Molecular phylogeny of Scaphopoda (Mollusca) inferred

from 18S rDNA sequences: support for a Scaphopoda

Cephalopoda clade
Blackwell Publishing Ltd.

GERHARD STEINER & HERMANN DREYER

Accepted: 15 September 2002

Steiner, G. & Dreyer, H. (2003). Molecular phylogeny of Scaphopoda (Mollusca) inferred

from 18S rDNA sequences: support for a ScaphopodaCephalopoda clade. Zoologica Scripta,
32, 343 356.
The phylogenetic relationships of the Scaphopoda, one of the lesser molluscan classes, with
the other conchiferan taxa are far from clear. They appear either as the sister-group to the
Bivalvia (Diasoma concept) or to a GastropodaCephalopoda clade or to the Cephalopoda
alone (helcionellid concept). We compiled a 18S rDNA sequence dataset of 48 molluscan species containing 17 scaphopods to test these hypotheses and to address questions regarding
high-level relationships with the Scaphopoda. Both parsimony and maximum likelihood trees
show low branch support at the base of the Conchifera, except for the robust clade uniting
Scaphopoda and Cephalopoda. This result is corroborated by spectral analysis and likelihood
mapping. We also tested alternative topologies which scored signicantly worse both in tree
length and in likelihood. The 18S rDNA data thus reject the Diasoma in favour of a Scaphopoda
Cephalopoda clade as proposed in the helcionellid concept. When plotted on the molecular tree, the pivotal morphological characters associated with the burrowing life style of the
Bivalvia and Scaphopoda, i.e. mantle/shell enclosure of the body and the burrowing foot with
true pedal ganglia, appear convergent in these groups. In contrast, the prominent and tilted
dorsoventral body axes, multiple cephalic tentacles and a ring-shaped muscle attachment on
the shell are potential synapomorphies of Scaphopoda and Cephalopoda. Most of the higher
taxa within the Scaphopoda are supported by the molecular data. However, there is no support
for the families Dentaliidae and Gadilidae. The basal position of the Fustiariidae within the
Dentaliida is conrmed.
Gerhard Steiner & Hermann Dreyer, Institute of Zoology, University of Vienna, Althanstr. 14,
A-1090 Vienna, Austria. E-mail: gerhard.steiner@univie.ac.at

Introduction
Scaphopoda is one of the less diverse major groups of conchiferan molluscs, with about 520 Recent species (Steiner &
Kabat 2001; Steiner & Kabat 2001) living in all types of
unconsolidated marine sediments (Shimek & Steiner 1997).
Scaphopoda are adapted to their infaunal habit by a tubular
mantle/shell, open at both ends, and a burrowing foot; there
are no gills or osphradia (Steiner 1992; Shimek & Steiner
1997). They are generally considered to be microcarnivores
collecting their prey items (mainly foraminifers) with numerous captacula cerebrally innervated cephalic appendages
and processing them with a large radula apparatus
(Shimek 1988, 1990; Palmer & Steiner 1998).
The phylogenetic relationships of Scaphopoda with the
other conchiferan taxa are far from settled. There are two
competing basic concepts: (1) the DiasomaCyrtosoma

The Norwegian Academy of Science and Letters Zoologica Scripta, 32, 4, July 2003, pp343 356

(Runnegar & Pojeta 1974; Pojeta & Runnegar 1976) or

LoboconchaVisceroconcha (Salvini-Plawen 1980) concept
proposing a ScaphopodaBivalvia vs. Gastropoda
Cephalopoda clade; and (2) the helcionellid concept (Peel
1991) placing Scaphopoda closer to, or within, the Gastropoda
Cephalopoda lineage (Fig. 1A,B). Neither concept was
fundamentally new at the time of proposal. The idea that
Scaphopoda and Bivalvia are closely related was introduced by
Lacaze-Duthiers (185758) who emphasized the similarities
in the weakly developed head, pedal morphology and in the
formation of mantle and shell. This was further developed by
Runnegar & Pojeta (1974; Pojeta & Runnegar 1976, 1979, 1985)
proposing the Rostroconchia, a palaeozoic group of laterally
compressed, pseudo-bivalved molluscs, as the common stem
group of Bivalvia and Scaphopoda and coining the term Diasoma for this lineage. The concept was widely accepted (e.g.
343

Molecular phylogeny of Scaphopoda G. Steiner & H. Dreyer

Fig. 1 AD. Competing hypotheses on the

phylogeny of extant conchiferan classes tested

in this study. A. DiasomaCyrtosoma (after
Pojeta & Runnegar 1976) or Loboconcha
Visceroconcha (Salvini-Plawen 1980, 1990),
with fossil Rostroconchia as stemgroup of
Scaphopoda and Bivalvia. B. Helcionellid
concept (Waller 1998), with fossil Helcionellida as stemgroup of Scaphopoda and Cephalopoda; ScaphopodaCephalopoda clade also
according to Grobben (1886). C. Modied
Visceroconcha concept (Haszprunar 2000).
D. ScaphopodaGastropoda clade according
to Plate (1892) and Simroth (1894).

