Conference PaperPDF Available

The origins of cephalopod body plans

Figures

Content may be subject to copyright.
Tanabe, K., Shigeta, Y., Sasaki, T. & Hirano, H. (eds.) 2010. Cephalopods - Present and Past
Tokai University Press, Tokyo, p. 23-34.
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; O’Dor and Webber, 1986).
To address the linkage between these two
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
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
1Department of Neurobiology, University of Chicago, 947 East 58th Street, Chicago, IL 60637, USA
(*corresponding author; e-mail: sshigeno@uchicago.edu)
2The University Museum, University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan (e-mail: sasaki@um.u-tokyo.ac.jp)
3C.N.R.S., Observatoire Océanologique, 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
Shuichi Shigeno et al.24
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
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
ndings 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 afnity 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 inter-
nal organs between a bird and an octopus. Cuvier used this gure
to support his functionalism opposed to Geoffroy’s 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 ver-
tebrate in contrast to the opposite side. The gure is from Cuvier
(1830).
Origins of cephalopod body plans 25
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 ndings, 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 (Buttereld, 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
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 ve 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 modied from the original of Naef (1928) and Holland (1987)
with permission by Geological Society of London).
Shuichi Shigeno et al.26
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 rm 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,
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 gures of the dorsal views of Nautilus and a squid Idiosepius embryo (modied from Shigeno
et al. 2008). ceph, cephalic compartment or head part. I-V, arm buds or a part of tentacle buds. mus, shell muscle.
Origins of cephalopod body plans 27
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 rst version of phylotype,
suggested by Boletzky (2003, 2006) based on coleoid
embryos, was composed of ve 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; Baguañà 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
gured 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
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.
Shuichi Shigeno et al.28
Figure 5. A simplied 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
specied neural characters and novel external organs such as the shell, mantle, and the foot. Cephalopods have the largest brain in inverte-
brates with many differentiated lobes, though the tripartite neural cord plan of the common molluscan ancestor is still conserved (Budelmann
et al., 1997). Each gure was constructed by data combined from various species to show developmentally conserved patterns. Source of g-
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).
Origins of cephalopod body plans 29
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 reected 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
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 ow of morphogenetic movement. The digestive organ formation is focused on this gure (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 migrat-
ed 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).
Shuichi Shigeno et al.30
Figure 7. Comparative scheme to characterize the shared or unique body plans of vertebrates, insects, cephalopods, and cnidar-
ians. 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 y Drosophila and a representative vertebrate (Reichert and Simeone, 2001; Holland, 2003), and the Hox genes of the squid Eu-
prymna (Lee et al., 2003).
Origins of cephalopod body plans 31
embryos, the similar inward or convergent movement
can be identied 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 Nübler-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 Nübler-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 (Prud’homme 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 Nübler-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.,
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
Shuichi Shigeno et al.32
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 Uni-
versity Press, Oxford.
Arendt, D., and Nübler-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 Nübler-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 bilat-
erian larval foregut. Nature, vol. 409, p. 81-85.
Arnold, J. M, and Carlson, B. A., 1986: Living Nautilus embryos: pre-
liminary 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.
Baguañà, J., and Riutort, M., 2004: The dawn of bilaterian animals:
the case of acoelomorph atworms. BioEssays, vol. 26, p. 1046-
1057.
Bandel, K., and Boletzky, S. v., 1988: Features of development and
functional morphology required in the reconstruction of early co-
