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The Significance of the Placophora for Molluscan Phylogeny*

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The Significance of the Placophora for Molluscan Phylogeny* VENUS 65 (1-2): 1-17, 2006 Review The Significance of the Placophora for Molluscan Phylogeny* Luitfried von Salvini-Plawen Institut für Zoologie der Universität Wien, Althanstr. 14, A-1090 Wien, Austria; [email protected] Abstract: The organisation of the Placophora is compared with that of the Conchifera and of the aplacophoran Solenogastres and Caudofoveata. This analysis, with special emphasis on the threefold regionated alimentary tract and the excretory system, not only reveals a close relationship of the Placophora with the Tryblidia (part of paraphyletic *Monoplacophora*), but also recognises that the Placophora and Conchifera represent a monophyletic group of Testaria. Synorganisationally, other characters shared (as *Aculifera*) only with the aplacophoran molluscs represent plesiomorphies rather than synapomorphies. In contrast to some earlier assumptions, the Placophora cannot be regarded as being derived from the conchiferan level; rather, there is a well-defined organisational sequence of gradually additive characters (anagenesis) from the a-placophoran to the poly-placophoran and to the mono-placophoran (conchiferan) configuration. The organisation of the Placophora thus plays a key role in bridging the conservative aplacophoran and the derived conchiferan evolutionary levels within molluscs. Keywords: Polyplacophora, Testaria, synapomorphies, plesiomorphies, digestive tract, excretory organ Introduction The Mollusca are characterised by several common organ systems (synapomorphies): Externally there is a dorso-ventral dominance with a ventral or pedal surface (foot), a calcium- carbonate producing dorsal epithelium or pallium (mantle), and a space roofed by some mantle portion (mantle groove or cavity) generally housing ventilatory/respiratory organs (ctenidia), mucous tracts (or hypobranchial glands), osphradial sense organs and the body outlets; characteristic internal features include the radula of the ventral foregut, paired dorsoventral muscle bundles (the lateral-outer portions intercrossing midventrally; e.g. Fig. 11) between mantle and foot, a tetraneurous nervous system, and a gono-pericardial complex with outlets, the complex including the heart as a motor for the open haemolymph system and as the site for ultrafiltration into the pericardium. The ecological and morphological adaptations have led to an enormous diversity recognised in eight recent classes. Based on the respective quantitative occurrence and anthropo-centric importance of these classes, however, our state of knowledge regarding them differs considerably. With regard to the fossil record as well as to the familiarity of terrestrial, limnic and coastal faunas, the Gastropoda and Bivalvia have long been the main focus of investigation and the source of phylogenetic hypotheses; this has culminated in the traditional acceptance that the “generalised” molluscan organisation distinctly reflects the conchiferan configuration (Fig. 1A). *Invited paper to the special number of Venus for the 2nd International Chiton Symposium, Tsukuba 2 Luitfried v. Salvini-Plawen Fig. 1. Range of basic molluscan organisation with respect to the significance of Placophora for phylogeny. A. An exemplified, traditional, Conchifera-dominated view of a “generalised mollusc” in textbooks, here with threefold axially regionated midgut (Testaria only), shell (Conchifera only) and vetigastropod mantle cavity (gill membrane, site of osphradium) (after Barnes in Ruppert et al., 2004). B. Most likely molluscan archetype according to current knowledge of comprehensive plesio- morphies (after Salvini-Plawen, 1991). Abbreviations: ce, cerebral ganglion; co, latero-ventral con- nective; ct, ctenidium; fg, ventral foregut gland; gd, gonoducal gutter (ciliary tracts or gonoducts?); go, gonad (separate sexes); lo, muco-ciliary gliding organ; ma, mantle (covered with chitinous cuti- cle and scaly aragonite sclerites); mc, mantle cavity; mdv, dorso-ventral musculature; mg, midgut; mo, mouth opening; nce, cerebral nerves; nsb, buccal nervous system; nsl, lateral nerve cord; nsv, ventral nerve cord; pc, pericardium; pd, pericardioduct; ph, pharyngeal glands; ra, radula; re, rectum; sd, dorsal blood sinus; sg, sole glands; so, terminal (osphradial) sense organ; src, supra-rectal com- missure; ve, heart ventricle. The conchiferan groups clearly dominate the molluscan fauna. Due to their common characters ̶ the two-layered concha, the head appendages, the statocysts and subrectal commissure, the jaw and the particular differentiation of the stomach (Figs. 6-10) ̶ they represent a well-defined monophyletic group (Salvini-Plawen, 1988a; Salvini-Plawen & Steiner, 1996; Haszprunar, 