Engeser & Riedel 1996; Ponder & Lindberg 1997; Reynolds

& Okusu 1999; Salvini-Plawen 1980, 1990; Salvini-Plawen &
Steiner 1996; Wagner 1997) although Steiner (1992, 1996)
pointed out discrepancies in the development of body axes
between Rostroconchia and Scaphopoda.
Connecting Scaphopoda to the GastropodaCephalopoda
line has a similarly long tradition. A close relationship of
Scaphopoda and Gastropoda based on the similarities of
branched head tentacles, prominent dorsoventral body axes
and the occurrence of shell slits was proposed by Plate (1892)
and Simroth (1894) (Fig. 1D). The common derivation of
Scaphopoda and Cephalopoda was favoured by Grobben
(1886) using similar arguments. These hypotheses have
recently gained new support. Waller (1998) elaborated on
and modied the helcionellid concept of Peel (1991) by
deriving the ScaphopodaCephalopoda line from helcionellid monoplacophorans as the sister-group of Gastropoda. In
a recent cladistic analysis of morphological data, Haszprunar
(2000) proposed Scaphopoda as the sister taxon of Gastropoda and Cephalopoda (Fig. 1C). The alternative to identifying any of the extant classes of Conchifera as sister-groups
and deriving Scaphopoda directly from an unknown, independent monoplacophoran stock was suggested by Edlinger
(1991), while Starobogatov (1974) and Chistikov (1979)
identied the palaeozoic Xenoconchia as the closest relatives
of Scaphopoda. Yochelson (1978, 1979) even considered the
derivation of an un-shelled ancestor.
This variety of competing phylogenetic hypotheses is
partly due to the lack of information provided by the fossil
record. Scaphopoda are the latest to appear in the fossil
344

record among all conchiferan classes, and there are no obvious transitional forms connecting them to other molluscs.
The oldest scaphopod reported is the Ordovician Rhytiodentalium kentuckyesnis Pojeta & Runnegar, 1979, although its
scaphopod nature has been questioned by Engeser & Riedel
(1996), as has that of several Devonian and Carboniferous
scaphopods (Yochelson 1999; Yochelson & Goodison 1999;
Palmer 2001).
It is evident from the competing hypotheses that we
have to deal with convergent morphologies in several organ
systems. The pivotal characters involved (discussed in
Haszprunar 2000; Reynolds & Okusu 1999; Steiner 1992, 1998,
1999a; Waller 1998) are listed in Table 1. Depending on the
topology of the conchiferan phylogenetic tree, at least one of
the sets of similarities must have arisen convergently. If the
DiasomaCyrtosoma/LoboconchaVisceroconcha concept
is favoured, elongation of the dorsoventral body axis (multiple) cephalic tentacles, and the ring-shaped attachment of
the dorsoventral body muscles (Mutvei 1964; Yochelson et al.
1973) must have evolved convergently in Scaphopoda and the
Cyrtosoma/Visceroconcha. If, however, the helicionellid
concept is assumed, the ventral mantle/shell extension with
similar innervation of the anterior mantle regions, epiatroid
nervous system with fully concentrated pedal ganglia, and
burrowing foot evolved convergently in the Scaphopoda
and Bivalvia. When faced with a tie like that, a morphologyindependent dataset such as that provided by DNA sequences
may help in addressing this question.
The relationships of the higher taxa within Scaphopoda
are only partly resolved. Cladistic analysis of morphological

Zoologica Scripta, 32, 4, July 2003, pp343 356 The Norwegian Academy of Science and Letters

G. Steiner & H. Dreyer Molecular phylogeny of Scaphopoda

Table 1 Potential synapomorphies of

Scaphopoda with Bivalvia, Gastropoda, and
Cephalopoda. Scoring refers to the
presumed ancestral states for each class.
Numbering of characters corresponds to that
of Fig. 7.

1
2
3
4
5
6
7

Scaphopod character states

Bivalvia

Gastropoda

Cephalopoda

Lateroventral extension of mantle-shell enclosing body

Burrowing foot with functionally hydraulic component
Epiatroid nervous system with true pedal ganglia
Visceral connectives lateral of dorsoventral muscles
Prominent dorsoventral body axis with resulting
U-shaped gut
More than two cephalic tentacles
Ring-shaped attachment of dorsoventral muscles

+
+
+
+

+
+

Fig. 2 Phylogenetic relationships of scaphopod family group taxa

from morphological data after Steiner (1998, 1999a). Taxa in
boldface are represented in the present molecular dataset.

data (Reynolds 1997; Reynolds & Okusu 1999; Steiner 1992,

1998, 1999a) has supported the basic dichotomy separating
the monophyletic Dentaliida and Gadilida and returned
identical topologies within the Gadilida: (Entalinidae
(Pulsellidae (Wemersoniellidae, Gadilidae))) (Fig. 2). In contrast, relationships of the dentaliid family taxa are less clear
due to the lack of reliable morphological characters for this
systematic level and to uncertain monophyly of certain
families and genera (Reynolds & Okusu 1999; Steiner 1998,
1999a). There is agreement on the basal position of the
Gadilinidae, but the position of the Fustiariidae is controversial. Reynolds & Okusu (1999) placed it in a derived position
as the sister-group of the Dentaliidae, whereas Steiner (1998,
1999a) recovered it either as a sister-group to the Gadilinidae
or in a position between Gadilinidae and the other dentaliid
families. In addition to these uncertainties, the relationships
of the families Laevidentaliidae, Calliodentaliidae, and Rhabdidae are completely unresolved.

