Tanabe, K., Shigeta, Y., Sasaki, T. & Hirano, H. (eds.) 2010.

Cephalopods - Present and Past Tokai University Press, Tokyo, p. 23-34.

The origins of cephalopod body plans: A geometrical and developmental basis for the evolution of vertebrate-like organ systems
Shuichi Shigeno*1, Sasaki Takenori2 AND Sigurd von Boletzky3
1

Department of Neurobiology, University of Chicago, 947 East 58th Street, Chicago, IL 60637, USA (*corresponding author; e-mail: sshigeno@uchicago.edu) 2 The University Museum, University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan (e-mail: sasaki@um.u-tokyo.ac.jp) 3 C.N.R.S., Observatoire Ocanologique, Laboratoire Arago, F-66651 Banyuls-sur-Mer, France (e-mail: boletzky@obs-banyuls.fr) Received May 6, 2008; Revised manuscript accepted September 28, 2008 Abstract. The evolution of cephalopod body plans has been one of the most intriguing topics in zoology. Their body parts, particularly of coleoids (squids, cuttlefishes, and octopuses), are composed of multiple sets of components including vertebrate-like analogical systems as a result of convergence. However, in spite of the potential importance for understanding the evolution and diversity in bilaterians, the origins of cephalopods have been poorly understood. There is little consensus of opinion for morphological linkage among the plans of cephalopods, basal molluscs, and other bilaterians. Here, we provide a review and new interpretation with an emphasis on the topographic transition of the soft parts that is shaped by a shared concentric circle or ovoid pattern in the embryos and adults of extant or fossil molluscs. The purpose of this article is also to characterize the cephalopod body plans, set against those of the other bilaterians, in the light of recent data from paleontology, embryology, and molecular gene expression patterns. Key words; embryo, evolution, development, molluscs, nervous system, nautilus

Introduction: Traditional views on the evolution of cephalopod body plans In 1830, two young naturalists, Meyranx and Laurencet, attempted a comparison of the anatomy of vertebrates and cephalopods, speculating that they have the same basic structural principle. While Geoffroy St. Hilaire adopted the idea as proof of his theory, on the unity of body plan that is composed of shared components of all animals, Georges Cuvier rejected it using questionable results of his anatomical study of an octopus (Figure 1; Appel, 1987; Le Guyader, 2004 for reviews). Ever since this pre-Darwinian academic debate, many zoologists have indulged in a long lasting discussion of how the cephalopod body plan and their organ systems can be linked to those of vertebrates (e.g. Packard, 1972; ODor and Webber, 1986). To a d d r e s s t h e l i n k a g e b e t w e e n t h e s e t w o phylogenetically distant taxa, data to infer the original condition was required. The traditional views on the origin of cephalopod soft parts largely relied on the anatomical analysis of extant cephalopods, particularly

nautiloids (Owen, 1832; Macdonald, 1855; Griffin, 1900; Willey, 1902). The numerous tentacles without suckers, the leathery hood, the pinhole eyes, the ovoid sacs of statocysts, the cord-like brain, the unfused funnel, absence of the ink sac, and also most of the other characters have been considered to be primitive states that enabled us to infer the common ancestor (see Saunders and Landman, 1987; Budelmann et al., 1997). Through a synthesis of the data in paleontology, embryology, and adult morphology (Naef, 1921-23, 1928), some evolutionary schemes were constructed to explain the transitory change (Figure 2) with the idea of a prototype of Conchifera and a hypothetical Nautilus embryo (Naef, 1928). In this view, the anterior-posterior (AP) and dorso-ventral (DV) axes are completely conserved during the changes from a gastropod to a cephalopod as initially suggested through the embryological study of the squid (Brooks, 1880) (the foot or arms define the ventral side of the bodies, and the head defines the anterior side). Along the DV axis, the arms, collar, funnel, mantle, and the shell of a cephalopod are respectively corresponding to the whole foot sole, epipodial region, mantle, and

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Shuichi Shigeno et al. stated above remain largely untested. In turn, a different approach has been adopted by some paleontologists and comparative malacologists (Figure 2; Yochelson et al ., 1973; Holland, 1987; Salvini-Plawen and Steiner, 1996; Lee et al., 2003). Their scenario was largely based on the important findings of the fossils of monoplacophoran-like shells, and the hypothetical reconstruction of the soft parts (Yochelson et al., 1973). In this view, the cephalopod tentacles/arms are derivates of both the differentiated cephalic region and anterior part of the foot. The posterior foot transforms into the funnel fold. The funnel is situated at the posterior end of the body; therefore, the posterior foot part of benthic ancestor is required to shift to more posterior and dorsal regions of the body of cephalopods. Unfortunately, no fossil record of soft parts has been found so far to infer the soft parts in the basal cephalopods. Therefore, no evidence exists to support this hypothesis (Boletzky, 2006). However, it is notable that the presence of multiple paired muscle scars on some fossil shells (Yochelson et al., 1973) suggests that the ancestor might have distinct pedal retractor muscles (or so called dorso-ventral musculature) like other molluscan groups (Haszprunar and Wanninger, 2000). Nautilus embryos: their unique concentric patterns How can we cover a large gap between the complex cephalopod body plans and the much simpler ones of other molluscs such as gastropods? The embryonic morphology is often a better guide to higher-grade evolutionary affinity than adult morphologies that vary greatly in their shapes. The plans of early stages of coleoid embryos (e.g., squid, Figure 3D) still exhibit substantial differences, because of their large eye regions, posteriorly situated collar with the funnel, and the arm buds are arranged along the transversely elongated ovoid patterns of the embryonic bodies, impeding direct comparison with those of a gastropod trochophore larva and adults. An attempt to resolve this problem came from the observation of living Nautilus embryos (Arnold and Carson, 1986; Arnold, 1987). The six variously staged embryos of Nautilus belauensis were successfully collected and the external morphology was observed. The embryos were direct developers characterized by a very large outer yolk sac. The egg size is the biggest of all invertebrates, and nearly one year is needed for their development to hatching. The embryonic bodies are more elongate along the AP axis compared to those