2000). Any modern approach, however, must consider the organisations of all molluscan classes as equivalently important for reconstructing phylogenetic relationships, irrespective of species number and of familiarity. Apart from the Placophora, the inclusion and consideration also of the Significance of Placophora for Molluscan Phylogeny 3 small and less familiar Solenogastres (Neomeniomorpha) and Caudofoveata (Chaetodermomorpha) yields a quite different evaluation of evolutionary pathways (cf. Salvini-Plawen, 1972, 1981a, 1991; Haszprunar, 1992), resulting in a small, aplacophoran archetype of Mollusca (Fig. 1B). The Relationships of Placophora The Placophora (Polyplacophora, Loricata; chitons) represent a class with distinct autapomorphies such as the development of aesthetes, the multiplication of ctenidia (see below), the particular differentiation of the valves including an articulamentum as a subdivision of the inner shell layer (Bergenhayn, 1930), the type of mineralization of the radular teeth, the extracellular egg hull formations and the particular sperm morphology (see Eernisse & Reynolds, 1994). Among extant representatives, both morphological characters and molecular analyses point to the Lepidopleurida as having retained the most conservative traits (Sirenko, 1993; Buckland- Nicks, 1995; Okusu et al., 2003). Nonetheless, the monophyletic Placophora share (as paraphyletic *Aculifera*) several characters with the aplacophoran molluscs. The most obvious character is the mantle, which in Placophora exhibits a peripheral area ̶ the perinotum or girdle ̶ that produces a chitinous cuticle and sclerites. This condition is identical with the entire mantle cover in Solenogastres and in Caudofoveata (Haas, 1981). Additional shared characters include the supra-rectal commissure of the lateral nerve cords, the heart-ventricle as a mid-dorsal invagination of the pericardium, the organisation of the ciliary apparatus, and possibly the paired ventral longitudinal muscle the animals use to roll up (Pelseneer, 1899; Salvini-Plawen & Bartolomaeus, 1995; Lundin & Schander, 2001; Wanninger & Haszprunar, 2002; Salvini-Plawen, 2003). The heart-ventricle and the ciliary apparatus distinctly point to plesiomorphies (Pelseneer, 1899; Salvini-Plawen & Bartolomaeus, 1995; Lundin & Schander, 2001), as does the mantle cover of cuticle and sclerites (Beedham & Trueman, 1967, 1968; Haas, 1981). The supposition of Scheltema et al. (2003) of a plesiomorphic biserial/distichous type of radula, however, cannot be supported: the investigated Solenogastres-Simrothiellidae (Helicoradomenia) represent a derived group (Salvini-Plawen, 2003) and their radula apparatus contrasts with the more conservative monoserial type of radula (cf. Salvini-Plawen, 1988a, 2003; Wolter, 1992). The configuration of the pallial cavity in all three classes (Fig. 16) demonstrates their mutual evolutionary connection (mucous tract portion of the mantle grooves) and likewise renders their common level more primitive in contrast to Conchifera; on the other hand it underlines the diphyletic evolutionary adaptation in Solenogastres and Caudofoveata (cf. Hoffman, 1949; Salvini-Plawen, 2003; in contrast to e.g. Scheltema, 1993, 1996). Together with the lack of statocysts, jaw formations and head appendages, these aculiferan characters express a conservative level within the Mollusca. Acoelomate organisms with spiral cleavage, a muco-ciliarily gliding organ for locomotion, a non-regionated midgut (see below) and a likewise chitinous cuticle point to Kamptozoa larvae as a possible sister-group of molluscs, united as the “Lacunifera” by Ax (1999; cf. Haszprunar, 1996; Salvini-Plawen, 2003). The absence of other suitable non-molluscan outgroups with comparable organisation makes the direct evaluation of further plesiomorphies difficult. The differentiation of calcareous scales in the basement membrane of some Platyhelminthes (cf. Rieger & Sterrer, 1975) should be mentioned, however, and points to a principal ability of “lower worms” to produce aragonitic spicules (see also Willmer, 1990). For a long time, the fossil record of the Placophora stratigraphically supported the idea that this group derived from the Conchifera by regression, with a shell broken up into eight valves (e.g. Yonge, 1939: 386; Fretter & Graham, 1962: 8; Runnegar & Pojeta, 1985: 46). This interpretation includes the principal homology of the eight valves with the concha (see below). Apart from the functional evolutive difficulties of such a “break up”-hypothesis (e.g. Haas, 1981), it is 4 Luitfried v. Salvini-Plawen Fig. 2. Axial regionation of the midgut in Testaria (Placophora + Conchifera) (after Mizzaro- Wimmer & Salvini-Plawen, 2001, Salvini-Plawen, 2003). Abbreviations: ae, anterior esophagus; (cr), crop (Conchifera only); dfg, salivary gland(s); eg, esophageal gland; ep,
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