The Norwegian Academy of Science and Letters Zoologica Scripta, 32, 4, July 2003, pp343 356

Having been used only as outgroup taxa in molecular

analyses of other molluscan groups, Scaphopoda are rather
under-represented in molecular data sets. There are three
partial cytochrome-oxidase-I sequences (Hoeh et al. 1998;
Giribet & Wheeler, 2002), two partial engrailed sequences
(Wray et al. 1995), three partial 28S rDNA sequences
(Rosenberg et al. 1997; Giribet & Wheeler, 2002) and ve
near-complete 18S rDNA sequences (Winnepenninckx et al.
1996; Giribet et al. 2000; Steiner & Hammer 2000) available
in GenBank. Inadequate representation of the crown-group
conchiferan taxa, at least of Scaphopoda and Cephalopoda,
and/or the use of inadequate molecular markers for resolving
conchiferan relationships (e.g. Rosenberg et al. 1997)
accounts for the lack of information on this question from the
molecular side.
In order to test the morphological data against an independent data set we obtained near-complete 18S rDNA
sequences of 12 scaphopod species from ve families and
aligned them to the existing ones and to a selected set of
gastropods, bivalves and cephalopods, using the available
polyplacophorans as outgroup. The resulting trees provide
a guideline for interpreting the patterns of homology of the
disputed morphological characters and for assessing the
sister-group of the Scaphopoda. Although some of the scaphopod family group taxa, especially those of the Dentaliida, are
not represented in the present data set, we are able to address
also some of their high-rank internal relationships.

Materials and methods

Most of the specimens were collected by dredging in the
North Atlantic off Trondheim, Norway, and south of Iceland;
Dentalium austini was collected from western Australia and
Fustiaria rubescens from Greece (Table 2).
DNA extraction, amplification and sequencing
Living specimens were xed in ethanol (96%) or frozen in
liquid nitrogen at 70 C. Total DNA was isolated from the
entire soft body (small specimens) or pieces of tissue (larger
specimens) of 12 scaphopods (eight Gadilida and four Dentaliida) with the DNeasy Tissue Kit (Qiagen) or with CTAB
(Winnepenninckx et al. 1993a).
345

Molecular phylogeny of Scaphopoda G. Steiner & H. Dreyer

Table 2 Species used in the phylogenetic analysis, arranged systematically, with GenBank accession numbers, sources, and sampling location

for those sequenced in this study.

Systematic position
Scaphopoda
Dentaliida
Dentaliidae

Rhabdidae
Fustiariidae
Gadilida
Entalimorpha
Entalinidae
Entalininae
Heteroschismoidinae

Gadilimorpha
Pulsellidae

Gadilidae
Siphonodentaliinae

Gadilinae

Bivalvia
Protobranchia
Solemyida
Solemyidae

346

Species

GenBank no.

Authors

Antalis pilsbry (Rehder, 1942)

Antalis inaequicostata (Dautzenberg, 1891)
Antalis vulgaris (Da Costa, 1778)
Antalis perinvoluta (Boissevain, 1906)
Dentalium austini (Lamprell & Healy, 1998)

AF120522
AJ389660
X91980
AJ389663
AF490594

Giribet et al. (2000)

Steiner & Hammer (2000)
Winnepenninckx et al. (1996)
Steiner & Hammer (2000)
this study

Fissidentalium capillosum (Jeffreys, 1877)

AF490596

this study

Fissidentalium candidum (Jeffreys, 1877)

AF490595

this study

Rhabdus rectius (Carpenter, 1864)

Fustiaria rubescens (Deshayes, 1825)

AF120523
AF490597

Giribet et al. (2000)

this study

Entalina tetragona (Brocchi, 1814)

Heteroschismoides subterfissum (Jeffreys, 1877)

AF490598
AF490599

this study
this study

Sampling locality

Watering Cove, Burrup

Dampier, NW Australia
Peninsula
BIOICE st. 3188, 6209.15
6208.73 N
2700.322701.31 W, 1339
1338 m
BIOICE st. 3172, 6005.42
6005.68 N
2051.302049.76 W, 2709 m
Near Athens, Greece

Trondheim Fjord, Norway

BIOICE st. 3167, 6054.88
6055.28 N
2247.262247.62 W, 1897
1899 m

Pulsellum affine (M. Sars, 1865)

AF490600

this study

BIOICE st. 3167, 6054.88

6055.28 N
2247.262247.62 W, 1897
1899 m

AF490601

this study

Polyschides olivi (Scacchi, 1835)

AF490602

this study

Cadulus subfusiformis (M. Sars, 1865)

Cadulus sp. A

AF490603
AF490604

this study
this study

Cadulus sp. B

AF490605

this study

BIOICE st. 3161, 6237.08

6237.59 N
2321.792321.48 W, 1230
1300 m
BIOICE st. 3187, 6209.04
6208.67 N
2700.742701.23 W, 1327
1326 m
Trondheim Fjord, Norway
BIOICE st. 3181, 6052.86
6052.62 N
2647.722648.30 W, 1543
1562 m
BIOICE st. 3173, 6005.38
6005.59 N
2051.232052.11 W, 2709
2710 m

Solemya reidi (Bernard, 1980)

Solemya togata (Poli, 1795)

AF117737
AJ389658

Distel (2000)
Steiner & Hammer (2000)

Siphonodentalium lobatum (Sowerby, 1860)

