2002;Wanninger et al, 2005Wanninger et al, , 2007; see also Table 3). However, the ventral nerves of Diurodrilus differ from those of the annelids in the presence of distinct paramedian ciliophore nerves in the ventral head as well by the lack of a midventral nerve.…”

“…However, the location of the anterior commissures in Diurodrilus, as well as a crossover of nerves between the two pairs of perikarya (tpk1, tpk4) do resemble what is described for the trochophore larvae of Ophryotrocha gracilis and Dinophilidae (Mü ller and Westheide, 2002). Seriality of the nervous system to a much greater extent than that of Diurodrilus is found in all proposed annelids so far, including larvae of Echiura (Hessling and Westheide, 2002) and the ''unsegmented'' Sipuncula that also possesse a midventral nerve (Wanninger et al, 2005).…”

“…The organization of the musculature and nervous system is often regarded as a key indicator of phylogenetic affinity among protostomes (Raikova et al, 1998;Hessling and Westheide, 2002;Wanninger et al, 2005). We document here the nervous system as well as the musculature of several Diurodrilus species using confocal laser scanning microscopy (CLSM) and transmission electron microscopy (TEM).…”

Re-evaluating the phylogeny of Sipuncula through transcriptomics

“…Third, sipunculans are valuable research organisms for reproductive biology (Rice, 1973(Rice, , 1989(Rice, , 1993Reunov and Rice, 1993;Adrianov and Maiorova, 2010), comparative development (Åkesson, 1958;Rice, 1967Rice, , 1975Rice, , 1988Schulze and Rice, 2009a) and life history character reconstruction and evolution (Jägersten, 1972;Rice, 1976Rice, , 1985. They are also emerging as important non-model organisms for evolutionary and developmental biology, or evo-devo (Schulze and Rice, 2009b;Wanninger et al, 2005Wanninger et al, , 2009Wanninger, 2008;Boyle and Seaver, 2010;Boyle and Rice, 2014). Fourth, due to an extended larval phase described for several species within multiple families Hall, 1965, 1975;Rice, 1976Rice, , 1981Scheltema and Rice, 1990), sipunculans constitute an interesting group for studying dispersal within and between widely separated oceanic regions, which is a topic addressed in several recent studies of cosmopolitanism in the marine realm (Staton and Rice, 1999;Kawauchi and Giribet, 2010;Kawauchi and Giribet, 2013;Schulze et al, 2012;Young et al, 2012;Lemer and Planes, 2014).…”

Systematics, evolution and phylogeny of Annelida – a morphological perspective

“…Irrespective of the taxa included, the state of almost every character considered varies greatly among annelids making ground pattern reconstruction a difficult task. Although there is general agreement that Annelida are organisms with a multiple repetition of identically organised segments Struck, 2011;Hannibal and Patel, 2013), there are certain taxa in which even this so-called key-character is virtually absent: e.g., Echiura, Sipuncula, Diurodrilus Wanninger et al, 2005;Worsaae and Rouse, 2008;Nielsen, 2012;Golombek et al, 2013). The number of segments varies between species and may comprise between only 6 or fewer (e. g. Parapodrilus psammophilus Westheide, 1965) to more than 1,000 segments (e. g. Eunice aphroditois (Pallas, 1788)) resulting in body lengths varying from less than 600 µm to about 6 m (see Paxton, 2000).…”