Figure 1. A classic example for the comparison of internal organs between a bird and an octopus. Cuvier used this figure to support his functionalism opposed to Geoffroys morphology. The dorsal side of octopus body corresponds to the ventral side of the vertebrate, showing similar U-shaped digestive organs. However, the large part of the brain is located dorsally in the vertebrate in contrast to the opposite side. The figure is from Cuvier (1830).

the shell of gastropods. This scheme supposes that cephalopod arms were developed from the whole foot region of a gastropod, and that the collar was derived from the epipodial region. Basically, concerning the DV axis, this view has long been adopted by subsequent authors (Raven, 1958; Seidel, 1960; Fioroni, 1978; Boletzky, 2003, 2006; Shigeno et al., 2008). Bandel and Boletzky (1988) suggested that cephalopod arms were derivates from the overall foot region, the funnel also a modification of the posterior foot (Boletzky, 1989, 1993). However, some different ideas also have been proposed about the concept on AP axis, for example, that the pre-trocheal head region of the spiralian trochophore larva corresponds to the location of the shell gland in cephalopods, given the apical position of the animal pole (Fioroni, 1978). To date, we can use a large amount of histological data for understanding development of each organ system in coleoids (see Fioroni, 1978; Budelmann et al ., 1997). However, when in the 20th century molecular research took the forefront, the developmental study of cephalopods fell out of favor, due to the lack of a model species amenable to molecular biology. As a result, unfortunately, the previous evolutionary hypotheses as

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Figure 2. Traditional views to explain the evolutionary transition of cephalopod body plans. Above: the arms as foot hypothesis by Naef (1928). The cephalopod arms are derived from the overall region of the foot. Below: the arms as head hypothesis by Holland (1987) based on Yochelson (1973). The five arm pairs are derived from the head and an anterior region of the foot surrounding the mouth. The posterior foot transforms into the funnel folds of the cephalopods. In this scenario, the arm-head needs to rotate ventrally since the funnel of cephalopods is located more dorso-posterior part of the body. (Figures were modified from the original of Naef (1928) and Holland (1987) with permission by Geological Society of London).

of coleoids. The cephalic compartment is situated at the most anterior, and the tentacle buds are arranged along each lateral side of the embryonic bodies. Following these findings, a more detailed analysis was conducted on the embryonic shell (Arnold et al., 1987; Tanabe and Uchiyama, 1997). Recently, the unknown earlier stages of Nautilus pompilius were analyzed, and the outline of developmental sequence was finally described (Figure 3A-C; Shigeno et al., 2008). The early arrangement of Nautilus embryonic bodies obviously exhibits a shared overall pattern with that of adult gastropods and of coleoid embryos (Figure 3D). The primordia of body parts are arranged in a concentric circle geometry; the central (the shell field and mantle), medio-lateral (the epipodial region or collar with funnel), and the lateral most (the foot or tentacle/arm buds). Compared to the patterns of an adult gastropod, Nautilus and coleoid embryo show; (1) a posterior enlargement of the head or cephalic compartment, (2) a morphological distinction of the

collar and funnel compartment, and (3) the appearance of the segmental buds in the whole foot compartment. This conserved configuration of organ systems seems to construct a topographical basis to explain how molluscan body plans evolved, since this pattern is typical and ubiquitous in molluscan groups such as monoplacophorans and polyplacophorans. The origins and early diversity of body plans: linkage to extant and fossil molluscs Recent paleontological findings have demonstrated unexpected diversity of body plans in the Ediacaran and Cambrian radiation of molluscs (Butterfield, 2006; Caron, et al. 2006; Sigwart and Sutton, 2007). The evidence from Kimberella (Fedonkin and Waggoner, 1997), Wiwaxia (Eibye-Jacobsen, 2004; Caron et al., 2006), Halkieria (Conway Morris and Peel, 1990; Vinther and Nielsen, 2005), Orthrozanclus (Conway Morris and Caron, 2007), and Odontogriphus (Caron

