4

Solenogastres, Caudofoveata, and Polyplacophora

Christiane Todt, Akiko Okusu, Christoffer Schander, and Enrico Schwabe

SOLENOGASTRES The phylogenetic relationships among the molluscan classes have been debated for There are about 240 described species of decades, but there is now general agree- Solenogastres (Figure 4.1 A–C), but many more ment that the most basal extant groups are are likely to be found (Glaubrecht et al. 2005). the “aplacophoran” Solenogastres (ϭ Neo- These animals have a narrow, ciliated, gliding meniomorpha), the Caudofoveata (ϭ Chae- sole located in a ventral groove—the ventral todermomorpha) and the Polyplacophora. fold or foot—on which they crawl on hard or Nevertheless, these relatively small groups, soft substrates, or on the cnidarian colonies especially the mostly minute, inconspicuous, on which they feed (e.g., Salvini-Plawen 1967; and deep-water-dwelling Solenogastres and Scheltema and Jebb 1994; Okusu and Giribet Caudofoveata, are among the least known 2003). Anterior to the mouth is a unique sen- higher taxa within the Mollusca. sory region: the vestibulum or atrial sense Solenogastres and Caudofoveata are marine, organ. The foregut is a muscular tube and usu- worm-shaped animals. Their body is covered by ally bears a radula. Unlike other molluscs, the cuticle and aragonitic sclerites, which give them midgut of solenogasters is not divided in com- their characteristic shiny appearance. They have partments but unifi es the functions of a stom- been grouped together in the higher taxon Aplac- ach, midgut gland, and intestine (e.g., Todt and ophora (e.g., Hyman 1967; Scheltema 1988, Salvini-Plawen 2004b). The small posterior 1993, 1996; Ivanov 1996), but this grouping is pallial cavity lacks ctenidia. The smallest soleno- viewed as paraphyletic by others (e.g., Salvini- gasters measure less than a millimeter in body Plawen 1972, 1980, 1981b, 1985, 2003; Salvini- length (e.g., Meiomenia swedmarki, Meioherpia Plawen and Steiner 1996; Haszprunar 2000; atlantica), whereas the largest species are more Haszprunar et al., Chapter 2). than 30 cm long (e.g., Epimenia babai) and

71 FIGURE 4.1. Living specimens of Solenogastres (A, B, C), Caudofoveata (D), and Polyplacophora (E). (A) Epimenia n. sp., from Japan, on its gorgonian prey, scale bar: 1 cm; there are blue patches on the dorsal mantle surface. From Okusu 2003. (B) Specimens of Wirenia argentea from Galicia (Spain) (micrograph by V. Urgorri), scale bar: 1.5 mm. (C) Biserramenia psammobionta from Galicia (Spain); note the long epidermal spicules of this interstitial animal (micrograph by V. Urgorri), scale bar: 0.25 mm. (D) Prochaetoderma sp. from Galicia, Spain; note the terminal knob with fringe of long, pointed sclerites at the posterium (micrograph by V. Urgorri), scale bar: 0.5 mm. (E) Acanthopleura gemmata, Sulawesi, Indonesia; with long hair-like projections covering the girdle; photo taken in the animal’s natural habitat. often colorful (Okusu 2003). There are a num- some comprehensive studies that focused on ber of overviews of solenogaster morphology the histology of the integument (Hoffman 1949) (e.g., Thiele 1913; Hoffmann 1930; Hyman 1967; or the histology or physiology of the digestive Salvini-Plawen 1971, 1978, 1985) and microscopic tract (Baba 1940a; Salvini-Plawen 1967, 1981a, anatomy (Scheltema et al. 1994), and there are 1988; Scheltema 1981).

72 solenogastres, caudofoveata, and polyplacophora CAUDOFOVEATA like fossil taxa. The general morphology of Polyplacophora, with some information on In Caudofoveata, a ventral groove and foot are histology, was described by Plate (1897, 1901), lacking (Figure 4.1D). The mouth opening is Hyman (1967), Kaas and Van Belle (1985), and partly or entirely surrounded by an oral shield Wingstrand (1985). Information on their micro- (foot shield), an area covered by a thick layer scopic anatomy was compiled by Eernisse and of cuticle without sclerites. Caudofoveates are Reynolds (1994). These animals, commonly infaunal and feed on detritus or selectively referred to as chitons, are dorsoventrally fl at- on foraminiferans by burrowing in the mud tened, exclusively marine molluscs character- with their oral shield. They have a muscular ized by the presence of eight dorsal aragonitic foregut bearing a radula, and their posterior shell plates (valves) and a broad ventral ciliated midgut is divided into a dorsal tubular region foot (Figures. 4.1E, 4.6A). The likewise ventrally (midgut duct) and a ventral midgut sac. The positioned head is separated from the foot by a small, posterior pallial cavity bears a pair of true transverse groove. Surrounding the dorsal shell ctenidia. Caudofoveates range in length from plates—or even completely engulfi ng them in a few millimeters (e.g., Prochaetoderma radu- some species—there is a thick marginal girdle liferum; Falcidens sterreri) to 14 cm (e.g., Chae- (perinotum) covered by a chitinous cuticle. toderma productum). Three major body regions Embedded in this cuticle are calcium carbon- are defi ned: anterium, trunk, and posterium. ate sclerites (Figure 4.6B), which are only occa- The latter may consist of a narrow shank and sionally lacking, and sometimes the cuticle a terminal knob with characteristic elongate additionally bears corneous processes (e.g., in sclerites (typical for Prochaetodermatidae). With Chaetopleura). The shell plates display a complex very few exceptions (e.g., Chaetoderma rubrum), morphology and are composed of four layers: caudofoveates are beige to brownish in color. properiostracum, tegmentum, articulamentum, About 120 species have been described so far and myostracum. The articulamentum projects (Glaubrecht et al. 2005). In caudofoveates, aside anteriorly and laterally beyond the tegmen- from the sometimes highly specialized radula, tum to form the sutural laminae and insertion the variation in structure and arrangement of plates. The shell plates characteristically bear internal organs is limited, and knowledge of so-called aesthetes, unique photo- and probably internal anatomy is mostly based on older stud- also mechano- and chemosensoric organs and ies (e.g.,Wirén 1892; Thiele 1913; Hoffmann in certain taxa ocelli (Figure 4.6C). The head in 1930; van Lummel 1930; Hyman 1967; Salvini- general lacks eyes and tentacles, but the mouth Plawen 1971, 1975, 1985; Scheltema et al. 1994). opening is laterally fl anked by mouth lappets. Occasionally (e.g., in the genus Placiphorella) POLYPLACOPHORA precephalic tentacles, which support the animal The monophyly of Polyplacophora has been well while feeding, may occur. The mantle cavity or established (most recently Okusu et al. 2003), pallial groove surrounds the foot and accom- even if in a recent molecular analysis a spe- modates the terminal anal papilla, a multi- cies of monoplacophoran appears to be nested tude of laterally positioned ctenidia, the paired within the chitons (Giribet et al. 2006). The osphradium, and lateral sense organs. Chitons name Polyplacophora dates back to Gray (1821), have complex muscle systems, including eight but the term Placophora, which was fi rst used paired sets of dorsoventral muscle units that by von Ihering (1876), is common, too, espe- insert at the shell plates, the musculus rectus, cially in German literature. The latter term is which runs longitudinally underneath the shell also used informally (e.g., Lindberg and Ponder plates, and a circular enrolling muscle. Usually 1996; Parkhaev, Chapter 3) to encompass the chitons are grazers with a broad and exception- Aplacophora, Polyplacophora, and mollusc- ally long stereoglossate radula (Figure 4.6D).

