Larval convergence in a colonial tunicate: the organization of the sarcotubular complex in Ecteinascidia turbinata (Perophoridae, Phlebobranchiata, Tunicata, Chordata)

Abstract

Ecteinascidia turbinata is a colonial ascidian that as an adult shares characters with phlebobranch ascidians, whereas the larvae are similar to aplousobranch ascidian larvae. The sarcotubular complex consists of invaginations of the sarcolemma that contact the sarcoplasmatic reticulum via dyads or triads. If present, the invaginations of the sarcolemma in tunicates have been characterized as laminar or tubular. We comparatively investigated the sarcotubular complex of E. turbinata and seven other tunicate species using 3D-reconstruction techniques based on electron micrographs of serial sections. The mononucleate muscle cells in E. turbinata possess intermediate and close junctions and contain several layers of peripheral myoWbrillae. The myoWbrillae are surrounded by continuous cisternae of the sarcoplasmic reticulum that forms interconnected rings around the z-bands. The invaginations of the sarcolemma are laminar, contacting the sarcoplasamatic reticulum at the height of the z-bands via dyads and triads. We present a clear deWnition of character states encountered in Tunicata: laminar invaginations are characterized by a width to length ratio of smaller than 1:20, tubular invagination by a width to length ratio of larger than 1:10. Laminar invaginations are found in stolidobranch ascidians and E. turbinata. Tubular invaginations are present in aplousobranch ascidians and appendicularians. This character state distribution across taxa supports the hypothesis that E. turbinata should be included in Phlebobranchiata as suggested by adult characters and that the larval similarities with Aplousobranchiata arose by convergent evolution.

Anatomy of the trunk mesoderm in tunicates: homology considerations and phylogenetic interpretation

“…This similarity in ontogenetic derivation in addition to the similar position lateral to the central skeletal element, the dorsal neural tube, and the ventral endodermal strand, supports the idea that the tail musculature is homologous across the chordate taxa (Conklin 1905;Kowalevsky 1866). However, while this hypothesis of homology is generally accepted (Ax 2001;Barrington 1965;Nielsen 1997Nielsen , 2001 and has been explored in detail (Nishino and Satoh 2001;Stach 2007;Stach and Kirbach 2008), more detailed homology hypotheses regarding further levels of mesoderm organization are not supported. For example, no diVerentiation in fast and slow muscle Wbers exists in tunicates.…”

“…Fig. 9 Phylogenetic relationships of tunicate taxa modiWed after Stach (2007) and Stach and Kirbach (2008). Apomorphic character states are mapped onto the lineages, on which they originated n.n.…”

“…d Electron micrograph of mesenchyme cells. at Atrium, cns central nervous system, en endoderm, ep epidermis, Xm Xoccular material, gs gill slit, mi mitochondrion, ms mesoderm, mu muscle cell(s), nc notochord, ns nervous system, nt neural tube, no nucleolus, nu nucleus, rer rough endoplasmic reticulum, sv sensory vesicle, tu tunic that in turn consists of mononucleated muscle cells that diVer in ultrastructure (Burighel et al 1977;SchiaYno et al 1976;Stach and Kirbach 2008) but that never form somites that fulWll the deWning criteria of chordate somites as clearly proposed by Ruppert (1997a). The second part of the tunicate tadpole mesoderm is found in the trunk of tadpole stages.…”

The postanal tail of the enteropneust Saccoglossus kowalevskii is a ciliary creeping organ without distinct similarities to the chordate tail

“…8; see e.g. Conklin 1905Conklin , 1932Kowalevsky 1866;Stach 2007;Stach and Kirbach 2009), all of which have a specific ontogenetic fate and origin (Nishida 1986(Nishida , 1987Shimeld and Holland 2000;Stach 2000;Nishida and Sawada 2001;Kuratani et al 2002;Stach et al 2008). As a central skeletal element the A C D B Fig.…”

Chordate phylogeny and evolution: a not so simple three‐taxon problem

“…This space is called myocoel (Ruppert, 1997 a ; Stach, 2000). No such space exists in tunicates, even in animals with many muscle cells (Burighel & Cloney, 1997; Stach & Kirbach, in press). While there are also reports that a sclerocoel is present in cephalochordates (Franz, 1925; Prenant, 1936; Ruppert, 1997 a ), based on ultrastructural evidence, these reports were phrased very carefully as preliminary (Ruppert, 1997 a ) and could not be detected in the electron microscopic investigation of earlier development (Hirakow & Kajita, 1994; Stach, 1999).…”