Zoologica Scripta, 32, 4, July 2003, pp343 356 The Norwegian Academy of Science and Letters

G. Steiner & H. Dreyer Molecular phylogeny of Scaphopoda

Table 2 continued.
Systematic position
Nuculida
Nuculanoidea
Nuculanidae

Neionellidae
Pteriomorpha
Arcoidea
Arcidae
Mytiloidea
Modiolinae
Mytilinae
Pterioidea
Pinnidae
Heteroconchia
Unionida
Unionidae
Carditoidea
Carditidae
Solenoidea
Pharidae
Veneroidea
Ungulinidae
Cyamioidea
Sportellidae
Gastropoda
Neritopsina
Neritidae
Vetigastropoda
Trochidae
Fissurellidae
Caenogastropoda
Nassariidae
Bursidae
Calyptraeidae
Cephalopoda
Nautiloidea
Nautilidae
Coleoidea
Loliginidae
Sepiidae
Polyplacophora
Ischnochitonina
Chitonidae
Acanthochitonina
Acanthochitonidae
Lepidopleurina
Lepidopleuridae

Species

GenBank no.

Authors

Nuculana minuta (O. F. Mller 1776)

Nuculana pella (Linn, 1767) Solemyida
Yoldiella nana (M. Sars, 1865)
Neilonella subovata (Verrill & Bush, 1897)

AF120529
AJ389665
AJ389659
AF207645

Giribet & Wheeler (2002)

Steiner & Hammer (2000)
Steiner & Hammer (2000)
Giribet & Wheeler (2002)

Arca noae (Linn, 1758)

Acar plicata (Dillwyn, 1817)

X90960
AJ389630

Steiner & Mller (1996)

Steiner & Hammer (2000)

Modiolus auriculatus (Krauss, 1848)

Mytilus edulis (Linn, 1758)

AJ389644
L33448

Kenchington et al. (1995)

Pinna muricata (Linn, 1758)

Atrina pectiniata (Linn, 1767)

AJ389636
X90961

Steiner & Hammer (2000)

Steiner & Mller (1996)

Elliptio complanata (Lightfoot, 1786)

AF117738

Distel (2000)

Carditamera floridana (Conrad, 1838)

AF229617

Campbell (2000)

Ensiculus cultellus (Linn, 1758)

AF229614

Campbell (2000)

Diplodonta subrotundata (Issel, 1869)

AJ389654

Steiner & Hammer (2000)

Basterotia elliptica (Rcluz, 1850)

AF229616

Campbell (2000)

Monodonta labio (Linn, 1758)

Diodora graeca (Linn, 1758)

X94271
AF120513

Winnepenninckx et al. (1998)

Giribet et al. (2000)

Zeuxis siquijorensis (A. Adams, 1852)

Bursa rana (Linn, 1758)
Crepidula adunca (Sowerby, 1825)

X94273
X94269
X94277

Winnepenninckx et al. (1998)

Winnepenninckx et al. (1998)
Winnepenninckx et al. (1998)

Nautilus macromphalus (Sowerby, 1848)

Nautilus scrobiculatus (Lightfoot, 1786)

AJ301606
AF120504

Bonnaud & Boucher-Rodoni (unpublished.)

Giribet & Wheeler (2002)

Loligo pealei (Lesueur, 1821)

Sepia elegans (Blainville, 1827)

AF120505
AF120506

Giribet & Wheeler (2002)

Giribet & Wheeler (2002)

Liolophura japonica (Lischke, 1873)

X70210

Winnepenninckx et al. (1993b)

Acanthochitona crinita (Pennant, 1777)

AF120503

Giribet et al. (2000)

Lepidopleurus cajetanus (Poli, 1791)

AF120502

Giribet et al. (2000)

Sampling locality

Nerita albicilla (Linn, 1758)

The Norwegian Academy of Science and Letters Zoologica Scripta, 32, 4, July 2003, pp343 356

347

Molecular phylogeny of Scaphopoda G. Steiner & H. Dreyer

Table 3 PCR and sequencing primers used in this study. The NS

primers were designed by White et al. 1990. All other primers were
designed for this project.
Name

Position on D. austini

Sequence

18A1
NS3
600 r
NS4 r
NS5
1400 f
1400 r
1800 r

200
580 600
669 650
1203 1184
1182 1203
1473 1495
1495 1473
18431865

5-CCT ACC TGG TTG ATC CTG CCA G-3

5-GCA AGT CTG GTG CCA GCA GCC-3
5-CCG AGA TCC AAC TAC GAG CT-3
5-CTT CCG TCA ATT CCT TTA AG-3
5-AAC TTA AAG GAA TTG ACG GAA G-3
5-GAG CAA TAA CAG GTC TGT GAT GC-3
5-GCA TCA CAG ACC TGT TAT TGC TC-3
5-ATG ATC CTT CCG CAG GTT CAC C-3