solenogastres, caudofoveata, and polyplacophora 73 FIGURE 4.2. Alternative phylogenies for the placement of Solenogastres, Caudofoveata and Polyplacophora relative to Conchifera. (A). Aplacophora and Testaria as sister groups (after Waller 1998). (B) Aplacophora as Monophylum, Amphineura (Aculifera) sister group to Conchifera (after Ivanov 1996; Scheltema 1996). (C) Solenogastres and Caudofoveata as independent clades with Solenogastres branching earliest (after most parsimonious tree in Salvini-Plawen and Steiner 1996), additionally Caudofoveata grouping with Testaria into Hepagastralia (after Haszprunar 2000). (D) Solenogastres and Caudofoveata as independent clades with unresolved relationship to Testaria (after Salvini-Plawen and Steiner 1996; Salvini-Plawen 2003).

Their diet consists mainly of diatoms, detritus, 1876a, b; Spengel 1881; Hoffmann 1930), while and encrusting algae, but special feeding habits a clade Aculifera was proposed for those groups have been adopted by the carnivorous Placi- having a cuticle with sclerites covering at least phorella and Lepidozona (Latyshev et al. 2004), part of the mantle (e.g., Hatschek 1891; Scheltema the xylophagous Ferreiraella (Sirenko 2004), 1988, 1996; Ivanov 1996). Other authors have or the true herbivorous Stenochiton. There are argued that aplacophorans are paraphyletic with about 920 living species (Schwabe 2005), most respect to a clade Testaria, comprising the remain- living in the marine intertidal or sublittoral, ing molluscs, within which Polyplacophora is a with some deep-sea species also known (Kaas sister taxon to Conchifera (e.g., Wingstrand 1985; et al. 1998). Salvini-Plawen 1980, 1985, 1990, 2003; Salvini- relationships The two aplacophoran taxa Plawen and Steiner 1996). Based on midgut and Polyplacophora were, and still are, consid- morphology, Haszprunar (2000) additionally ered by most morphologists as basal within defi nes the clade Hepagastralia for Caudofoveata Mollusca, preceding the conchiferan radiation, plus Testaria. A sister group relationship of Poly- although their relative placement varies between placophora with Conchifera is often assumed in proposed hypotheses (Figure 4.2A–D). In one studies of conchiferan relationships (e.g., Giribet scheme, Solenogastres and Caudofoveata have and Wheeler 2002), but it is also questioned been incorporated in the phylum Aplacophora, (e.g., Lindberg and Ponder 1996). the sister group of a clade Testaria consisting of Recent discoveries of sclerite-bearing fossils Polyplacophora and Conchifera (Waller 1998). (see following discussion), additional develop- Alternatively, based on similarities in their ner- mental work with new techniques, and recent vous system, Polyplacophora was considered morphological and molecular studies have to be the sister group to Aplacophora, the two shed new light on molluscan origins and the together forming the Amphineura (von Ihering evolution of Solenogastres, Caudofoveata, and

74 solenogastres, caudofoveata, and polyplacophora FIGURE 4.3. Fossils interpreted as early molluscs (drawings by C.-O. Schander). (A) Wiwaxia corrugata from the Burgess Shale. (B) The Silurian Acaenoplax hayae. Note the rows of acicular skeletal elements seen either as aculiferan-like sclerites or as polychaete-like chaetae. (C) The Cambrian Odontogriphus omalus from the Burgess Shale.

Polyplacophora. Here, we revisit some old based on their sluglike appearance, muscular ven- hypotheses and review the newest fi ndings for tral foot, dorsal calcifi cation patterns, gill arrange- these fascinating groups. ment, and the possible presence of a radula (e.g., Conway Morris and Peel 1995, Caron et al. 2006). Controversies still remain as to which extant THE FOSSIL RECORD AND Metazoa these fossils are most closely related, MOLLUSCAN ORIGINS but, in any case, they assist in understanding the Molluscan lineages probably extended at least as evolution of external calcifi cation in Mollusca as far back as the base of the Cambrian (543 Mya) well as in Metazoa in general. (Glaessner 1969; Runnegar and Pojeta 1985; The Middle Cambrian Wiwaxia corrugata Bengtson 1992) or the Upper Precambrian, if from the Burgess Shale (Figure 4.3A) was con- trail-like impressions in the Ediacaran strata are sidered “strikingly similar” to molluscs on the correctly interpreted as traces left by the ventral basis of body shape and the radular-like feeding muscular foot of Kimberella quadrata, a limpet- apparatus (Conway Morris 1985). This radular- like animal with possibly molluscan affi liations like structure was interpreted as homologous (Fedonkin and Waggoner 1997; see also Parkhaev, to the radula of an extant solenogaster Helico- Chapter 3). The known polyplacophoran fos- radomenia (Scheltema 1998, Scheltema et al. sil record extends from as early as the Upper 2003). Analyses of Wiwaxia’s sclerites, however, Cambrian (Yochelson et al. 1965; Runnegar et al. have led to doubts as to its molluscan affi nity 1979; Yates et al. 1992; Stinchcomb and Darrough (Butterfi eld 1990, 1994; Watson Russel 1997) 1995; Slieker 2000). No fossil aplacophorans are because the solid wiwaxiid sclerites were origi- known, and thus there is no direct evidence of the nally chitinous and had longitudinal ornamenta- time of origin of solenogasters or caudofoveates. tion on their dorsal side, much like chrysopetalid Recently, increasing numbers of problem- polychaete paleae (specialized chaetae). The atic sclerite-bearing metazoans from the Early most recent and, so far, the most comprehensive and M iddle Cambrian have been discovered study of the phylogenetic placement of Wiwaxia, and assigned a taxonomic placement close to, or was carried out by Eidbye-Jacobsen (2004). He within, Mollusca. These animals have been com- found “no characters that could indicate any pared to aplacophorans and polyplacophorans close relationship with Polychaeta or Annelida.”

