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, esophageal pouch; in, intes- tine; (j), jaw (Conchifera only); mg, midgut gland; mo, mouth opening; pe, posterior esophagus; ph, pharynx; pp, pharyngeal pouch; ras, radula sheath; re, rectum; sro, subradular organ; (ss), style sac (Conchifera only); st, stomach; vfg, ventral foregut gland(s). contradicted by the ontogenetic conditions; the splitting of the shell-gland into several secretive fields could only be a developmental malformation in larvae, without any selective advantage functionally. Moreover, should the late Cambrian Matthevia really represent placophorans (as advanced by Runnegar et al., 1979), then the arrangement of their dorsoventral musculature points to a highly specialised organisation (Salvini-Plawen, 1980). This would entail a longer evolution towards the Matthevia configuration and thus support the existence of articulamentum- less Placophora already in the earliest Cambrian, as interpreted ̶ though this is not undisputed ̶ by Yu (1987) or Yates et al. (1992) (see also Eernisse & Reynolds, 1994). The hypothesis that the placophoran stem group was characterized by seven plates only (Heptaplacota) is strongly supported by developmental patterns; though the fossil Septemchiton is a misnomer, it meets the predominant abnormality of seven valves in recent representatives (cf. Salvini-Plawen, 1980, 1991) and would thus classify the Multiplacophora with an articulamentum (Vendrasco et al., 2004) as a paedomorphically derived line. All these conditions would likewise presuppose early Cambrian placophorans and contradict even more the notion of the Placophora as conchiferan descendants. On the other hand, there is no reliable fossil record of aplacophoran molluscs: neither the trace fossil Bunyerichnus nor the conodonts can credibly be attributed to them (cf. Briggs et al., 1987; Salvini-Plawen, 1991), and this is likewise true for the “plated aplacophoran” Acaenoplax (a contradiction in itself; cf. Steiner & Salvini-Plawen, 2001); the recently expressed relationship of Acaenoplax to the Solenogastres (Sutton et al., 2004) refers to the incorrect coding of added characters (the Solenogastres distinctly possess a foot, and their mouth is behind the atrial/preoral sense organ; a pedal gland is likewise present in the Scaphopoda, as an anterior gland in part of the Bivalvia, and as a funnel-gland in the Siphonopoda/cephalopods; Salvini-Plawen, 1972). In the meantime, the earlier hypothesis that the aplacophoran molluscs were derived from the Placophora by regression (Pelseneer, 1890) has been widely rejected (cf. Nierstrasz, 1910; Boettger, 1956; Scheltema, 1996).

The Testaria

Apart from the plesiomorphic aculiferan configuration, the Placophora have several other distinct characters in common with the monophyletic Conchifera (cf. Hyman, 1967; Salvini- Plawen, 1985, 1988a; Eernisse & Reynolds, 1994). These mainly include the midgut axially regionated into an esophagus, a stomach with a paired midgut gland, and a narrowed, somewhat coiled intestine (Fig. 2). Moreover, the esophagus itself is subdivided into an anterior region with special longitudinal folds and ciliary tracts (dorsal “food channel” etc.; Fig. 3) as well Significance of Placophora for Molluscan Phylogeny 5

Fig. 3. Three successive cross sections through the esophagus (after Salvini-Plawen, 1988a). A. Chiton olivaceus Spengler, 1797 (Placophora). B. Nuculana commutata (Philippi, 1844) (Bivalvia- Nuculida). C. Dentalium sp. (Scaphopoda). D. Patina pellucida (Linnaeus, 1758) (Gastropoda- Patellida). E. Emarginula sp. (Gastropoda-Vetigastropoda). Abbreviations: ae, anterior esophagus; df, ciliated dorsal fold/ridge; dfc, dorsal food channel; dt, dorsal ciliary tract; ep, esophageal pouch; pa, papillae; pe, posterior esophagus; rap, radular apparatus; vf, ciliated ventral fold/ridge (in B con- tinuous with the posterior labial palp); vt, ventral ciliary tract. 6 Luitfried v. Salvini-Plawen

Fig. 4. Common esophagus configuration of basal Testaria (cf. Fig. 3) (after Salvini-Plawen, 1988a). A. Cross section through anterior esophagus. B. Cross section through beginning posterior esophagus. Abbreviations: df, ciliated dorsal fold; ep, esophageal pouch; fc, (dorsal) food channel; pe, posterior esophagus; vt, ventral ciliary tract.