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Figure 3. A-C. The embryonic development of Nautilus. D. The early body plans of Nautilus display a similar geometric concentric circle pattern with the form of the primitive gastropod (Lottia gigantea) and the coleoid cephalopod (Idiosepius paradoxus). The embryos of Nautilus pompilius, lateral view. A. 3 months after oviposition, DAPI whole mount staining. B. 4 month old embryo, and C. 6 month old embryo (the shell was removed). Details for the all the Nautilus embryos are given in Shigeno et al. (2008). D. The dorsal and lateral views of an adult of Lottia gigantea, and schematic figures of the dorsal views of Nautilus and a squid Idiosepius embryo (modified from Shigeno et al. 2008). ceph, cephalic compartment or head part. I-V, arm buds or a part of tentacle buds. mus, shell muscle.

et al. , 2006) is supporting the hypothesis that the early stem-group of molluscs had always a bilaterally symmetrical concentric body and the dorso-ventrally compressed patterns as seen in a prototype of Mollusca (Haszprunar, 1992). Interestingly, Kimberella, unlike extant polyplacophorans and monoplacophorans, obviously displays a serial repetition pattern in the foot sole (Figure 4). The halwaxiid Orthrozanclus , possibly a more derived form of stem-mollusc, had one prominent shell, a head-like convex at the anterior end, and blade-like, slightly curved spines in the epipodial region (Figure 4). Given the similar topography, these characters may permit precise comparisons with Nautilus and coleoid embryonic body plans to reconstruct homological relationships. The most substantial differences in the Nautilus embryonic body plan with other stem-molluscs are the following; (1) the reduced shell field, (2) the specialization of the hood, collar, and funnel in the epipodial region, (3) the segmental four or more compartments for tentacles in the foot region, and (4) the enlargement

of the cephalic complex including large eye parts. The similarity with the early embryonic body plans does not necessarily mean a similarity with the adult plan of the real cephalopod ancestor. We have actually no information whether the common cephalopod ancestor went through a so-called larval and/or benthic juvenile stage during the ontogeny. However, in any case, the shared concentric or oval entire patterns in fossil and extant molluscs, seem to also provide a firm geometric basis for understanding the structural constraints and the evolutionary plasticity in molluscan forms. Evolutionary transition of phylotypes What kinds of events occurred during the long evolutionary process from a bilaterian ancestor to cephalopods? To address this question, a simple scenario may be helpful for a comparison among the phylotypic stages of key animals (Figure 5). The phylotype or phylotypic stage is a stage of development at which all members in the taxon look essentially the same (Slack,

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Figure 4. Topographical patterns in the fossil molluscs Kimberella and Orthozanclus with a primitive cephalopod Nautilus embryo to show the similar body plans; the segmental nature or spines developed in the foot region along the anterior-posterior axis (see inboxes for details), the anterior head part (except for Kimberella), and the oval shell morphology at the dorsal side. These views are seen from the lateral (above) and dorsal (below) side. The 3D models are reproduced for Kimberella (Fedonkin and Waggoner, 1997), Orthozanclus (Conway Morris and Caron, 2007), and Nautilus (Shigeno et al., 2008) by the three dimensional digital model software, Amorphium ver.3, EI Technology Group LLC. ceph, cephalic compartment or head part.

2003, i.e., the stage at which various adaptive pressures for changes are minimized, and therefore, the stage most likely to retain the features of the common ancestor). In cephalopod embryology, the first version of phylotype, suggested by Boletzky (2003, 2006) based on coleoid embryos, was composed of five pairs of arm rudiments, the arm base elongated from each rudiment, the anterior head with eyes, the rostral mouth, and the mantle part with concentric or oval patterns of the overall embryonic body. In the second version (Shigeno et al., 2008), different interpretations were given for the collar, funnel, head part, details of tentacles buds, and nervous systems from the data of Nautilus embryos. Based on the Nautilus embryos, interpretation for the origins of some organs was modified. The phylotypes, in any version, have to be tested by further morphological and molecular analysis. The last common bilaterian ancestor has been considered to be a creature like cnidarian planula larvae, or acoelomorphs, or annelid trochophora larvae, although there are still many controversial issues (e.g. Arendt et al., 2001; Bagua and Riutort, 2001; Holland, 2003; Erwin, 2006; Hejnol and Martindale, 2008). In any event, it may be enough to suppose that

the earliest condition already has a polarity for the AP and DV axes, and some segregated neurons and sensory ciliary cells might have been present in the anterior region (Figure 5) (Holland, 2003; Raikova et al., 2004; Hejnol and Martindale, 2008). For the common molluscan ancestor, a benthic adult form has been suggested as the molluscan prototype (Salvini-Plawen, 1972; Haszprunar, 1992), but the phylotype may be reconstructed by a developmental state such as the trochophora larva, since all extant members other than cephalopods including aplacophorans, polyplacophorans, and some other crown classes share a similar developmental patterns of the larva (Naef, 1928; Raven, 1958; Okusu, 2002; Friedrich et al., 2002; Nielsen, 2004; Nielsen et al., 2007). Notably, in the phylotype, the anterior head is figured with an apical tuft, the ventral foot region may be represented as a medial groove like an aplacophoran larva (Okusu, 2002), and the nervous system consists of the cerebral ganglia, pedal, and pleural cords as shared by all members of molluscs (Haszprunar, 1992). At this stage in the gastropods, the foot sole is particularly distinct. The mantle including the shell field, and the visceral mass develop dorsally. The tripartite neural