solenogastres, caudofoveata, and polyplacophora 75 Thus, a molluscan affi nity of Wiwaxia again are certain hollow aplacophoran sclerites that seems plausible. form around an organic template protrud- The Cambrian Odontogriphus omalus ing from the sclerite-producing cell (Hoffman (Figure 4.3C) was originally interpreted as a 1949; Okusu 2002). Moreover, the terminal lophophorate or with a possible connection to valves and sclerites of Halkieria may have been some Cambrian conodonts (Conway Morris aragonitic and thus similar in their mineral- 1976). This interpretation was based on a single ogical composition to those of aplacophorans specimen in rather poor condition. Newly dis- and polyplacophorans (Eernisse and Reynolds covered specimens from the Burgess Shale 1994; Vinther and Nielsen 2005). Similarities allowed a reinterpretation of this fossil, revealing between the three distinct types of sclerites in several characters with possible molluscan affi n- halkieriids (siculates, cultrates, and palmates) ity (Caron et al. 2006a; but see also Butterfi eld and wiwaxiids (ventro-laterals, upper-laterals, 2006 and Caron et al. 2006b). Odontogriphus and dorsals) and the zones of sclerites in was a dorsally-ventrally compressed, elongated aplacophorans and polyplacophorans have been animal with an oval body up to 12 mm long. It noted (Conway Morris and Peel 1990; Bengtson had a muscular foot lined by simple gills and a 1992; Conway Morris and Peel 1995; Scheltema ventral mouth with a radula strikingly similar 1998). Scheltema and Ivanov (2002) also sug- to that of Wiwaxia. There is also indications of gested that the serially clustered siculate scler- a pair of salivary glands. It lacked a mineralized ites in Halkieria are homologous to the seven shell and sclerites. It was most likely a bacterial transverse regions devoid of sclerites seen in a grazer feeding on the cyanobacterium Morania. solenogaster postlarva. Most recently, Vinther The general shape of the body is suggestive of and Nielsen (2005) convincingly demonstrated the Precambrian fossil Kimberella as well as the the molluscan affi nity of Halkieria. They stressed Cambrian Wiwaxia. a number of similarities between Halkieria and Another fossil repeatedly referred to as a Polyplacophora, such as the overall morphol- mollusc is the Early Cambrian Halkieria from ogy and sclerite arrangement, but the terminal northern Greenland. The fi rst entire articulated valves of Halkieria are different from polypla- halkieriid to be discovered, Halkieria evangelista, cophoran valves and more similar to conchif- is described as a long fl at animal with a ventral eran shells in lacking a tegmentum layer and creeping sole, dorsal sclerites, and two terminal pore canals. The hollow siculate sclerites also valves (Conway Morris and Peel 1990, 1995). show resemblance to those in the fossil poly- Although it possesses several mollusc-like char- placophoran Echinochiton (Pojeta et al. 2003). acters, Conway Morris and Peel (1995) placed Consequently, the new class Biplacophora for Halkieria either as the sister group to Annelida molluscs with two shell plates and a covering or within Brachiopoda. Halkieriid sclerites are of sclerites was introduced (Vinther and Nielsen fi lled with phosphate, leading to speculation 2005), and the class Coeloscleritophora, a taxon that they originally were fi lled with tissue and that used to unify a number of fossils with formed by “external mineralization of a protrud- hollow sclerites (Bengtson and Missarzhevsky ing organic template,” like polychaete chaetae 1981), was declared to be polyphyletic. (Butterfi eld 1990; Bengtson 1992; Conway Intrepretations of Halkieria as a mollusc have Morris and Peel 1995). The mode of sclerite for- raised further questions regarding the evolution mation was thought by Bengtson (1992, 1993) of shell and sclerites among molluscs. It has to be in contrast to that in aplacophorans and been suggested that polyplacophoran and halki- polyplacophorans, where sclerites are produced eriid valves are formed through coalescence by invagination of a single cell or, in chitons, of calcium carbonate sclerites (Pojeta 1980; by invaginated groups of cells (Haas 1981; Salvini-Plawen 1985; Eernisse and Reynolds Eernisse and Reynolds 1994). However, there 1994). The extant chiton, Acanthochitona, and

76 solenogastres, caudofoveata, and polyplacophora the fossil ?coeloscleritophoran? Maikhanella, both Hoare and Mapes (1995) discussed the have valves with scaly sculptures that appear to Devonian problematic taxon Strobilepis from be composed of merged neighboring sclerites the Moscow Formation in New York (United (Bengtson 1992). Other spicule-bearing fossils, States) and introduced a new Carboniferous however, lack those sculptures. The valves (shells) (Pennsylvanian) problematic genus Diadeloplax, of Maikhanella have been suggested to grow by from the Gene Autry Formation in Oklahoma marginal accretion and their sclerites by interpo- (United States). These two genera were placed lation, just as occurs in some molluscs and was in the new family Strobilepidae and new class suggested for halkieriids (Bengtson 1992; Con- Multiplacophora whose phylum assignment way, Morris, and Peel 1995), but new fi ndings on remained uncertain. They noted that multi- a Recent vetigastropod, Vacerrena kesteveni, show placophorans characteristically have 12 plates that a scaly shell-surface may be a calcifi ed perio- that have diverse shapes and, at least in part, stracal sculpture (Ponder et al. 2007). Scheltema lack bilateral symmetry, and that small auxiliary (1998) doubts that chiton valves are formed by plates are always associated with larger interme- coalescence of calcium carbonate sclerites and diate plates. The recent discovery of an excep- points out that seven transverse regions devoid tionally well-preserved specimen of another of sclerites in a solenogaster postlarva (see pre- multiplacophoran, Polysacos vickersianum, from ceding paragraph) may be homologous to the the Carboniferous of Indiana (United States), chiton larval shell fi elds. If chiton valves are not enabled a more accurate reconstruction of formed by coalescence of sclerites, they may the body plan of this group (Vendrasco et al. have originated simply through modifi cation of 2004). The animal is very similar to a chiton spicular calcifi cation mechanisms (Carter and in body shape and bears 17 shell plates and a Hall 1990), necessitating only a simple step in lateral fringe of spines. Both plates and spines the evolution of a shell from sclerites (Scheltema are most likely homologous to polyplacophoran and Schander 2006). valves, and the valves are articulated as in mod- The exceptionally well-preserved Silurian ern chitons. The oldest multiplacophoran fos- Acaenoplax hayae (Figure 4.3B) was thought sils are Devonian and thus much younger than to be related to aplacophorans (Sutton et al. the oldest chitons (see following discussion). 2001a, b, 2004). Acaenoplax is a vermiform fos- Vendrasco et al. (2004) place the multiplacoph- sil with about 18 iterated rows of ridges bear- orans as an order within the Polyplacophora, ing needle-shaped sclerites similar to those in implying an early divergence from the eight annelids, seven dorsal calcareous plates similar shell plate plan in Polyplacophora. It is possi- to those in chitons, a single posterior ventral ble that changes in the number and patterning plate, and posterior gills (Sutton et al. 2001a, b). of shell plates involved only small changes in Its seven dorsal valves and single ventral valve homeobox genes, analogous to the changes that have been interpreted to be homologous with have occurred in the relative number of verte- valves 1–6 and 8 of chitons and with the seven brae in modern snakes (Cohn and Tickle 1999; dorsal transverse regions free of sclerites in an Wiens and Slingluff 2001). Although it has been aplacophoran postlarva (Scheltema and Ivanov shown that homeobox genes are involved in the 2002; see preceding paragraphs). Although this patterning and formation of modern chiton may seem to corroborate the Aculifera hypoth- shell plates (Jacobs et al. 2000), details have not esis, this placement was challenged by Steiner yet been investigated. and Salvini-Plawen (2001), who suggested that The oldest polyplacophoran fossils are an annelid affi nity of Acaenoplax was just as known from the Upper Cambrian (Yates et al. likely because of its lack of explicit molluscan 1992), and since then, with exception of multi- characters and overall similarity to some Recent placophorans, their general body plan and valve tube-dwelling annelids. morphology did not change signifi cantly. This