leoid cephalopods. In, Wiedmann, J., Kullmann, J., eds. Cephalo-
pods Present and Past, p. 231-246. Schweiz Verlags, Stuttgart.
Baratte, S., Andouche, A., and Bonnaud, L., 2007: Engrailed in ce-
phalopods: a key gene related to the emergence of morphological
novelties. Development, Gene and Evolution, vol. 217, p. 353-
362.
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 homol-
ogies. American Malacological Bulletin, vol. 10, p. 61-69.
Boletzky, S. v., 2003: Biology of early life stages in cephalopod mol-
luscs. Advanced Marin Biology, vol. 44, p. 143-203.
Boletzky, S. v., 2006: From head to foot–and 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 Bur-
gess Shale. Nature, vol. 442, p. 159–163.
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 hal-
waxiids 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.,
Prud’homme, 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 poly-
chaetes 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 Geobiol-
ogy 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 Signikanz des Blastoporus-Verhaltens in evo-
lutiver Hinsich. Revue suisse de Zoologie, vol. 87, p. 261-272.
Friedrich, S., Wanninger, A., Brückner, 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, embryo-
nale Blutbildung und Dotterabbau bei Eledone cirrosa LAM.
(Cephalopoda, Octopoda). Zoologische Jahrbücher, Abteilung
für Anatomie und Ontogenie der Tiere. vol. 91, p. 31-92.
Grifn, 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 sco-
lopes: evidence for a role in eye, sensory organ and brain devel-
opment. Mechanisms of Development, vol. 120, p. 177-183.
Haszprunar, G., 1992: The rst 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. De-
velopmental Biology, vol. 272, p. 145-160.
Hinman, V. F., O’Brien, 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.
Origins of cephalopod body plans 33
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. 617-
627.
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: Expres-
sion 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: Ce-
phalopod 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., Stange-
Thomann, 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 Trans-
action 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 evolu-
tionary 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: Ge-
nomic organization, gene structure, and developmental expres-
sion 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., 1921–1923: Die Cephalopoden. Systematik. Fauna Flora
Golf Napoli, vol. 35, p. 1–863. English translation, Jerusalem,
Israel program for scientic translations, available from Smithso-
nian 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: Expres-
sion of Patella vulgata orthologs of engrailed and dpp-BMP2/4
in adjacent domains during molluscan shell development sug-
gests a conserved compartment boundary mechanism. Develop-
mental 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 orthoden-
ticle/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 Experi-
mental 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 Chaeto-
derma. Acta Zoologica (Stockholm), vol. 88, p. 231-247
O’Dor, R. K., and Webber, D. M., 1986: The constraints on cephalo-
pods: Why squid aren’t sh. 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 struc-
ture. Council Royal College Surgeons, London.
Packard, A., 1972: Cephalopods and sh: 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.
Prud’homme, 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 wing-
less 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 develop-
ment, 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 Sole-
nogastres 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 classication 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 biol-
ogy and paleobiology of a living fossil, 636p. New York, Ple-
num.
Sacarrao, G. F., 1962: On the position of the ontogeny of cephalopods
in relation to the development of the other molluscs. Revista Fac-
uldade Ciencias Lisboa (2nd series), vol. 10, p. 1-54.
Seidel, F., 1960: Körpergrundgestalt und Keimstruktur – Eine Erörter-
ung über die Grundlagen der vergleichenden und experimentel-
len Embryologie und deren Gültigkeit bei phylogenetischen
Überlegungen. 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 Nau-
tilus 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. Proceed-
ings of the Royal Society of London Ser. B, vol. 274, p. 2413-
2419.
Slack, J. M., 2003: Phylotype and zootype, In, Hall, B. K., and Olson,
W. M., eds. Keywords and concepts in evolutionary developmen-
tal 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., Ge-
hring, W. J., and Piatigorsky, J., 1997: Squid Pax6 and eye devel-
opment. Proceedings of the National Academy of Science USA,
Shuichi Shigeno et al.34
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. Contri-
butions 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 de-
velopment in larval chiton Ischnochiton hakodadensis (Mollusca:
Polyplacophora). Journal of Comparative Neurology, vol. 444, p.
25-38.
Willey, A., 1902: Contribution to the natural history of the pearly Nau-
tilus. 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.