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Figure 5. A simplified evolutionary scheme for the possible transition from the common bilaterian ancestor to cephalopod body plans. The focus is particularly on the similar geometric patterns arranged along the conserved anterio-posterior and dorso-ventral axes with specified neural characters and novel external organs such as the shell, mantle, and the foot. Cephalopods have the largest brain in invertebrates with many differentiated lobes, though the tripartite neural cord plan of the common molluscan ancestor is still conserved (Budelmann et al., 1997). Each figure was constructed by data combined from various species to show developmentally conserved patterns. Source of fig ures: the nautiloid cephalopod (Shigeno et al., 2008), the late trochophora larva of primitive and derived gastropods (Page, 1992; Nederbragt et al., 2002a; Hejnol et al., 2007), the putative larval plan of a molluscan ancestor similar to the trochophora larva of aplacophorans (Okusu, 2002; Nielsen et al. 2007) with polyplacophorans (Voronezhskaya et al., 2002; Friedrich et al., 2002; Henry et al., 2004), and a bilaterian ancestor like an acoelomorph (Raikova et al., 2004; Hejnol and Martindale, 2008).

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Figure 6. Comparison of the ventral side of the trochophore larva and the octopus embryo (without the outer yolk sac) to show the similar inward flow of morphogenetic movement. The digestive organ formation is focused on this figure (black). The head part, ventral/ pedal neural territories, and inner yolk sac are represented by light shading. Left: a mode of amphistomy in the annelid trochophore larva (Nielsen, C., 2001; for gastropods, see also Fioroni, 1980; van Biggelaar et al., 2002). The ventral lateral sides of amphistome are to fuse leaving two openings of the anterior aperture for the mouth, and a posterior opening becomes anus. Ventral neural territories are also migrated together in the larva (Denes, et al., 2007). Right: in the early octopus embryo, the half circle midgut primordia centralize to fuse a single tube of digestive tract (large arrows) during the drastic centralization of whole bodies including neural tissues (Fuchs, 1973; Shigeno et al., unpublished). In turn, the ecto-mesodermal arm bases elongate dorsally to cover the whole head part (small arrows).

components (the cerebral, pedal, and pleural cords or ganglia) are always associated with the apical tuft of the pre-trocheal region, the foot, and the mantle/ visceral mass, respectively. It is not clear whether the gastropods and extinct basal cephalopods shared a veliger-like larva that was adapted to planktonic life. The common ancestor of gastropods and cephalopods had already established a topographical arrangement of organ systems that are commonly identifiable along the AP and DV axes (Naef, 1928) as seen in the phylotype of cephalopods (Boletzky, 2003). Based on the position of the foregut and mantle, the head part at the whole anterior region of the prototroch of

gastropods may correspond to the cephalic compartment including eyes and the cerebral cord of primitive cephalopods. Therefore, the position of the apical tuft may additionally be compared to the labial part in cephalopods. The cerebral and pleural components of the nervous systems are retained as cord-like features (Shigeno et al., 2008). If the superficial relationships are present in each organ as stated above, how is the similarity reflected in the real events of organogenesis? One similarity is seen in the comparative morphogenetic tissue movement of the trochophora larva and cephalopod embryo (Figure 6). In the comparable regions of the ventral side of both

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Figure 7. Comparative scheme to characterize the shared or unique body plans of vertebrates, insects, cephalopods, and cnidarians. The neural structure is shown by light shading or black (anterior non-Hox genes or otd/otx gene expressed territories). The foregut or esophagus is situated at the anterior part of each animal body. The Hox gene expression code is simply represented by black bars along the AP axis. The expression of decapentaplegic (dpp/BMP2/4) orthologs is similarly expressed dorsal or ventral side with a gradual or discrete manner. Though the expression of dpp in cephalopods has not been reported yet, but that of a patellogastropod appear at the dorsal side of pretrochal head region and mantle of the larva (Nederbragt et al., 2002a). The data was used from the multiple Anthox, dpp, and otx genes of sea anemone Nematostella (Finnerty et al., 2004; Matus et al., 2006; Mazza et al., 2007), the orthodenticle/otx gene, Hox code, and dpp/ BMP2-4 of fly Drosophila and a representative vertebrate (Reichert and Simeone, 2001; Holland, 2003), and the Hox genes of the squid Euprymna (Lee et al., 2003).