solenogastres, caudofoveata, and polyplacophora 77 is confi rmed by fi ndings of numerous complete have free-swimming, lecithotrophic larvae with articulated specimens, such as Glaphurochiton an enlarged swimming test (pericalymma) with concinnus from the Carboniferous of Illinois differing numbers of rows of ciliated prototrochs. (United States) (Yochelson and Richardson The apical test of E. babai larvae is completely cil- 1979). Fossil plates, however, show that the iated with an apical tuft and a single prototroch occurrence of microaesthete structures must composed of compound cilia (Figure 4.4A). It is be interpreted as a post-Paleozoic innovation lost during metamorphosis. The pericalymma (Hoare 2000). test is often regarded as homologous to the Smith and Hoare (1987) divided the Poly- enveloping test of protobranch bivalve larvae as placophora into three subclasses: Paleoloricata, well as to the velum of bivalve and gastropod veli- Phosphatoloricata, and Neoloricata. Later ger larvae (for review see Nielsen 2004). Homol- (Sirenko 1997) followed Bergenhayn (1955) and ogy of these structures remains uncertain, and Van Belle (1983) in accepting two lineages within either they are interpreted as similarly modifi ed the Polyplacophora: Paleoloricata and the more apical structures evolved from a basic trocho- derived, articulamentum-bearing Neoloricata phore specialized in swimming (Jaegersten 1972; (or Loricata in Sirenko 1997). All extant Nielsen 1987, 2004) or the pericalymma test is chitons belong to Neoloricata, whereas fossil seen as a primitive trait within the Mollusca forms are classifi ed within both groups. In the (Salvini-Plawen 1972, 1980, 1988; Chaffee and Neoloricata there are Cenozoic and Mesozoic Lindberg 1986). The trunk region of the larvae taxa, while only Paleoloricata are known from is unciliated and gives rise to defi nitive ectoder- the Paleozoic. Sirenko (1997) recognized four mal structures, such as cuticle, epidermis, and orders, including fi ve suborders and 14 families epidermal sclerites. No external metameric itera- from the Paleozoic. Hoare (2000) suggested tion can be found at any stage, and there is no minor changes in the system but otherwise evidence of protonephridia. accepted Sirenko’s conclusions. Nevertheless, a Earlier fi ndings (Nielsen 1995, 2004) have few problems with uncertain affi liations to Poly- been recently supported by a thorough study on placophora still exist, such as Luyanhaochiton Chaetoderma employing electron microscopy and from the Lower Cambrium of China (Hoare fl uorescence staining of musculature (Nielsen 2000; see also Parkhaev 2007, Chapter 3). et al. 2007). This study shows lecitotrophic (pseudo-)trochophore larvae with a prototroch and a telotroch and a pair of protonephridia. In DEVELOPMENT the later stages, a ventral suture and seven dorsal Studies on the early embryology and develop- transverse rows of spicules are present. ment of aplacophoran molluscs are rare, and Chiton embryos, as studied to date, undergo thus comparisons with other molluscan classes equal cleavage in a typical spiralian pattern remain diffi cult (for review see Verdonk and Van (Heath, 1899; Grave, 1932; Van den Biggelaar, den Biggelaar 1983; Buckland-Nicks et al. 2002). 1996). The resulting trochophore larvae are Knowledge of the development of Solenogastres lecithotrophic and possess a unique prototroch is restricted to a few species, whereby the early composed of two to three irregular rows of studies of Pruvot (1890), Heath (1918), and Baba differentially ciliated trochoblasts, as shown (1938, 1940b) were only recently added to by for Chiton polii (see Kowalevsky 1883), Ischno- Okusu’s (2002) work on the embryogenesis and chiton rissoi (see Heath 1899), Lepidopleurus development of Epimenia babai. This description asellus (see Christiansen 1954), and Chaeto- of early embryogenesis revealed that cleavage is pleura apiculata (see Henry et al. 2004). The spiral, unequal, and holoblastic. Solenogastres free-swimming larval stage ranges from a few are hermaphrodites with internal fertilization and minutes to a few days. After settlement, the

78 solenogastres, caudofoveata, and polyplacophora apical tuft and the prototroch may persist for a Lydeard et al. 2000; Giribet and Wheeler 2002). while. Metamorphosis starts with a dorsoven- There are only a few molecular analyses that tral fl attening of the body. A detailed summary have included representatives of Solenogastres of larval development in chitons was presented (Okusu 2003; Okusu et al. 2003; Passamaneck by Buckland-Nicks et al. (2002). et al. 2004; Giribet et al. 2006) and Caudofoveata The relationship of larval shell formation with (Winnepenninckx et al. 1994; Okusu 2003; Okusu expression of the engrailed gene has been reported et al. 2003; Passamaneck et al. 2004; Giribet et al. in various molluscs (Wray et al. 1995), as has the 2006). Obtaining DNA sequence data has been expression of this gene in cells adjacent to the challenging for aplacophoran taxa because they shell fi elds in chiton larvae (Jacobs et al. 2000). are diffi cult to collect and because of contamin- A fi rst cell lineage study (Henry et al. 2004) ation issues in Solenogastres (Okusu and Giribet pointed out that polyplacophoran epidermal 2003). In an investigation of molluscan phy- sclerites arise from different, if overlapping, logeny using large-subunit and small-subunit sets of cells than the shell plates and the con- nuclear rRNA sequences of 33 molluscan taxa, chiferan shell, an important fi nding for con- including a solenogaster, a caudofoveate, and four sideration of the evolution of molluscan shells. chitons, neither the Aculifera hypothesis nor the The same study demonstrated that the larval Testaria hypothesis is supported (Passamaneck ocelli of Chaetopleura apiculata develop post- et al. 2004). In this study, Polyplacophora does trochally from a unique set of cells not seen in not emerge as a basal clade, and it groups only other spiralians. in some of the analyses with Solenogastres and Detailed investigations of myogenesis using never with Caudofoveata. A recent analysis of fl uorescent markers during the early devel- fi ve genes and gene fragments from 101 species opment of chitons showed that serial mus- representing all molluscan classes shows Soleno- cle structures and dorsal shell plates do not gastres and Caudofoveata as independent clades develop simultaneously (Friedrich et al. 2002; near the base of the tree but Polyplacophora as Wanninger and Haszprunar 2002). This indi- more derived and forming a clade (Serialia) with cates that hypotheses indicating a sister taxon Monoplacophora (Giribet et al. 2006). relationship between molluscs and other seg- Recent attempts to study chiton phylogenetic mented protostomes such as Annelida, based on relationships using several combined genes the serial repetition of organs (e.g., Götting 1980; (Okusu et al. 2003) resulted in a well-resolved Ghiselin 1988; Nielsen 1995), are not supported. phylogeny of chitons but could not resolve the placement of chitons relative to Solenogastres, Caudofoveata, and Conchifera. PHYLOGENY AND SYSTEMATICS The notion of a basal position of Soleno- gastres, Caudofoveata, and Polyplacophora was SISTER GROUP RELATIONSHIPS recently supported by Lundin and Schander’s Although a number of attempts have been made studies on the ultrastructure of locomotory cilia to resolve molluscan phylogeny using both mor- in Solenogastres (2001b), Caudofoveata (1999), phological and molecular sequence data, there and Polyplacophora (2001a). These cilia are of has not yet been any consensus on the position the common metazoan type, with paired ciliary of aplacophoran taxa and Polyplacophora within rootlets orientated at almost 90° to each other Mollusca (see Figure 4.2). and without an accessory centriole. Such paired One problem with most phylogenetic stud- ciliary rootlets do not occur in gastropods, ies is the lack of a representative taxon sampling bivalves, and monoplacophorans (Lundin and for the basal clades (Ghiselin 1988; Winnepen- Schander 2001b), nor in scaphopods (Lundin ninckx et al. 1994, 1996; Rosenberg et al. 1997; and Schander, unpublished data).