The complete 18S rRNA gene was amplied in overlapping fragments using the primer pairs 18A1/600r, NS3/
1800r, NS3/1400r and NS5/1800r (Table 3). The PCR
was performed on a Robocycler 96 (Stratagene) in a 30-L
reaction mix containing 1.5 mM MgCl2, each dNTP at
250 M, each primer at 0.5 M, 0.6 units Taq polymerase
(Biotaq Red, Bioline) and the supplied reaction buffer at
1 concentration. The PCR cycle conditions were as follows: initial denaturation step of 2 min at 94 C, 36 cycles of
30 s denaturation at 94 C, 45 s annealing at 50 C, and 2 min
primer extension at a 72 C, followed by a nal primer extension step of 10 min at 72 C. PCR products were puried
with the Concert Rapid PCR Purication System (Life Technologies) and sequenced automatically with a range of
primers (Table 3) on an ABI 3700 at VBC-Genomics Bioscience
Research GmbH, Vienna.
Choice of taxa, alignment and phylogenetic analysis
In addition to the ve published sequences we obtained 18S
rDNA sequences of 12 species of Scaphopoda resulting in 17
ingroup taxa of a sufciently wide systematic range to address
major phylogenetic relationships within the group. For the
assessment of the conchiferan relationships we selected 17
bivalve species (six each of the Protobranchia, Pteriomorpha,
and ve of the Heteroconchia), seven streptoneuran gastropods, the four available cephalopod species, and rooted the
trees with three polyplacophoran species.
Sequences were aligned with CLUSTALX 1.8 (Thompson
et al. 1997) applying several combinations of gap penalties
(opening penalty: 1020; extension penalty: 512) and subsequent manual corrections. The strategy we used was to align
the species of each class rst in the multiple alignment mode
and united these in the prole alignment mode. The alignment is available upon request from the corresponding
author (G.S.).
Phylogenetic analyses were performed with PAUP* 4.0b8a
and 4.0b10 (Swofford 1998) on a PC and on the Schrdinger
1 Linux-Cluster at the Central Informatics Service,
348

University of Vienna. Unweighted heuristic maximum

parsimony (MP) searches were made with 50 random addition
sequences and TBR branch swapping. Bootstrap support
(BS) was assessed by 1000 replicates, each with three random
sequence additions and number of trees limited to 200 per
replicate. Decay indices (DI) (Bremer 1988, 1994) were
calculated using a batch le produced by TREEROT (Sorensen
1996) with 10 random addition sequences, keeping 100 trees
per replicate for each search.
For maximum-likelihood analyses (ML), the most parsimonious trees (MPTs) were used as starting trees for the
calculation of the model parameters and subsequent branch
swapping. Empirical nucleotide frequencies and the parameters for the transition/transversion ratio, proportion of invariable sites, and the gamma shape value were estimated under
the HKY85 model with rate heterogeneity and four categories of substitution rates following a gamma distribution
(HKY85 + I + model). The resulting values were then set
for subtree-pruning-regrafting (SPR) branch swapping with
rearrangements limited to cross four branches. We tested the
signal in, and the robustness of, the ML tree with the quartetpuzzling program TREE-PUZZLE 5.0 (Schmidt et al. 2000)
under the same model as the ML analysis and parameters
estimated by the program and with 100.000 puzzling steps.
Four-cluster likelihood-mapping (Strimmer & Haeseler
1997) implemented in TREE-PUZZLE 5.0 was performed with
10 000 randomly chosen quartets to test the relationships of
the four conchiferan classes. Resulting trees were visualized
with TREEVIEW 1.6.1 (Page 1996). Competing alternative
phylogenies were obtained by searching under topological
constraints and subsequently compared with the KH
(Kishino & Hasegawa 1989) and Templeton tests for MP, and
the SH (Shimodaira & Hasegawa 1999) test for ML as implemented in PAUP* under the RELL option.
The programs PREPARE and HADTREE (Hendy & Penny
1993) were used for spectral analysis using the options for
recoding the data to two-state characters and sum-of-7 as
in Steiner (1999b) and Steiner & Hammer (2000). As the
number of species is limited to 20 in these programs we
created two data sets, one for the Scaphopoda only and one
with selected molluscan species to address the sisterg-roup
relationships of the Scaphopoda.

Results
The 18S rDNA sequences of scaphopods obtained in this
study range in length from 1808 to 1854 basepairs in the
Dentaliida and from 1915 to 1991 basepairs in the Gadilida.
The increased sequence lengths of the Gadilida are due to
inserts in helices E23_1 and E23_2 to E23_5 of the V4 region
(Table 4), according to the secondary structure model in
Wuyts et al. (2002). Sequence similarity of these inserts is
high and suggests homology. The alignment has 2500

Zoologica Scripta, 32, 4, July 2003, pp343 356 The Norwegian Academy of Science and Letters

G. Steiner & H. Dreyer Molecular phylogeny of Scaphopoda

Table 4 Comparison of 18S rDNA sequence

lengths of Scaphopoda with the gastropod
Limicolaria kambeul as reference for the
secondary structure elements. The
representatives of the scaphopod order
Gadilida show extensions in the helices
E23_1 and E23_2 to E23_5 of the V4 region.
Abbreviations: BE, beginningend; Dr,
difference to reference.