Fig. 5. Configuration of the stomach in Placophora (after Salvini-Plawen, 1988). A. Hanleya type. B. Most Chitonida. C. Lepidopleurus type. Abbreviations: dc, “dorsal channel” and “ductus choledochus” respectively; in, intestine; op, opening of midgut gland; pe, posterior esophagus; vs, ventral stomach sac. as with a paired, glandular esophageal pouch, and into a simple posterior esophagus (Salvini- Plawen, 1988a). This demonstrates a similar common basic configuration of the esophagus in the Placophora and Conchifera (Figs. 3, 4). In contrast to the stomach in Placophora (Fig. 5), the differentiation of a style-sac type of stomach appears to be synapomorphic for the Conchifera only (Figs. 6-10). No such threefold axial midgut regionation exists in the aplacophoran molluscs. On the one hand, the carnivorous Solenogastres exhibit a voluminous midgut filling the entire body cavity (where the serial dorso-ventral muscle bundles often cause lateral pouches) except for the dorsal gonads (Fig. 11A), and the entire midgut shows a mid-dorsal ciliary tract. On the other hand, the omni-microvorous Caudofoveata feature a basically identical midgut configuration, though subdivided into an anterior and a posterior portion: the body-filling anterior midgut continues posteriorly to the voluminous midgut sac, from which, however, a narrow dorsal duct is longitudinally (not axially) separated (Fig. 11B; Salvini-Plawen, 1981b, 1988a, 2003). This dorsal midgut duct may represent a former middorsal ciliated tract (occurring in the anterior midgut of some species) which became split off, and does not represent an axially following intestine proper (no threefold regionation). Nourishment (herbivory, microvory, carnivory) and elaboration Significance of Placophora for Molluscan Phylogeny 7

Figs. 6-10. Configuration of the stomach in Conchifera (after Salvini-Plawen, 1988). 6. Basic con- chiferan organisation. 7A. Bivalvia-Nuculida. 7B. Most Bivalvia-Eulamellibrachia. 8. Scaphopoda. 9A. Gastropoda-Fissurellidae. 9B. Gastropoda-Trochoidea. 9C. Microherbivorous Caenogastropoda. 10. Siphonopoda (cephalopods). Abbreviations: ce, caecum; cs, crystalline style; dp, dorsal pouch (hood); gs, gastric shield; ig, intestinal groove; in, intestine; op, opening of midgut gland; pe, poste- rior esophagus; ps, protostyle; ri, ridge (typhlosole); ri1, major typhlosole; ri2, minor typhlosole; sa, sorting area; sc, cecal stomach (cecum); ss, stomach sac. of the alimentary tract are known to be correlated, and comparative analysis shows (Salvini- Plawen, 1988a) that carnivory leads to simplification of the midgut structures (e.g. Scaphopoda, Bivalvia-Septibranchia, Siphonopoda/Cephalopoda, see Figs. 8, 10). It does not eliminate, however, the threefold axial regionation of the midgut. This makes the axially non-regionated midgut in aplacophoran molluscs (probably with a mid-dorsal ciliary tract) a primary condition. The identical regionation of the midgut in Placophora and Conchifera thus clearly points to synapomorphy of sister-groups and reflects a monophyletic taxon defined as Testaria (Salvini- Plawen, 1972; Wingstrand, 1985; Haszprunar & Wanninger, 2000; Mizzaro-Wimmer & Salvini- Plawen, 2001). To further underline the monophyletic Testaria with respect to the alimentary tract, the Placophora and the Tryblidia (recent representatives of the paraphyletic *Monoplacophora*) show an almost identical differentiation of the radular apparatus into a rigid band upon a specialised support (Wingstrand, 1985). This support includes the arrangement and configuration of particular bolsters (a pair of fluid-filled vesicles and pairs of so-called cartilages of turgescent cells; Fig. 12), as well as the complex musculature. Along with the evolutive regionation of the midgut, the radula ̶ in concert with the supporting bolsters ̶ was adapted into a tongue with a limited 8 Luitfried v. Salvini-Plawen