Origins of cephalopod body plans embryos, the similar inward or convergent movement can be identified to form two openings (mouth and anus) and a single midgut as the main part of the digestive organs. Molecular signature: how are the gene regularity networks shared? A surprising result of recent years is that the expression patterns of developmental control genes are highly conserved across animal phyla (e.g. Bruce and Shankland 1998; Arendt and Nbler-Jung, 1999; Lowe et al., 2003; Finnerty et al., 2004; Denes et al., 2007). Some key transcription factors related to the embryonic pattern formation have been studied to characterize the cephalopod body plans at the molecular level; pax-6 (Tomarev et al., 1997; Hartmann et al., 2003), Hox (Lee et al., 2003), and engrailed gene (Baratte et al., 2007; Shigeno et al., 2008). In these studies, evidence has been shown to support a conserved and derived molecular signature for developing embryos in cephalopods and other bilaterians (Figure 7). First, Hox genes of the squid exhibit a roughly colinear expression code in the arm primordium along the AP axis as seen in the segments with neural structures of insects and vertebrates (particularly, Scr, Antp, Scr/Hox5) (Arendt and Nbler-Jung, 1999; Reichert and Simeone, 2001). The expression of posterior Hox gene Abd-B / Post-2 was detected in the most posterior territory in a developmental stage of gastropods (Hinman et al., 2003 ), squids (Lee et al., 2003), and annelids (Prudhomme et al. , 2003). Interestingly, no Hox genes are ever expressed in a large part of the anterior head part, whereas otx/otd orthologous are expressed in the territories as seen in those of insects, vertebrates, annelids, and gastropods to characterize a comparable territory for the shared head parts (Arendt and Nbler-Jung, 1999; Nederbragt et al., 2002b; Hinman et al., 2003; Kulakova et al., 2007). Second, a paired domain containing transcription factor pax-6/eyeless of the squid is expressed at the early eye primordium like those of insects and vertebrates. The gene is usually expressed in the retinal cells in vertebrate and insects, however it is not seen in such cells of squids (Tomarev et al., 1997), suggesting a derived feature for photoreceptor development of cephalopods in a conserved manner of the eye evolution. Third, a homeodomain containing transcription factor Engrailed of the decabrachian cephalopods is expressed in various organ primordia such as arms, funnel, collar and the mantle (Baratte et al., 2007; Shigeno et al.,

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2008). Unlike the patterns of insects and vertebrates, the feature did not exhibit a segmental pattern as a polarity gene along the AP axis. The cephalopod engrailed also may not be involved in the neural patterning as reported in that of gastropods (Nederbragt et al., 2002a). Interestingly, the cephalopod and gastropod engrailed genes are highly expressed at structures such as the shell field and the mantle margin, suggesting a novel role in shaping such organs along the DV axis. It is still an open question whether cephalopod embryos have a shared genetic program to form a DV axis (Figure 7). However, evidence for the expression of decapentaplegic(dpp)/BMP2/4 at the dorsal side of various bilaterians including gastropods (Nederbragt et al., 2002a), and the involvement of Brachyury gene to the ventral side of foregut development (Lartillot et al., 2002) may indicate that a shared molecular signature along the body axes had already been established at a pre-bilaterian animal (Finnerty et al., 2004; Matus et al., 2006). Finally and more speculatively, if the dorsal side of vertebrates corresponds to the ventral side of molluscs, it may be possible to propose that the common inward movement on the ventral side of trochophore larva and cephalopod embryo (as seen in Figure 6) can be compared to the medial convergent movement to form the neural tube of vertebrates (as partly suggested by van den Biggelaar et al., 2002). Conclusion In this review, we have attempted to describe an evolutionary linkage between cephalopod body plans and other bilaterians with special focus on early topographic pattern formation. The patterns of organ systems have obviously displayed a conserved signature as well as evolutionary novelty. Our knowledge is too limited to elucidate the complete understanding of the origins of cephalopods; however, the emerging idea and new interpretation of recently obtained data support the conclusion that cephalopods exhibit an enigmatic evolutionary history compared to those of well investigated model animals such as insects and vertebrates. Acknowledgements We thank Takeya Moritaki, Toba Aquarium in Japan, for the collection of nautiloids. This work was supported by the postdoctoral fellowship for research aboard from the Japan Society for Promotion of Science, and Foundation of Research Institute of Marine