solenogastres, caudofoveata, and polyplacophora 79 SYSTEMATICS AND PHYLOGENY OF Sterrofustia: Cuticle is thick, sclerites are APLACOPHORAN MOLLUSCS solid acicular or scalelike elements, lateroventral foregut glands are diverse Histology has been the standard method used (e.g., Phyllomeniidae, Imeroherpiidae). for species identifi cation and classifi cation in aplacophorans, mostly because of their small Cavibelonia: Cuticle is thick, sclerites are size, lack of a shell, and often poor preservation hollow acicular elements, additional solid of sclerites in non-buffered fi xatives. Thus, the elements may occur, lateroventral foregut morphological and histological data available glands are diverse and include tubular for Solenogastres and Caudofoveata are sur- glands with intraepithelial glandular cells prisingly detailed compared to other molluscan (e.g., Pararrhopaliidae, Rhopalomeniidae, taxa. External characters are suffi cient for a spe- Simrothiellidae, Epimeniidae). cies diagnosis in many caudofoveates but only Solenogaster phylogenetics still struggles with in relatively few solenogasters. However, the the great diversity of hard-part as well as soft- addition of internal hard-part characters (radula body characters among the families and with and copulatory stylets), usually allows identifi ca- the lack of a general concept as to the plesio- tion of members of both groups (Scheltema and morphic character states. Most phylogenetic Schander 2000), but knowledge of anatomical analyses based on morphology (e.g., Scheltema and histological characters is of great importance and Schander 2000) have included only a for systematics and phylogenetic analyses. limited number of taxa. A recent comprehen- In both Solenogastres and Caudofoveata, sive study of solenogaster phylogeny based on classifi cation is based on comprehensive pub- morphological characters included all genera lications by Salvini-Plawen (1975, 1978). Some (Salvini-Plawen 2003). Although poor reso- recent additions have been made and doubts lution was obtained, Cavibelonia was mono- on the monophyly of certain clades raised (e.g., phyletic and derived (see also Salvini-Plawen Scheltema 1999), but the general concepts 2004), whereas Pholidoskepia emerged from remain unchallenged. a basal polytomy. Handl and Todt (2005) solenogastres Solenogaster higher clas- discussed the evolution of foregut glands in sifi cation uses external characters, such as types solenogasters and the so-called Wirenia-type of sclerites (solid elements versus hollow ele- lateroventral foregut glands (Figure 4.4B, a), ments, fl at scales versus rimmed or trough-like without a duct or lumen, seen in the pholido- elements), thickness of the cuticle, and gen- skepian Gymnomeniidae, were considered to eral characteristics of the lateroventral foregut be the most primitive exant type. Pararrhopalia- glands. Four orders were recognized by Salvini- type glands (Figure 4.4B, c) occur in some Pholi- Plawen (1978) (see also Figure 4.8): doskepia and Cavibelonia taxa, while certain gland types (e.g. Helicoradomenia-type, Figure 4.4B, d; Pholidoskepia: Cuticle is thin, scerites Simrothiella-type, Figure 4.4B, e) occur in Cavi- are scales in one layer, lateroventral belonia only. foregut glands are either endoepithelial Due to the ontogenetic change from solid (no glandular duct) or with duct and sclerites to hollow needles seen in some species, exoepithelial gland cells (e.g., Wireniidae, the hollow epidermal sclerites are considered Dondersiidae, Lepidomeniidae). derived, thus ruling out Cavibelonia as a basal Neomeniamorpha: Cuticle is thin; sclerites are clade. Hollow needles, however, also occur in scales, massive acicular elements, rimmed, the Acanthomeniidae, a taxon closely related to trough-like, and harpoon-shaped elements; pholidoskepian taxa, such as the Dondersiidae no lateroventral foregut glands present (e.g., (Salvini-Plawen 2003; see also Scheltema 1999, Neomeniidae, Hemimeniidae). Handl and Salvini-Plawen 2001). Thus the

80 solenogastres, caudofoveata, and polyplacophora FIGURE 4.4. Solenogastres and Caudofoveata, development and important characters. (A) Larvae of Epimenia babai (Solenogastres) during the completion of metamorphosis, 1: 4–6 days old, 2, 3: 9–12 days old; scale bar: 100 µm. From Okusu 2002. (B) Examples for lateroventral foregut glands of Solenogastres, 1: Wirenia-type, 2: Meioherpia-type, 3: Pararrhopalia-type, 4: Helicoradomenia-type, 5: Simrothiella-type. (C) Radula of Scutopus robustus (Caudofoveata), light micrograph; scale bar: 50 µm. (D) Part of the right half of a radula of Helicoradomenia sp. (Solenogastres), scanning electron micrograph; scale bar: 20 µm. (E) Ultrathin section of a radular plate of Helicoradomenia acredema, transmission electron micrograph, Db ϭ denticle base; Ph ϭ pharynx lumen; Rm ϭ radular membrane; Rp ϭ radular plate. (F) Confocal scanning micrograph of Alexa-phalloidin stained Meioherpia atlantica, the arrows indicate spiral muscle fi bers of the body wall; Bm ϭ buccal musculature; V ϭ vestibulum; scale bar: 0.1 mm. homology of certain hollow sclerites may be usually a single pair of teeth with prominent lat- questioned (Salvini-Plawen 2003). eral and ventral supports, and the stomach has Attempts toward a phylogeny of solenogas- a gastric shield. The radula of Prochaetoderma- ters by means of molecular methods has been tidae appears to represent an intermediate state hampered by technical problems (see Okusu (Salvini-Plawen and Nopp 1974; Salvini-Plawen and Giribet 2003), but refi ned techniques and 1975: fi g. 6, and slightly modifi ed in 1988: fi g. 1), intensifi ed efforts should provide results in the but the phylogenetic relationship between Pro- near future. chaetodermatidae and the other families is not caudofoveata This taxon is less diverse than well resolved (see Figure 4.8). Solenogastres, with only three or four families rec- morphological characters Over the last ognized, which are based on characters of the rad- few decades, modern techniques, such as scan- ula, mouth-shield, and body shape (Salvini-Plawen ning and transmission electron microscopy, 1975, but see Ivanov 1981) (see Figure 4.8): have provided new insights into the morphol- ogy and histology of solenogasters and caudo- Limifossoridae: Radula is bipartite, of several foveates and helped to further defi ne characters transverse rows, without lateral supports; valuable for systematics and phylogeny. Some body is homogenously shaped; mouth shield recent studies are summarized as follows. is disk- or U-shaped posterior of mouth Haszprunar (1986, 1987) supported the opening, or paired lateral to mouth opening. homology of the dorsoterminal sense organ Prochaetodermatidae: Radula is bipartite, in (DTS) in Solenogastres and Caudofoveata with several transverse rows, with ventral and the usually paired osphradia of chitons and lateral supports; posterior body is tail- higher molluscs but suggested an independent shaped, mouth shield is paired lateral to origin of the unpaired condition of the DTS in mouth opening. the two aplacophoran taxa. Chaetodermatidae: Radula is generally In both solenogastres and caudofoveates, represented by only one pair of teeth, with the mantle sclerites exhibit extraordinary vari- large ventral and lateral supports; body is ability in size and shape, but certain sclerite homogenously shaped or posterior body types are characteristic at higher taxonomic is tail-shaped; mouth shield is U-shaped levels (e.g., the hollow hooklike elements of posterior to mouth opening or encircling Pararrhopaliidae). Information on sclerite mouth opening. thickness can be gained by the use of cross- polarized light or by scanning electron micros- An additional family, Scutopodidae, was intro- copy (Scheltema and Ivanov 2000, 2004). duced by Ivanov (1981) but was rejected by Because they vary according to their location, Salvini-Plawen (e.g., 1992), who included sclerites should be sampled from standardized Scutopus within Limifossoridae. body regions for taxonomic purposes (e.g., There are no modern phylogenetic analy- Scheltema 1976, 1985; Scheltema and Ivanov ses published for Caudofoveata. Scutopus and 2000). Psilodens are probably the most basal genera Scheltema et al. (2003), in a review of the because some species have traces of a retained radula of basal molluscs, presented a theory on ventral suture innervated from the ventral nerve the nature of the primitive molluscan radula. cords, as well as primitive radular (distichous Like Eernisse and Kerth (1988), she argued pairs of teeth with median denticles; Figure 4.4C) that the most basal type was the distichous or (Salvini-Plawen 1975, 1985, 1988) and midgut bipartite radula with rows of paired radular confi guration (Scheltema 1981; for Psilodens plates. This type is present in the solenogaster see Salvini-Plawen 1988, 2003). In contrast, genus Helicoradomenia (Figure 4.4D) and the Chaetodermatidae have a highly derived radula, caudofoveate genus Scutopus (Figure 4.4C). In