Fig. 11. Aplacophoran molluscs: external aspect of an animal (Solenogastres: Nematomenia bany- ulensis (Pruvot); Caudofoveata: Falcidens sagittigerus S.-Plawen); organisational sketch of alimen- tary tract, gono-pericardial system and mantle cavity; section through midbody according to lines indicated (after Salvini-Plawen, combined). Abbreviations: cg, cerebral ganglion; dvm, dorso-ventral muscle bundles; go, gonad; md, glandular duct (of unknown homology); mg, midgut; mgd, midgut duct; mgs, midgut sac; mt, spawning duct (internalised mucous tract portion of pallial groove); pc, pericardium; pg, pedal gland; ps, pedal shield; so, dorsoterminal or osphradial sense organ. number of teeth (11-17 in each transverse row) that acts as a rasp parallel to the longitudinal axis. Such a stereoglossate radula type is elaborated in the Placophora, Tryblidia, Scaphopoda and Gastropoda-Docoglossa; in contrast, other gastropods are defined as Flexoglossata (Fretter & Graham, 1962: 200-201, 1994: 192-194 & 593; Salvini-Plawen & Haszprunar, 1987; Salvini- Plawen, 1988a). This complex was functionally supplemented by the development of the chemoreceptive subradular organ, present in both the Placophora and the (lower) Conchifera. In aplacophoran molluscs, again no such condition of the radular apparatus and no subradular organ is differentiated (Salvini-Plawen, 1972, 1985, 1988a). A closer relation between the Placophora and the Tryblidia is also supported by the configura- tion of the dorsoventral musculature. Irrespective of the evolutionary sequence, the sixteen pairs of dorsoventral muscles in the Placophora ̶ two pairs each attached to one of the eight valves ̶ directly correspond to the eight pairs of dorsoventral bundles in the Tryblidia. Note also that these latter bundles in Neopilina galatheae Lemche are sometimes still composed of two successive bundles (Fig. 13) and that a portion is still divided (see the mediopedal portion of the VIIth = G bundle in Lemche & Wingstrand, 1959; Salvini-Plawen, 1969, 1981a). In other members the dorsoventral bundles already tend to fuse (Haszprunar & Schaefer, 1997), as in the fossil *Monoplacophora* (e.g. Wingstrand, 1985) or more obviously in the higher Conchifera (Fig. 14). In contrast, the multiplicity of pairs of ctenidia in the Placophora and the Tryblidia does not appear to be homologous. In the Placophora, the increase in number is independent of the internal organisation, showing primitively a merobranchial-posterior, abanal or adanal arrangement (cf. Plate, 1901; Russel-Hunter, 1988; Eernisse & Reynolds, 1994); in the Tryblidia the multiplication is dispersed along the entire mantle cavity and is combined with a seriality of excretory organs (emunctoria) from posterior to anterior (cf. Haszprunar & Schaefer, 1997). These two conditions are not comparable and reflect convergent autapomorphous multiplication within each class, originating from a single pair of ctenidia, the first “post-renal” = “largest” one in Placophora (Pelseneer, 1899; Plate, 1901; Yonge, 1939; Eernisse & Reynolds, 1994). Significance of Placophora for Molluscan Phylogeny 9

Fig. 12. Radula support (ventral view) in Tryblidia (A, B) and Placophora (C, D) (after Wingstrand, 1985). A. Vema ewingi (Clarke & Menzies, 1959). B. Neopilina galatheae. C. Schizoplax sp. D. Leptochiton asellus (Gmelin, 1791). Abbreviations: lc, lateral cartilage; mc, medial cartilage; rv, radula vesicle; va, ventral unpaired horizontal approximator muscle (musculus impar).