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Conway Morris, S., and Peel, J. S., 1990: Articulated halkieriids from the Lower Cambrian of north Greenland. Nature, vol. 345, p. 802-805. Conway Morris, S., and Caron, J. B., 2007: Lophotrochozoans halwaxiids and the early evolution of the lophotrochozoans. Science, vol. 315. p. 1255-1258. Cuvier, G., 1830: Considerations sur les Mollusques, et en Particulier sur Ics Cepisalopodes. Aususles des Sciences Naturelles, vol. 19, p. 241-259. Denes, A. S., Jekely, G., Steinmetz, P. R., Raible, F., Snyman, H., Prudhomme, B., Ferrier, D. E., Balavoine, G. and Arendt, D., 2007: Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in Bilateria. Cell, vol. 129, p. 277-288. Eibye-Jacobsen, D., 2004: A reevaluation of Wiwaxia and the polychaetes of the Burgess Shale. Lethaia, vol. 37, p. 317-335. Erwin, D. H., 2006: The developmental origins of animal body plans. In, Xiao, S., and Kaufman, A. J., eds., Neoproterozoic Geobiology and Paleobiology, p.159-197. Fedonkin, M. A., and Waggoner, B. M., 1997: The Late Precambrian fossil Kimberella is a mollusc-like bilaterian organism. Nature, vol. 388, p. 868-871. Finnerty, J. R., Pang, K., Burton, P., Paulson, D., Martindale, M. Q., 2004: Origins of bilateral symmetry: Hox and dpp expression in a sea anemone. Science, vol. 304, p. 1335-1337. Fioroni, P., 1978: Morphogenese der Tiere. G 5-I: Cephalopoden, 181p. Fischer-Verlag, New York. Fioroni, P., 1980: Zur Signifikanz des Blastoporus-Verhaltens in evolutiver Hinsich. Revue suisse de Zoologie, vol. 87, p. 261-272. Friedrich, S., Wanninger, A., Brckner, M., Haszprunar, G., 2002: Neurogenesis in the mossy chiton, Mopalia muscosa (Gould) (Polyplacophora): evidence against molluscan metamerism. Journal of Morphology, vol. 253, p. 109-117. Fuchs, E., 1973: Organo- und Histogenese des Darmsystems, embryonale Blutbildung und Dotterabbau bei Eledone cirrosa LAM. (Cephalopoda, Octopoda). Zoologische Jahrbcher, Abteilung fr Anatomie und Ontogenie der Tiere. vol. 91, p. 31-92. Griffin, L. E., 1900: The anatomy of Nautilus pompilius. Memoir of the National Academy of Sciences, vol. 8, p. 101-197. Hartmann, B., Lee P. N., Kanga Y. Y., Tomarev, S. I., de Couet S. H. G., Callaerts P., 2003: Pax6 in the sepiolid squid Euprymna scolopes: evidence for a role in eye, sensory organ and brain development. Mechanisms of Development, vol. 120, p. 177-183. Haszprunar, G., 1992: The first molluscs - small animals. Bolletino di Zoologia, vol. 59, p. 1-16. Haszprunar, G., and Wanninger, A., 2000: Molluscan muscle systems in development and evolution. Journal of Zoological Systematics and Evolutionary Research, vol. 27, p. 46-52. Hejnol, A, Martindale, M. Q., Henry, J. Q., 2007: High-resolution fate map of the snail Crepidula fornicata: The origins of ciliary bands, nervous system, and muscular elements. Developmental Biology, vol. 305, p. 63-76. Hejnol, A., and Martindale, M. Q., 2008: Acoel development supports a simple planula-like urbilaterian. Philosophical Transaction of Royal Society of London, B, vol. 363, p. 1493-1501. Henry, J.Q., Okusu, A., Martindale, M.Q., 2004: The cell lineage of the polyplacophoran, Chaetopleura apiculata: variation in the spiralian program and implications for molluscan evolution. Developmental Biology, vol. 272, p. 145-160. Hinman, V. F., OBrien, E. K., Richards, G. S., Degnan, B. M., 2003: Expression of anterior Hox genes during larval development of the gastropod Haliotis asinina. Evolution and Development, vol. 5, p. 508-521. Holland, C. H., 1987: The nautiloid cephalopods: A strange success.

Invertebrates to S.S. This study was also supported by a Grant-in-Aid from Japan Society of the Promotion of Science (No. 20540445) to T.S. References
Appel, T. A., 1987: The Cuvier-Geoffroy Debate, 307p. Oxford University Press, Oxford. Arendt, D., and Nbler-Jung, K., 1997: Dorsal or ventral: similarities in fate maps and gastrulation patterns in annelids, arthropods and chordates. Mechanisms of Development, Vol. 61, p. 7-21. Arendt, D., and Nbler-Jung, K., 1999: Comparison of early nerve cord development in insects and vertebrates. Development, vol. 126, p. 2309-2325. Arendt, D., Technau, U., Wittbrodt, J., 2001: Evolution of the bilaterian larval foregut. Nature, vol. 409, p. 81-85. Arnold, J. M, and Carlson, B. A., 1986: Living Nautilus embryos: preliminary observation. Science, vol. 232, p. 73-76. Arnold, J. M., Landman, N. H., Mutvel, H., 1987: Development of the embryonic shell of Nautilus. In, Saunders, W. B., Landman, N. H., eds. Nautilus, the biology and paleobiology in a living fossil, p. 373-400. Plenum, New York. Arnold, J. M., 1987: Reproduction and embryology of Nautilus. In, Saunders, W. B, Landman, N. H, eds. Nautilus, The biology and paleobiology in a living fossil, p. 353-372. Plenum, New York. Bagua, J., and Riutort, M., 2004: The dawn of bilaterian animals: the case of acoelomorph flatworms. BioEssays, vol. 26, p. 10461057. Bandel, K., and Boletzky, S. v., 1988: Features of development and functional morphology required in the reconstruction of early coleoid cephalopods. In, Wiedmann, J., Kullmann, J., eds. Cephalopods Present and Past, p. 231-246. Schweiz Verlags, Stuttgart. Baratte, S., Andouche, A., and Bonnaud, L., 2007: Engrailed in cephalopods: a key gene related to the emergence of morphological novelties. Development, Gene and Evolution, vol. 217, p. 353362. Boletzky, S. v., 1989: Early ontogeny and evolution: The cephalopod model viewed from the point of developmental morphology. Geobios, Special vol. 12, p. 67-78. Boletzky, S. v., 1993: The arm crown in cephalopod development and evolution: A discussion of morphological and behavioral homologies. American Malacological Bulletin, vol. 10, p. 61-69. Boletzky, S. v., 2003: Biology of early life stages in cephalopod molluscs. Advanced Marin Biology, vol. 44, p. 143-203. Boletzky, S. v., 2006: From head to footand back again: brachial crown development in the Coleoidea (Mollusca, Cephalopoda). Acta University Carolina, Geologica, vol. 49, p. 35-41. Brooks, W. K., 1880: The homology of the cephalopod siphon and arms. American Journal of Science, 3rd Ser. vol. 20, p. 288-291. Bruce, A. E., and Shankland, M., 1998: Expression of the head gene Lox22-Otx in the leech Helobdella and the origin of the bilaterian body plan. Developmental Biolology, vol. 201, p. 101-112. Budelmann, B. U., Schipp, R., Boletzky, S. v., 1997: Cephalopoda. In, Harrison, F. W., Kohn, A. J., eds. Microscopic Anatomy of Invertebrates, vol. 6A, Mollusca II, p. 119-414. Wiley-Liss., New York. Butterfield, N. J., 2006: Hooking some stem-group worms: fossil lophotrochozoans in the Burgess Shale. BioEssays, vol. 28, p. 1161-1166. Caron, J.-B., Scheltema, A., Schander, C., and Rudkin, D., 2006: A soft-bodied mollusc with radula from the Middle Cambrian Burgess Shale. Nature, vol. 442, p. 159163.