82 solenogastres, caudofoveata, and polyplacophora FIGURE 4.5. Alternative phylogenies for Recent Neoloricata. (A) Unresolved tree based on Kaas and Van Belle (1994) and Kaas et al. (1998). (B) Phylogenetic tree after Sirenko (1993, 1997).

contrast, Salvini-Plawen (1988, 2003; see also POLYPLACOPHORA SYSTEMATICS Sirenko and Minichev 1975), suggested that the AND PHYLOGENY monoserial radula type, consisting of rows of Until recently, the higher classifi cation of Poly- single teeth, was the most primitive. Wolter placophora has remained unsettled (Bergenhayn (1992) showed that radular formation in apla- 1955; Smith 1960; Van Belle 1983; Eernisse cophoran groups is like that in higher molluscs, 1984; Sirenko 1993, 1997; Buckland-Nicks although each tooth is continuous with the 1995). Traditionally, classifi cations were based underlying membrane, there being no sepa- primarily on the morphology of shell plates rate tooth base as in chitons or conchiferans (valves), spicules, and perinotum processes (Figure 4.4E) and there is no subradular mem- (e.g., Smith 1960; Van Belle 1983; Kaas et al., brane. The radula is basically composed of a 1998), the shell and spicules being the only chitin-rich organic matrix (Peters 1972; Salvini- characters available for fossil chitons (Smith Plawen and Nopp 1974; Wolter 1992) with depo- 1960; Van Belle 1983). Of the four layers of sition of minerals (caudofoveates: Cruz et al. the shell plates (properiostracum, tegmentum, 1998; solenogasters: C. Todt, personal observa- articulamentum, myostracum) two are of high- tion). As in chitons (see following), such studies est taxonomic relevance: the often colorful and promise additional phylogenetic characters. sculptured tegmentum and the articulamentum, In solenogaster systematics, foregut glands which underlies the tegmentum and also forms are among the most important characters, espe- the insertion plates (see previous discussion). cially the multicellular lateroventral and dorsal All extant species (order Neoloricata) have been glands (Salvini-Plawen 1972, 1978). Handl and divided into three suborders (e.g., Bergenhayn Todt (2005) clarifi ed the foregut gland terminol- 1930; Smith 1960; Kaas and Van Belle 1985; ogy and modifi ed Salvini-Plawen’s (1978) clas- Van Belle 1983, 1985). Gowlett-Holmes (1987) sifi cation system of the lateroventral glands. In reestablished the monotypic Choriplacina (for addition, a number of ultrastructural studies Choriplax grayi), and her proposal was followed showed the complexity of multicellular fore- by others (Kaas and Van Belle 1994; Kaas et al. gut glands, which are composed of up to fi ve 1998) (Figure 4.5A). different types of glandular cells and nonglan- dular supporting cells (Todt and Salvini-Plawen Lepidopleurina: Articulamentum may have 2004a, 2005; Todt, in press). unslit insertion plates or none; tegmentum Attempts to apply modern fl uorescence tech- is well developed; perinotum is narrow niques to study musculature (Figure 4.4F) and to wide, dorsally covered with elongate nervous systems in Solenogastres are under scale-like spicules, ventrally either naked way, and preliminary results have been pre- or with scales. sented as conference contributions (D. Eheberg Choriplacina: Articulamentum is well and G. Haszprunar, R. Croll, and R. Hochberg, developed with large, unslit insertion personal communication). plates; tegmentum is reduced; perinotum

solenogastres, caudofoveata, and polyplacophora 83 FIGURE 4.6. Polyplacophora; characters relevant for taxonomy and systematics. (A) Specimen of Ischnochitonidae, ventral view showing head (H), foot (F), and gills (arrow); scale bar: 2 mm. (B–D) Scanning electron micrographs of Acanthopleura spp. provided by L. Brooker. (B) Three girdle scales from A. loochooana, note the sculptured surface; scale bar: 100 µm. (C) Section of the lateral region of an intermediate valve of A. brevispinosa showing three ocelli and numerous apical and subsidiary pores of aesthetes; scale bar: 50 µm. (D) Radula of A. echinata, scale bar: 400 µm. (E) Back-scattered electron image of ground and polished resin-infi ltrated major lateral tooth of A. spinosa composed of tooth base (Tb) and tooth proper (T) fused at a distinct junction zone (Jz); brightness of tooth compartments varies according to mineral contents: magnetite region (Mr), lepitocrocite-region (Lr), anterior cusp region (Acr), posterior cusp region (Pcr); scale bar: 50 µm (micrograph by L. Brooker). FIGURE 4.7. Polyplacophora, characters important for phylogeny illustrating variations in gill placement (A), egg hull sculpture (B), and sperm morphology (C). A, from Okusu (2003), B, two left hand fi gures from Buckland-Nicks and Hodgson (2000), others from Sirenko (1993), C, schematic drawings from Okusu et al. (2003), others from Buckland-Nicks and Hodgson (2000). For further information see text.