The Conchifera as well as the Placophora differentiate their pericardioducts into excretory organs. Whereas all molluscs produce primary urine by ultrafiltration through podocytes at the atrial epithelium of the heart (Andrews, 1988; Reynolds, 1990; Reynolds, Morse & Norenburg, 1993; Morse & Reynolds, 1996; Salvini-Plawen & Bartolomaeus, 1995), only the Placophora and Conchifera transform this into a secondary urine with their altered pericardioducts (Figs. 15, 16). Following the proximal portion at the pericardium (“renopericardial” canals), the central portion of the pericardioducts in Placophora and Conchifera is elaborated to secrete solutes and to reabsorb organic molecules, as well as to abstract resulting waste material. It produces the secondary urine by an emunctorial process and thus represents an excretory organ or emunctorium (“kidney”), with an outleading lower pericardioduct (excretory duct or exit canal, “ureter”). Again, the condition in the aplacophoran molluscs contrasts with that in the Testaria: neither in the Solenogastres nor the Caudofoveata do the pericardioducts serve excretory functions (Fig. 16). In the Caudofoveata a (non-homologous) parallel organ may be present – the enigmatic, voluminous outleading glandular ducts (`md´ in Fig. 16C; Salvini-Plawen, 2003) – thus perhaps performing excretion by an analogous mechanism; in any case, however, this supports the conclusion that 10 Luitfried v. Salvini-Plawen

Fig. 13. Dorso-ventral musculature and nerv- ous system in Neopilina galatheae (Tryblidia) in dorsal view. In this individual the IIIrd bundle C at left is composed of two distinctly separate portions (after Wingstrand, 1985). Abbreviations: A-H, Ist to VIIIth dorso- ventral muscle bundles; bg, buccal ganglion; cg, cerebral ganglion; gi, ctenidium basis; gn, ctenidium nerve; lc, lateral nerve cord; lpc, latero-pedal connective; mop, posterior oral muscle bundle; np, excretory pore; pc, pedal nerve cord; poc, post-oral commissure; r, rec- tum; srg, subradular ganglion; st, statocyst.

Fig. 14. Cladogram of Mollusca with the schematic arrangement of dorso-ventral musculature (after Haszprunar & Wanninger, 2000). Significance of Placophora for Molluscan Phylogeny 11

Fig. 15. Gono-pericardial system of Testaria (Placophora + Conchifera) (after Mizzaro-Wimmer & Salvini-Plawen, 2001, and Salvini-Plawen, 2003). Abbreviations: ao, aorta; aob, bulb of aorta; at, heart auricle; em, emunctorium (excretory organ); exd, lower periocardioduct or excretory duct (“ure- ter”); exs, excretory sac; gd, gonoduct; gdg, gonoduct gland; go, gonad; gpd, gono-pericardial inter- connection; pc, pericardium; pd, upper pericardioduct (“reno”-pericardial canal); ve, heart ventricle. the proper pericardioducts in the common forerunners (archimolluscs) were not excretory organs. In summary, the excretory function of the pericardioducts did not evolve prior to the common ancestors of the Placophora and Conchifera. The monophyly of the Testaria is finally supported by the eponymous ability to produce extensive calcareous mantle secretions, which form two-layered plates, valves or shells covered by a properiostracum or a periostracum respectively (Beedham & Trueman, 1967; Haas, 1981). The “break up” hypothesis includes the direct homology of the eight valves with the concha. The evolutionary sequence, however, is more likely reversed and the homology accepted in a broader sense only: a coalescence of the eight placophoran secretive fields to a shell gland. Such a course of events is supported by the retained eight-part dorso-ventral musculature in the Tryblidia (above). The coalescence was then followed by the formatively and structurally different elaborations evident in the recent clades (Haas, 1981; Eernisse & Reynolds, 1994). The subsequent stages of eight-valved Placophora and of one-shelled Conchifera appear also to be bridged by the Merismoconchia (Yu, 1984, 1987).