E23_1

E23_2 to E23_5

Species

Length

BE

Length

Dr

BE

Length

Dr

Reference
Limicolaria kambeul (Gastropoda)

1839

662713

51

714773

59

Dentaliida
Dentalium austini
Fissidentalium candidum
Fissidentalium capillosum
Antalis vulgaris
Antalis inaequicostata
Antalis perinvoluta
Antalis pilsbryi
Rhabdus rectius
Fustiaria rubescens

1842
1808
1812
1865
1762
1744
1804
1810
1854

669716
649695
651697
683730
635682
621668
648694
649695
681727

47
46
46
47
47
47
46
46
46

4
5
5
4
4
5
5
5
5

717785
696755
698757
731792
683744
669727
695754
696758
728793

68
59
59
61
61
58
59
62
65

9
0
0
2
2
1
0
3
6

Gadilida
Entalina tetragona
Heteroschismoides subterfissum
Pulsellum affine
Siphonodentalium lobatum
Polyschides olivi
Cadulus subfusiformis
Cadulus sp. A
Cadulus sp. B

1915
1915
1974
1926
1926
1986
1991
1991

675757
675758
682774
677763
677763
684772
684776
685754

82
83
92
86
86
88
92
69

31
32
41
35
35
37
41
18

758847
759847
775902
764857
764857
773915
777921
755921

89
88
127
93
93
142
144
166

30
29
68
34
34
83
85
107

characters, of which 948 are parsimony-informative. Parsimony

analysis returns three MPTs of 3206 steps (CI = 0.522,
RC = 0.3935) (parsimony-uninformative characters excluded).
The strict consensus tree (Fig. 3A and B) is 3220 steps long.
The single ML tree (Fig. 4) has a ln L = 20050.762 (transition/transversion ratio = 1.338, proportion of invariable sites
= 0.18, gamma shape parameter = 0.5). Likelihood-mapping
(Fig. 5A) associates 91.1% of all quartets with areas of wellresolved topologies (tips of the triangle) and 5.1% with the
area of unresolved or star topologies (centre of the triangle).
This indicates a strong phylogenetic signal in the dataset,
although some parts of the trees can be expected to show low
resolution and /or support.
Class relationships
Scaphopoda is a well-supported monophylum in all analyses,
with BS of 92, DI of 9, and quartet-puzzling support (QP) of
74 (Figs 3A, 4 and 6A). There is also high support for the
monophyly of Polyplacophora (BS = 100, QP = 83, DI = 25)
and Cephalopoda (BS = 100, QP = 87, DI = 53). Monophyletic Gastropoda are not supported by MP (BS = 29) as
the Nerita sequence renders them paraphyletic with regard
to the Cephalopoda and Scaphopoda. However, ML nds
Gastropoda monophyletic with moderate puzzling support
(QP = 63), although the clade appears as sister taxon to the
solemyid bivalves. None of the analyses supports monophyly of the Bivalvia, which appears as a set of paraphyletic
branches at the base of the conchiferan tree. In general,

The Norwegian Academy of Science and Letters Zoologica Scripta, 32, 4, July 2003, pp343 356

branch support and phylogenetic signals in the deep parts of

the tree is low. In contrast to this, the only supported sistergroup relationship of molluscan classes is that of Scaphopoda
and Cephalopoda (BS = 86, QP* = 51, DI = 10). Parsimony
places Gastropoda as the sister-group of the Scaphopoda
Cephalopoda clade but with low support (BS = 38, DI = 5).
This topology is not represented in the ML tree where Gastropoda root within the Bivalvia. However, puzzling support
(QP = 33) for this topology indicates that the signal is also
detected by ML. Spectral analysis results (Fig. 6A) corroborate the (Gastropoda (Scaphopoda, Cephalopoda)) topology.
The six top-ranked splits are those of the four cephalopod
species, the scaphopod orders Dentaliida and Gadilida, and
the Polyplacophora. The seventh split unites Cephalopoda
and Scaphopoda, whereas the scaphopod split ranks 10th.
Two splits ranking immediately before that of the Scaphopoda is the rst nonsense-split uniting the vetigastropod
Monodonta labio with the two coleolids, Loligo pealei and Sepia
elegans (split 8), and a split within the Scaphopoda (split 9).
The 49th split is that uniting the Gastropoda with Cephalopoda and Scaphopoda. There is also signal for a Gastropoda
and Cephalopoda split which ranks 60th.
The comparison of alternative competing topologies
against the MP and ML trees shows that trees with all conchiferan classes being constrained as monophyletic is not signicantly worse (Table 5). The latter tree also features a
ScaphopodaCephalopoda clade like the unconstrained trees
but with monophyletic Bivalvia. The other trees tested differ
349

Molecular phylogeny of Scaphopoda G. Steiner & H. Dreyer

(Scaphopoda + Bivalvia) and (Scaphopoda + Gastropoda)

have 19.5% and 2.3% support, respectively.
Relationships within Scaphopoda
The two ordinal taxa, Dentaliida and Gadilida, are robustly
supported by all analyses (Figs 3A and B, 4, 5B). The monophyly of the Gadilida is further corroborated by the
homologous extensions in the helices E23_1 and E23_2 to
E23_5; the topology within it is identical in MP and ML trees,
although the internal branches have only moderate to low
support. Note that the puzzling values exceed the bootstrap
values for these branches indicating the ML method being
more efcient in assessing the phylogenetic signal. The basal
dichotomy separating Entalimorpha from Gadilimorpha has
low BS and QP support (Fig. 3B) but takes fth rank of all
scaphopod splits in the spectral analyses (Fig. 5B). Monophyly of the Entalinidae and Siphonodentaliidae is fully
supported, whereas the robustness of the Gadilidae is low. The
three Cadulus sequences representing the Gadilidae are set
off together with the single pulsellid species from the Siphonodentaliidae by a better supported branch (QP = 76). Thus,
Gadilidae and Siphonodentaliidae are not sister taxa.
As in the Gadilida, the dentaliid topology is consistent
between the analyses. However, branch support is considerably higher for most clades, and bootstrap values tend to be
higher than puzzling values in this subtree. Fustiaria appears
as the rst offshoot within the Dentaliida. The monophyly of
the Dentaliidae receives no support, with Rhabdus rectius
(Rhabdidae) emerging from among the dentaliid species.
Furthermore, the genus Antalis represented by four species is
polyphyletic, with only A. inaequicostata and A. vulgaris forming a clade. Antalis pilsbryi appears closer related to the two
Fissidentalium species than to its congeners.