is wide and fl eshy, appears naked, dorsally various types of elements (scales, hairs, with randomly distributed minute spicules. spicules). Ischnochitonina: Articulamentum is well Acanthochitonina: Articulamentum is well developed, generally with slits in all valves; developed with insertion plates in all valves; teeth of insertion plates are pectinated or number of slits in the fi rst valve does not smooth; number of slits in the fi rst valve exceed fi ve; teeth of insertion plates never generally higher than fi ve; perinotum has pectinated; perinotum wide and fl eshy,

solenogastres, caudofoveata, and polyplacophora 85 FIGURE 4.8. Tree diagram summarizing major clades within Solenogastres, Caudofoveata, and Polyplacophora with regard to recent knowledge. Within Caudofoveata, families are given as the highest taxonomic level because there are no orders defi ned. Note the lack of resolution in many positions and on different levels.

generally with spicules of different size, egg hull type, sperm morphology, and gill place- never scaly. ment (Eernisse 1984; Sirenko 1993; Buckland- Nicks 1995; Okusu et al. 2003) (Figure 4.7). Some of the diagnostic characters in the Chiton eggs have hull processes that are pri- preceding list have been criticized as being marily secreted by the egg (Richter 1986) and inappropriate for the higher classifi cation of seem to direct sperm to localized areas during chitons. Although the tegmental structure of fertilization (Buckland-Nicks 1993). The pro- shell plates is of taxonomic relevance at the cesses are typically either cup-shaped or spiny specifi c level (Haas 1972), the nature of the (Figure 4.8B) and show species-specifi c dif- articulamentum is of interest for higher clas- ferences (Pearse 1979). Chitons with elaborate sifi cation and refl ects an evolutionary trend egg hulls also have sperm with asymmetrically (Sirenko 1997). Therefore, an undeveloped arranged mitochondria and a long fi lamentous articulamentum lacking insertion plates in anterior extension of the nucleus (Pearse 1979), the terminal and intermediate valves and with which has a reduced acrosomal vesicle at its tip short and mainly unconnected apophyses is (Type I and II sperm sensu Buckland-Nicks et al., seen as the basal condition, and is still pres- 1990; Buckland-Nicks 1995) (Figure 4.8C). The ent in a few extant chitons (e.g., Leptochiton). ctenidia are positioned in characteristic num- The derived condition with either slit (e.g., bers and arrangements along each side of the Ischnochiton) or unslit insertion plates (e.g., foot within the pallial cavity (for example, see Choriplax) is more common. Insertion plates Kaas and Van Belle 1985: fi g. 3), even if varia- with smooth teeth (e.g., Ischnochiton) are con- tions in the exact number of ctenidia within sidered to be more primitive than those with species occur (Plate 1897, 1899, 1901). During pectinated teeth (e.g., Chiton). ontogeny, the fi rst ctenidial pair to appear is Russell-Hunter (1988) discussed the impor- post-renal (immediately behind the nephrid- tance of gill placement in chiton phylogeny, and iopore) (Pelseneer 1899). In certain chitons, recent work has shown a correlation among ctenidia are added exclusively anterior to the

86 solenogastres, caudofoveata, and polyplacophora post-renal gill pair (abanal type), while in This classifi cation of Polyplacophora is cor- others they are added anteriorly and posteri- roborated by a recent molecular phylogenetic orly (Eernisse 1984; Sirenko 1993; Eernisse and analysis of chiton relationships (Okusu et al. Reynolds 1994). 2003), which included representatives of Sirenko (1993, 1997) updated the former 28 species belonging to 13 families based on classifi cations (Thiele 1909–1910; Bergenhayn the combination of fi ve genes (18S rRNA, 28S 1930; Smith 1960; Van Belle 1983) and divided rRNA, 16S rRNA, COI, and histone 3). The extant chitons into two orders, Lepidopleurida resulting topology supports the two lineages, and Chitonida, the latter having two suborders, Lepidopleurida and Chitonida, but refutes Chitonina and Acanthochitonina (Figure 4.5B). monophyly of many classical taxonomical This is consistent with Buckland-Nicks’ (1995) groups sensu Kaas and Van Belle. Okusu et al. phylogenetic analysis, using 25 characters (2003) further showed a strong correlation scored from egg hull, sperm, shell valves and of egg hull morphology with the molecular ctenidia, of 10 polyplacophoran families (25 spe- phylogenetic trees. The study showed Lepi- cies examined in total), with two aplacophorans dopleurida to be the more basal clade and as outgroup taxa. Chitonida was divided into three lineages: taxa with simply round to weakly hexagonal Lepidopleurida: Valve characters are cupules of the egg hull, abanal gills, and type presumably primitive, without slits in the I sperm (clade A in Okusu et al. 2003: fi g. 8); insertion plates; ctenidia are adanal and taxa with egg hulls with strongly hexagonal restricted to the posterior region; sperm cupules with fl aps, abanal gills, and type I are ectaquasperm; eggs are smooth with sperm (clade B in Okusu et al. 2003: fi g. 8); extraordinary thick egg hulls. and taxa with various shapes of spiny egg Chitonida: Valve characters are presumably hulls, adanal gills, and type II sperm (clade C derived, with either slit or unslit insertion in Okusu et al. 2003, fi g. 8; Chitonoidea sensu plates extending laterally into the girdle; Sirenko 1997). ctenidia are of adanal or abanal type, A number of additional characters, useful always with a space between them and for systematics and phylogeny at different lev- the anus papilla; sperm have a fi lamentous els, have been investigated over the past few extension of the nucleus and reduced decades, and are summarized in the following acrosome; there are elaborate egg hull paragraphs. processes. The position and morphology of osphradia vary among chiton taxa and may also be useful The Chitonida was further divided into two phylogenetically. According to ultrastructural suborders: data (Haszprunar 1986, 1987), a true osphra- dium is present only in Chitonida, while the Chitonina: Ctenidial placement is adanal; more basal Lepidopleurida show branchial and a posterior extension of midpiece alters lateral sense organs that do not appear to be sperm shape; spiny, narrow-based egg hull homologous. However, some (if not all) gen- projections; ocelli occur in some genera era of Lepidopleuridae have dark pigmentation (e.g., Onithochiton). under the mouth lappets, which may repre- Acanthochitonina: Ctenidial placement is sent a true, anteriorly positioned osphradium abanal; the overall sperm shape differs (E. Schwabe, personal observation). from the preceding groups (for detailed The occurrence and distribution of other descriptions see Buckland-Nicks 1995); sensory elements, including various types of egg hull with broadly based cupules that aesthetes and ocelli in the shell plates (e.g., are not spiny; ocelli are absent. Fischer and Renner 1979; Currie 1992), as well