The Phylogenetic Significance of the Placophora

All these conditions reflect convincing synapomorphies for the Placophora and Conchifera (rather than parallelisms or convergencies, as expressed in Scheltema, 1996) and argue for a monophyletic taxon defined as the Testaria. The morphological sequence of homologies can, based on the synapomorphies, clearly be defined (along with the mantle cover) as a progressive, anagenetic process from the aplacophoran to the polyplacophoran to the monoplacophoran = conchiferan level (Salvini-Plawen, 1972, 1981a, 1990, 2003; Yu, 1987; Salvini-Plawen & Steiner, 1996; Haszprunar, 2000). This determination of the reading direction (character polarisation) of this sequence agrees fully with the non-regionated configuration of the midgut and the lack of emunctoria (excretory organs) in the aplacophoran classes in contrast to the Testaria. In addition, this is strongly supported by the development of the musculature in the Placophora, which reflects an original “worm-grid” and a concentration of numerous, serially repeated dorsoventral muscles (Haszprunar & Wanninger, 2000; Wanninger & Haszprunar, 2002). The character polarisation also corresponds to a concentration of dorsoventral bundles from an indefinitely serial arrangement in the aplacophoran level to the sixteen bundles in the Placophora and to the 8-1 pairs of bundles 12 Luitfried v. Salvini-Plawen

Fig. 16. Relation of pericardium, pericardioducts and mantle cavity (after Salvini-Plawen, 2003). At left schematic views from lateral, at right schematic oblique cross sections (as indicated at left) projected from behind. A. Placophora. B. Solenogastres (no ctenidia). C. Female Caudofoveata. Abbreviations: ct, ctenidium; em, emunctorium (excretory portion of pericardioduct); go, gonad; md, glandular duct (of unknown homology); ml, enrolling muscle (not homologous in adults); mt, mucous tract of pallial groove/mantle cavity (black); pc, pericardium; pd, pericardioduct; re, rectum; so, osphradial sense organ. Significance of Placophora for Molluscan Phylogeny 13

Fig. 17. The intermediate position of Placophora, bridging aplacophoran and conchiferan Mollusca.

in the various fossil and recent Conchifera (Fig. 14; cf. Salvini-Plawen, 1969, 1972, 1981a; Haas, 1981; Yu, 1987; Wanninger & Haszprunar, 2002). With respect to the archimolluscan configuration, however, it remains unclear whether the lack of true gonoducts in the Solenogastres and in the Caudofoveata represents a plesiomorphic condition (“progenesis” in Scheltema, 1993, 1996) or merely convergent apomorphic suppressions (“losses”) as an adaptation to the narrowing of the body (Solenogastres) or to the worm-like shape (Caudofoveata). On the other hand, the molluscan excretory organs definitely represent novelties within the phylum and are an apomorphy for the Testaria; morphologically and phylogenetically these emunctoria are by no means related to “metanephridia” (in coelomate spiralians) or “kidneys” (in vertebrates). Though the aplacophoran level is more primitive than the placophoran-conchiferan (testarian) level, the question which of the recent classes Solenogastres or Caudofoveata, represents the sister-group of Placophora remains open (Fig. 17; Salvini-Plawen & Steiner, 1996; Salvini- 14 Luitfried v. Salvini-Plawen