Origins of cephalopod body plans

Journal of Geological Society of London, vol. 144, p. 1-15. Holland, N. D., 2003: Early central nervous system evolution: An era of skin brains? Nature Review of Neuroscience, vol. 4, p. 617627. Kulakova, M., Bakalenko, N., Novikova, E., Cook, C.E., Eliseeva, E., Steinmetz, P. R. H., Kostyuchenko, R. P., Dondua A., Arendt, D., Akam, M., Andreeva, T., 2007: Hox gene expression in larval development of the polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa). Development, Genes and Evolution, vol. 217, p. 39-54. Lartillot, N., Lespinet O., Vervoort, M., Adoutte1, A., 2002: Expression pattern of Brachyury in the mollusc Patella vulgata suggests a conserved role in the establishment of the AP axis in Bilateria. Development, vol. 129, p. 1411-1421. Le Guyader, H., 2004: Etienne Geoffroy Saint-Hilaire: a visionary naturalist, 288p. Translated by Grene. M., University of Chicago Press, Chicago. Lee, P. N., Callaerts, P., Couet, H. G., Martindale, M. Q., 2003: Cephalopod Hox genes and the origin of morphological novelties. Nature, vol. 424. p. 1061-1065. Lowe, C. J., Wu, M., Salic, A., Evans, L., Lander, E., StangeThomann, N., Gruber, C. E., Gerhart, J., and Kischner, M., 2003: Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell, vol. 113, p. 853-865. Macdonald, J. D., 1855: On the anatomy of Nautilus umbilicatus, compared with that of Nautilus Pompilius. Philosophical Transaction of Royal Society of London B, vol. 145, p. 277-288. Matus, D. Q., Pang, K., Marlow, H., Dunn, C. W., Thomsen, G. H. and Martindale, M. Q., 2006: Molecular evidence for deep evolutionary roots of bilaterality in animal development. Proceedings of the National Academy of Sciences, vol. 103, p. 11195-11200. Mazza, M. E., Pang K., Martindale, M. Q., Finnerty, J. R., 2007: Genomic organization, gene structure, and developmental expression of three clustered otx genes in the sea anemone Nematostella vectensis. Journal of Experimental Zoology. Part B. Molecular and Developmental Evolution, vol. 308, p. 494-506. Naef, A., 19211923: Die Cephalopoden. Systematik. Fauna Flora Golf Napoli, vol. 35, p. 1863. English translation, Jerusalem, Israel program for scientific translations, available from Smithsonian Institution Libraries, Washington. Naef, A., 1928: Die Cephalopoden. Embryologie. Fauna Flora Golf Neapel, vol. 35, p. 1-357. English translation by Boletzky, S. v. 2001. The cephalopoda-embryology. Smithsonian Institution Press, Washington. Nederbragt, A. J., Loon, A. E. v., Dictus, W. J. A. G., 2002a: Expression of Patella vulgata orthologs of engrailed and dpp-BMP2/4 in adjacent domains during molluscan shell development suggests a conserved compartment boundary mechanism. Developmental Biology, vol. 246, p. 341-355. Nederbragt, A. J., Welscher, P., van den Driesche S., van Loon A. E., Dictus, W. J., 2002b: Novel and conserved roles for orthodenticle/otx and orthopedia/otp orthologs in the gastropod mollusc Patella vulgata. Development, Genes and Evolution, vol. 212, p. 330-337. Nielsen, C., 2001: Animal evolution. Interrelationships of the living phyla, 563p. Oxford University Press, Oxford. Nielsen, C., 2004: Trochophora larvae: cell-lineages, ciliary bands, and body regions. 1. Annelida and Mollusca, Journal of Experimental Zoology. Molecular and Developmental Evolution, Part B, vol. 302, p. 35-68. Nielsen, C., Haszprunar, G., Ruthensteiner, B. and Wanninger A. 2007: Early development of the aplacophoran mollusc Chaetoderma. Acta Zoologica (Stockholm), vol. 88, p. 231-247 ODor, R. K., and Webber, D. M., 1986: The constraints on cephalo-