Supplementary resource (1)

Article
Significance A theoretical model suggests that a mechanically induced twist of the soft body underlies the formation of helicospiral shells in snails and ammonites and also accounts for the startling and unique meandering shells observed in certain species. This theory addresses fundamental developmental issues of chirality and symmetry breaking: in the case of ammonites, how a bilaterally symmetric body can sometimes secrete a nonsymmetric shell; for gastropods, how an intrinsic twist possibly due to the asymmetric development of musculature can provide a mechanical motor for generating a chiral shell. Our model highlights the importance of physical forces in biological development and sheds light on shell coiling in snails, which have been used for a century as model organisms in genetic research.
Book
This volume is a reprint of a classic book about Nautilus, first published in 1987, with an introductory chapter summarizing all of the work on Nautilus and its habitat since the publication of the first edition more than 20 years ago. The surge in articles in the last two decades indicates an expanded interest in the subject, reflecting a renewed appreciation of the complexity and fragility of the marine habitat and its biota. The 37 chapters are written by 48 experts in the field and cover all aspects of this living fossil from its ecology to its embryology. This volume also features new photos, including an impressive image of the first hatched Nautilus in captivity. Nautilus is an iconic animal in the marine realm and represents part of the diverse fauna of the Indo-Pacific. It is also a member of a lineage of shelled cephalopods dating back more than 400 million years. As a result, this volume will be relevant to the fields of marine science, evolutionary biology, and paleontology.
Article
The so-called arm crown (brachial crown) of the Cephalopoda is the most conspicuous part of the pedal complex in this class of molluscs (earlier reports claiming a cephalic nature of arms notwithstanding). In contrast to what is expected of an archetypal "molluscan foot", the brachial appendages of coleoid cephalopods are able to perform very complex motor actions, individually, in pairs (e. g. ejectible tentacles) or in concert (whole arm crown, with or without web). The brachial armament (suckers, sucker-derived structures) adds another level of functional integration to those of the brachial crown and of the individual arms. Proximally the arm crown of cephalopods is very closely associated with the cephalic complex, as reflected by the technical term cephalopodium (designating the "head-foot"). In the ontogeny of cephalopods, this close morphological association and functional integration of the foot and the head is achieved during advanced stages of embryogenesis. The ventral parts are finally marked by a pseudo-radial arrangement, in that the brachial appendages encircle the mouth ("circum-oral" appendages), whereas the dorsal parts (funnel tube, secondary head cover with extraocular eye muscles) continue to reveal the original bilateral symmetry.
Article
The origin of the cephalopods from the Monoplacophora is briefly considered. The first rare Upper Cambrian Plectronoceras are known to be succeeded by a later Cambrian radiation involving the Plectronoceratida, Ellesmeroceratida, and two other orders, all well documented from Chinese occurrences. The greatest success of the nautiloid cephalopods came in the Ordovician Period with three evolutionary pulses in the Tremadoc, Arenig, and later Ordovician. Three particular Palaeozoic problems are treated: gigantism in cephalopods, the orthocone operculum Aptychopsis, and the Chinese Pagoda Limestone as an example of an 'Orthoceras' limestone. Devonian developments included the origin of the ammonoids through their first suborder, the Bactritina; the origin of the coleoids; and the beginning of the long history of the coiled Nautilida. After a brief aside on the classification of the cephalopods, the Nautilida are treated in terms of their survival after the extinction of the ammonoids. Finally, there are comments on the living Nautilus.-Author
Chapter
Embryology increasingly came to be viewed as the way to understand relationships among different groups of organisms. As discussed in the first section of this chapter, Von Baer played a pivotal role in this development. His ideas were rapidly assimilated into Britain as scientists there responded to the implications of the Geoffroy-Cuvier debate (s. 5.2). Richard Owen made a lasting impact when he separated homology from analogy (s. 5.3), and Darwin took account of these developments in formulating his theory (s. 5.4). The search for embryological archetypes and establishment of an evolutionary embryology was carried furthest by Ernst Haeckel in Germany and Francis Balfour in England. By the late 19th century a solution to the generation of organismic form appeared to be at hand in homologous germ layers and conserved stages of embryonic development. This evolutionary embryology was applied to relationships among organisms and in a search for the ancestors of the vertebrates (s. 5.5).