Plawen, 2003). Data on molecular sequences demonstrate that the aplacophorans are diphyletic (e.g. Okusu & Giribet, 2003; Okusu et al., 2003; Passamaneck et al., 2004), but they unfortunately fail to provide any reliable hint on this issue. Considering the alimentary tract, especially the radula (Salvini-Plawen, 2003), as well as certain other characters, the Solenogastres could well represent the earliest offshoot within the Mollusca (Fig. 14). Because the Solenogastres lack ctenidia, however, in this case we cannot definitively state whether the original molluscs (archimolluscs) already possessed ctenidia, as is generally assumed (Fig. 1 B) ̶ and even less so if the aplacophoran Mollusca are regarded to be monophyletic (e.g. Scheltema, 1996). Apart from their particular autapomorphies, the organisation of the Placophora clearly points to one main phylogenetic conclusion: the Placophora play a key role in bridging the conservative aplacophoran and the derived conchiferan evolutionary levels within molluscs (Fig. 17). With regard to the seriality (as expressed by the eight shell plates and the correspondingly arranged dorsoventral musculature), this reflects the aut-adaptive level of placophorans within molluscan evolution, and not purportedly “segmented” ancestors (cf. Russel-Hunter, 1988; Salvini-Plawen, 1988b; Haszprunar & Wanninger, 2000; Wanninger & Haszprunar, 2002; Friedrich et al., 2002).

Acknowledgements

The author wishes to thank Dr. Hiroshi Saito (National Science Museum, Tokyo) and his colleagues for inviting him to the 2nd Chiton Symposium, and he is very grateful to Dr. Michael Stachowitsch (Institute of Ecology, University of Vienna) for polishing the English text.

References

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(Received April 1, 2004 / Accepted December 17, 2004) Significance of Placophora for Molluscan Phylogeny 17

軟体動物系統発生における多板類の重要性

L. v. サルビニ‐プラウエン

要 約

多板綱の体制を介殻類や，無板類の溝腹綱・尾腔綱の体制と比較した。この比較研究は消化管構造の 分化の程度や排泄器官の構造について特に注目して行なった。 多板綱は枝状器官の発達，多数の鰓，殻板の独特な分化，歯舌歯の鉱物化，卵殻突起の形成，精子の 特別な構造などの固有派生形質をもつ単系統群である。 多板綱は無板類との間に次のような共有形質をもつ：キチン質のクチクラ層と，小棘や鱗片など石灰 質の構造物（スクレライト）を生成する外套膜，側神経の直腸上連合，囲心腔背部が陥入してできる心 臓（心室），繊毛の構造，おそらく腹側の縦走筋など。 他方，多板綱は介殻類との間に次のような共有形質をもつ：中腸が長軸方向に 3 区分されること，す なわち食道，中腸腺が付属した胃，多少なりとも旋回する細い腸が区分されること。食道も特別な縦襞 と繊毛帯をもつ前部と，腺の分布する対になった食道嚢部，および単純な後部食道に区分される。さら に消化管に関する顕著な共有形質は多板綱と単板類（Tryblidia）との間に見られるほとんど同一の歯舌保 持器官である。この両者の近縁な関係は連続する背腹筋の形状・配置によっても支持される。もうひと つの重要な共有形質として，多板綱と介殻類は囲心管（pericardioducts）を “腎臓” に分化させているこ とがあげられる。すべての軟体動物は心室の上皮にある足細胞による限外濾過によって原尿を作るが， 多板綱と介殻類だけがその変化させた囲心管によって原尿から（二次的な）尿を作り出す。 これらの形質を比較研究した結果，多板綱は単板綱と近い類縁関係にあるのみならず，介殻類とともに 単系統群 Testaria として認識されることを明らかにした。無板類と多板綱のみに共有される形質は共有派 生形質ではなく共有原始形質と考えられる。 これまでのいくつかの仮説に反して，多板綱は介殻類から派生した（すなわち１枚の貝殻が８枚に分 割された）とは考えられず，無板類から，多板綱，そして単板綱へと向かう向上進化的な過程で出現し たと考えられる。したがって多板綱の体制は原始的な無板類レベルからより派生的な介殻類レベルへの 系統発生上の掛け橋としての役割を演じたと考えられる。