Discussion

Fig. 3 A, B. Strict consensus tree (L = 3220, CI = 0.5199, RC = 0.3906)

of three MPT (L = 3206, CI = 0.5221, RC = 0.3935) with support
indices. Bootstrap and puzzling values are above, and decay index
below branches. A. Subtree showing relationships of Scaphopoda
with the other molluscan taxa. B. Subtree of Scaphopoda.

in the sister-group relationship of the Scaphopoda and are

signicantly worse (P < 0.05) both than the unconstrained
trees and the monophyletic classes trees, both in terms of
tree length and likelihood. The tree with the Diasoma
Cyrtosoma topology is the least parsimonious and least likely of
those tested. The likelihood-mapping with four clusters represented by Scaphopoda, Bivalvia, Gastropoda and Cephalopoda (Fig. 5B), returns the highest support, 51.6%, to the
(Scaphopoda + Cephalopoda) topology. The topologies with
350

Class relationships
Scaphopoda and Cephalopoda are robustly monophyletic in
all analyses. Gastropoda appear as a clade only in the ML
tree, which is likely due to the long branch of the Nerita
sequence and the greater sensitivity to long branch attraction
effects of the MP method. As in previous analyses (Steiner &
Mller 1996, Giribet & Carranza 1999; Steiner 1999b;
Steiner & Hammer 2000), the Bivalvia clade is difcult to
detect, and here they are always paraphyletic at the base of
the conchiferan clade. A likely explanation (see Steiner &
Mueller 1996) posits their low average substitution rates
compared to the other conchiferans. However, the MP and
ML trees found under the constraint for all classes being
monophyletic are insignicantly longer or less likely than the
optimal trees, allowing for assessing their phylogenetic relationships. Although there are several long-branch taxa e.g.
the Vetigastropoda (Monodonta labio and Diodora graeca), the

Zoologica Scripta, 32, 4, July 2003, pp343 356 The Norwegian Academy of Science and Letters

G. Steiner & H. Dreyer Molecular phylogeny of Scaphopoda

Fig. 4 Maximum likelihood tree of ln L = 20050.7621 under the

HKY85 + I + model with transition/transversion ratio = 1.3,
proportion of invariable sites = 0.17217, gamma shape parameter =
0.4632, and four categories of substitution rates.

heterodont Bivalvia (except for Carditamera oridana), the

gadilid Scaphopoda, and all four cephalopods they do not
seem to seriously affect the results as these long branches
do not come together in the trees and do not cluster near the
root. All analyses of the present dataset strongly support the
sister-group relationship of Scaphopoda and Cephalopoda,
whereas there is no apparent signal for a Scaphopoda
Bivalvia clade. Spectral analysis and likelihood-mapping
using clusters also detect the signal for a Cephalopoda
Gastropoda clade. It is, however, much weaker in both cases.
This result is further corroborated by the comparison of the
alternative tree topologies (Table 5) showing that they are all
signicantly worse than both the best trees and the trees forcing all classes to be monophyletic. Thus, there is no support
for the Diasoma/Loboconcha concept, its respective topology being the worst of all alternative trees tested.
In the light of these results, the helcionellid concept as
proposed by Waller (1998) gains considerable support. When
plotted on the topology with monophyletic Bivalvia, the

The Norwegian Academy of Science and Letters Zoologica Scripta, 32, 4, July 2003, pp343 356

Fig. 5 A, B. Maximum likelihood mapping using TREE-PUZZLE

5.0. Areas at the corners of the triangle represent one of the three
possible fully resolved four-taxon (quartet) topologies, those along
the edges partly resolved quartets for which it is not possible to
decide between two possible topologies. The central area represents
unresolved quartets. Figures give percentages of 10 000 randomly
chosen quartets in each area. A. General likelihood mapping
showing 91.1% of all quartets being fully resolved and only 5.1%
unresolved. This indicates high phylogenetic information content of
the 18S rDNA data. B. Four-cluster likelihood mapping of the
conchiferan classes, testing their phylogenetic relationships. The
corners of the triangle are labelled with the corresponding unrooted
tree topology. The ScaphopodaCephalopoda topology receives
greatest support with 51.6% of all quartets, compared to 19.5 and
2.3% for the competing topologies. Note that the topology at the top
corner does not necessarily represent the DiasomaCyrtosoma concept
because the root can also be placed at the Bivalvia branch, resulting
in the modied Visceroconcha concept of Haszprunar (2000).

morphological similarities of Scaphopoda and Cephalopoda,

i.e. multiple cephalic tentacles and a ring-shaped dorsoventral muscle attachment (see Table 1), can be interpreted as
synapomorphies (Fig. 7). The pronounced dorsoventral axis
is already developed in the Gastropoda and therefore
plesiomorphic for this clade. Consequently, the similarities of
351