solenogastres, caudofoveata, and polyplacophora 87 as so-called ampullary cells and FMRF-amide- from 12 to 26, with Acanthochitonidae showing positive1 neurons situated anteriorly underneath a higher variability, ranging from 16 to 24, while the apical ciliary tuft in chiton larvae (Haszprunar Chitonidae are more uniform, ranging from et al. 2002; Voronezhskaya et al. 2002), also 24 to 26 and all Ischnochitonidae are 24. In appear to refl ect phylogenetic relationships. Ischnochitonidae, the chromosome arm mor- Radular characters have been used for chi- phology is meta- or submetacentric only, while ton classifi cation in the past (e.g., Thiele 1893, additional telo- or subtelocentric arm morphol- 1909–1910) but since then have been shown ogies occur in other chiton taxa. to be too homoplastic at the deeper levels The oxygen-binding protein hemocya- (Eernisse 1984; Sirenko 1993, 1997; Eernisse nin has been found in chitons, cephalopods, and Reynolds 1994; Buckland-Nicks 1995; protobranch bivalves, and gastropods. As its Okusu et al. 2003). Nevertheless, they are valu- origin is calculated to be Precambrian it has able at certain taxonomic levels (e.g., Bullock been explored for its potential to resolve mol- 1988; Saito 2004). Saito (2004), for example, luscan evolution (Lieb and Markl 2004). The points out that selected radular characters importance of this protein for a species-level within the Cryptoplacoidea correlate with a phylogeny and as a marker for evolutionary reduction of the tegmentum within that group. studies was demonstrated for basal gastropods Morphometric data such as the ratio of radular by Streit et al. (2006), and attempts to reveal length to total body length, length of the radular chiton phylogenetic relationships by means of cartilages to total radular length, and number of this new molecular approach are in progress radular teeth rows to radular length may also be (B. Lieb, personal communication). of phylogenetic relevance (E. Schwabe, personal observation). There is a wealth of data on radular ADAPTIVE RADIATIONS mineralization in chitons (e.g., Macey et al. 1994; Macey and Brooker 1996; Macey et al. 1996; Lee The most outstanding innovations of early et al. 1998; Brooker et al. 2003; Wealthall et al. molluscs in comparison to their putative pre- 2005) and, according to Brooker and Macey decessors, and to other exant spiralians with (2001), specifi c traits in radular biomineraliza- similar lifestyles, are the differentiation of a tion can also be of systematic importance. With dorsal mantle completely covered in cuticle and the help of light and scanning electron micros- sclerites, a ciliated ventral foot for locomotion, copy as well as energy-dispersive spectroscopy and the development of the radula as an effec- (see Figure 4.6E), they showed that iron levels in tive feeding apparatus. the teeth of some species only recently merged A protective cover composed of sclerites into Acanthopleura by Ferreira (1986) differ con- (scleritome) can be found in many of the earli- siderably from the traditional members of this est known putative molluscs (Wiwaxia, Halki- taxon, including its type species. eria) as well as in all three basal groups of extant Interesting information is also available molluscs (with additional shell plates in Polypla- on the karyotypes of chitons. Yum (1993) pro- cophora) and thus may be viewed as a symple- vided cytogenetic data for eight species and siomorphy of modern Mollusca (most recently thus extented Nakamura’s (1985) list to 22. The by Scheltema and Schander 2006). It is inter- diploid chromosome number in chitons ranges esting to note, however, that the earliest fossils presumably belonging to the molluscan lineage (Kimberella, Odontogriphus) did not possess any 1. FMRF-amide, a molluscan cardio-excitatory neuro- shell or scleritome at all, indicating that these transmitter, is a tetrapeptide composed of phenylalanine structures were derived within early molluscs. (F), methionine (M), arginine (R), and phenylalanine (F) residues, with the terminal acid group converted to an The evolutionary advantage of a scleritome com- amide group. posed of numerous small sclerites, such as in

88 solenogastres, caudofoveata, and polyplacophora solenogasters and caudofoveates, is obviously with long and pointed denticles and a variety protection against predators and not so much of other radular morphologies adapted for car- against the physical impacts of tides and water nivory were developed in solenogasters. The currents. This probably accounts for aplacopho- extremely long radular ribbon of all modern rans being largely restricted to more sheltered chitons, which bears multiple sclerotized and habitats such as deep-water soft sediments and sturdy teeth in part impregnated with metals, sublittoral hard bottoms. The very few shal- is, in contrast, a specialized tool for grazing on low-water species (mostly Solenogastres) occur hard substrates. in coral reefs or are part of the subtidal meio- benthos. In contrast, many chitons inhabit the GAPS IN KNOWLEDGE rocky intertidal, where they withstand strong physical forces protected by their tough cuticle As shown above, recent research in the fi elds and shell plates and are kept in place by their of palaeontology, ultrastructure, and molecu- broad, highly muscular foot. lar biology has led to a better understanding The model archimollusc of textbooks typi- of basal molluscs, their biology, and internal cally resembles a chiton or untorted limpet in relationships. Although modern approaches, body shape, and the vermiform shape of apla- such as selective staining techniques for ner- cophorans is usually viewed as a derived feature vous tissues and musculature, in situ hybridiza- (Salvini-Plawen 1972, 1985, 2003; Scheltema tion combined with tracing of gene expression 1993, 1996) or sometimes a plesiomorphic one in development, and multigene approaches for (Haszprunar 2000; Haszprunar et al., Chapter 2). phylogenetic analyses, have already brought The expansion along the longitudinal body axis a wealth of important knowledge about may be explained as an adaptation to epizoism Polyplacophora, such investigations are still (Solenogastres) or burrowing (Caudofoveata) largely lacking for the aplacophoran taxa. In (Salvini-Plawen 1972; but see Scheltema 1996 for Polyplacophora, however, information about a contrasting view). The complete reduction of a more taxa needs to be added to the existing foot in caudofoveates, combined with the appear- data matrices to strengthen phylogenetic con- ance of a mouth shield, is generally seen as con- cepts. This includes morphological data, such nected to their burrowing lifestyle. as sperm and egg hull structure, chromosome The radular morphologies of the three clades numbers, and radula characters, as well as discussed herein, refl ect divergent feeding molecular data. Comparative investigations habits. Based on fossil evidence, the most of sense organs, excretory organs, and larval primitive radula (Wiwaxia, Odontogriphus) was characters are needed to clarify the usefulness used for algal mat grazing (Caron et al. 2006). of these characters for phylogeny. The same Some authors argue that the primitive radula is true for protein coding sequences, such was used for either shoveling in detritus or as hemocyanin or ribosomal protein coding grabbing large food items and was a broad sequences, revealed by expressed sequence structure consisting of several rows of wide, tag (EST) projects or selective analysis. For sclerotized teeth with denticles, the individ- the aplacophoran taxa we still lack molecular ual teeth connected by a fl exible cuticle (e.g., studies that include a representative set of Salvini-Plawen 2003; Scheltema et al. 2003). taxa. Even though our knowledge of the mor- This type of radula is found in some caudo- phology of Solenogastres and Caudofoveata is foveates (Scutopus; Figure 4.4C) and soleno- extensive, the homology of certain characters gasters (Helicoradomenia; Figure 4.4D). From between these taxa (mouth shield, vestibulum, this state pincer-like structures for picking up foot; regions of the gonopericardial tract) and individual diatoms evolved within caudofove- Polyplacophora (midgut regions; excretory ates, while multiple rows of distichous hooks system) is not yet well established. Moreover,

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