33

pods: Why squid arent fish. Canadian Journal of Zoology, vol. 64, p. 1591-1605. Okusu, A., 2002: Embryogenesis and development of Epimenia babai (Mollusca Neomeniomorpha). Biological Bulletin, vol. 203, p. 87-103. Owen, R., 1832: Memoir on the Pearly Nautilus (Nautilus pompilius Linn.) with illustrations of its external form and internal structure. Council Royal College Surgeons, London. Packard, A., 1972: Cephalopods and fish: The limits of convergence. Biological Review vol. 47, p. 241-307. Page, L. R., 1992: New interpretation of a nudibranch central nervous system based on ultrastructural analysis of neurodevelopment in Melibe leonina. I. Cerebral and visceral loop ganglia. Biological Bulletin, vol. 182, p. 348-365. Prudhomme, B., de Rosa, R., Arendt, D., Julien, J. F., Pajaziti, R., Dorresteijn, A. W., Adoutte, A., Wittbrodt, J, and Balavoine, G., 2003: Arthropod- like expression patterns of engrailed and wingless in the annelid Platynereis dumerilii suggest a role in segment formation. Current Biology, vol. 13, p. 1876-1881. Raikova, O. I., Reuter, M., Gustafsson, M. K. S., Maule, A. G., Halton, D.W., and Jondelius, U., 2004: Evolution of the nervous system in Paraphanostoma (Acoela). Zoological Scripta, vol. 33, p. 71-88. Raven, C., 1958: Morphogenesis. The analysis of molluscan development, 311p. Pergamon Press, New York. Reichert, H., and Simeone, A., 2001: Developmental genetic evidence for a monophyletic origin of the bilaterian brain. Philosophical Transaction of the Royal Society of London Ser. B, vol. 356, p. 1533-44. Salvini-Plawen, L. v., 1972: Zur Morphologie und Phylogenie der Mollusken: die Beziehungen der Caudofoveata und der Solenogastres als Aculifera, als Mollusca und als Spiralia. Zeitschrift fur Weissenschaftliche Zoologie, vol. 184, p. 205-394. Salvini-Plawen, L. v. and Steiner, G., 1996: Synapomorphies and plesiomorphies in higher classification of Mollusca. In, Taylor J. (ed). Origin and evolutionary radiation of the Mollusca, p. 29-51. Oxford University Press, Oxford. Saunders, W. B., and Landman, N. H., eds., 1987: Nautilus: The biology and paleobiology of a living fossil, 636p. New York, Plenum. Sacarrao, G. F., 1962: On the position of the ontogeny of cephalopods in relation to the development of the other molluscs. Revista Faculdade Ciencias Lisboa (2nd series), vol. 10, p. 1-54. Seidel, F., 1960: Krpergrundgestalt und Keimstruktur Eine Errterung ber die Grundlagen der vergleichenden und experimentellen Embryologie und deren Gltigkeit bei phylogenetischen berlegungen. Zoologischer Anzeiger, vol. 164, p. 245-305. Shigeno, S., Sasaki, T., Moritaki, T., Kasugai, T., Vecchione, M., Agata, K., 2008: Evolution of the cephalopod head complex by assembly of multiple molluscan body parts: evidence from Nautilus embryonic development. Journal of Morphology, vol. 269, p. 1-17. Sigwart, J. D., and Sutton, M. D., 2007: Deep molluscan phylogeny: synthesis of palaeontological and neontological data. Proceedings of the Royal Society of London Ser. B, vol. 274, p. 24132419. Slack, J. M., 2003: Phylotype and zootype, In, Hall, B. K., and Olson, W. M., eds. Keywords and concepts in evolutionary developmental biology, p. 309-318. Harvard Univ. Press, London. Tanabe, K., and Uchiyama, K., 1997: Development of the embryonic shell structure in Nautilus. Veliger, vol. 40, p. 203-215. Tomarev, S. I., Callaerts, P., Kos, L., Zinovieva, R., Halder, G., Gehring, W. J., and Piatigorsky, J., 1997: Squid Pax6 and eye development. Proceedings of the National Academy of Science USA,

34

Shuichi Shigeno et al.

25-38. Willey, A., 1902: Contribution to the natural history of the pearly Nautilus. In: Willey A, editor. Zoological Results Based on Material from New Britain, New Guinea, Loyalty Islands and elsewhere, collected during the years 1895, 1896 and 1897, vol. 6, p. 75-83 and p. 691-830. Cambridge University Press, Cambridge. Yochelson, E. L., Flower, R. H., Webers, G.. F., 1973: The bearing of the new late Cambrian monoplacophoran Knightconus upon the origin of the Cephalopoda. Lethaia, vol. 6, p. 275-309.

vol. 94, p. 2421-2426. van den Biggelaar, J. A. M, Edsinger-Gonzales, E., Schram, F. R., 2002: The improbability of dorso-ventral axis inversion during animal evolution as presumed by Geoffroy Saint Hilaire. Contributions to Zoology, vol. 71, p. 29-36. Vinther, J., and Nielsen, C., 2005: The Early Cambrian Halkieriais a mollusc. Zoologica Scripta, vol. 34, p. 81-89. Voronezhskaya, E. E., Tyurin, S.A., Nezlin, L. P., 2002: Neuronal development in larval chiton Ischnochiton hakodadensis (Mollusca: Polyplacophora). Journal of Comparative Neurology, vol. 444, p.