Molecular phylogeny of Scaphopoda G. Steiner & H. Dreyer

Fig. 6 A, B. Spectral analysis. Histogram of signal (positive values on ordinate) and normalized conict (negative values on ordinate) for the
top 60 splits (abscissa) in the alignment, ranked by net signal (signal minus conict). A. Analysis of 20 selected molluscan taxa assessing sistergroup relationships of Scaphopoda (Polyplacophora: Lepidopleurus cajetanus, Acanthochitona critina; Bivalvia: Solemya togata, Yoldiella nana, Arca
noae, Ensiculus cultellus, Elliptio complanata; Gastropoda: Nerita albicilla, Monodonta labio, Zeuxis siquijorensis; Cephaolopoda: Nautilus
macromphalus, N. scrobiculatus, Loligo pealei, Sepia elegans; Scaphopoda: Antalis perinvoluta, A. pilsbryi, Rhabdus rectius, Entalina tetragona,
Siphonodentalium lobatum, Cadulus subfusiformis). Solid bars represent nodes present in the strict consensus tree. The split uniting Scaphopoda
and Cephalopoda ranks seventh whereas the split uniting Cephalopoda and Gastropoda ranks 60th. B. Analysis of all scaphopod
species. Solid bars represent nodes present in the unrooted topology of the ML subtree (inset), numbers at branches indicate their rank in
the spectrum.

Scaphopoda and Bivalvia emphasized by the Diasoma/Loboconcha concept must have arisen convergently. The characters associated with the burrowing, infaunal habit of these
two groups, i.e. the enclosure of the body by the mantle/shell
and the burrowing foot innervated by fully concentrated
pedal ganglia, are certainly good candidates for convergent
evolution.
352

More difcult to explain is the derived position of the visceral connectives median to the dorsoventral muscles shared
by Cephalopoda and Gastropoda, as this is unlikely to be the
result of a similar life-style. However, the shift of nerve position is not necessarily homologous when the highly concentrated central nervous system of Cephalopoda is considered.
While the shift in Gastropoda is apparently a result of a

Zoologica Scripta, 32, 4, July 2003, pp343 356 The Norwegian Academy of Science and Letters

G. Steiner & H. Dreyer Molecular phylogeny of Scaphopoda

Table 5 Comparison of MP and ML trees with those of competing hypotheses obtained by heuristic searches with topological constraints

enforced. The unconstrained MP and ML trees and the tree with all classes were constrained as monophyletic, showing Scaphopoda and
Cephalopoda as sister-groups. For the MP criterion, tree lengths were tested with KH, for the ML criterion, with SH (see text); the probability
of the null hypothesis (P ) is listed. * indicates signicant differences (P < 0.05). Note that with reference to the Bivalvia the best trees with all
classes monophyletic are not signicantly worse. All trees showing Scaphopoda as not being the sister-group of Cephalopoda are signicantly
worse than both the unconstrained and monophyletic trees.
Constraint

Tree length

Diff.

KH-Test (P)

ln L

Diff.

SH-Test (P)

No [Scaphopoda + Cephalopoda]
Monophyletic classes
[Scaphopoda + Cephalopoda]
Scaphopoda + Bivalvia (Diasoma)
Scaphopoda + Gastropoda
Cephalopoda + Gastropoda

3206

20050.762

3213
3246
3236
3232

7
40
30
26

0.3624
0.0006*
0.0019*
0.0079*

20058.367
20078.994
20077.761
20076.278

7.605
28.228
26.999
25.516

0.4328
0.0289*
0.0452*
0.0452*

Fig. 7 Character-state transitions of characters from Table 1 plotted

on the topology supported by 18S rDNA. Solid bars indicate
nonhomoplastic, empty bars homoplastic characters. 1, lateroventral
extension of mantle-shell enclosing body; 2, burrowing foot; 3, epiatroid
nervous system with true pedal ganglia; 4, visceral connectives lateral
of dorsoventral muscles (change to median of dorsoventral muscles
indicated); 5, prominent dorsoventral body axis with resulting
U-shaped gut; 6, more than 2 cephalic tentacles; 7, ring-shaped
attachment of dorsoventral muscles. Note that the homoplastic
characters 13 are associated with infaunal, burrowing life style and,
thus, prone to convergent evolution. Scaphopoda and Cephalopoda
are linked by synapomorphic multiple cephalic tentacles and the
ring-shaped muscle attachment. Both share the prominent
dorsoventral body axis and the U-shaped gut with Gastropoda.

change in developmental timing of muscle and neuronal differentiation, there are no data on this process for Cephalopoda (Haszprunar & Wanninger 2000).
The differentiation of a distinct head is yet another problematic issue. We have not included this character in Table 1
because delimiting character states and subsequent character
coding are not as straightforward as in the other characters.
The head of Scaphopoda, consisting of a movable buccal tube

The Norwegian Academy of Science and Letters Zoologica Scripta, 32, 4, July 2003, pp343 356

and a pair of shields from which the captacula arise (Shimek

& Steiner 1997), is clearly separated from foot but not from
the visceral sac or the mantle. It does not protrude from the
shell or directly contact the substratum. Scaphopoda are
thus intermediate between the headless Bivalvia and the
Gastropoda and Cephalopoda with their well-developed heads.
They are at a similar level of head differentiation as the
Tryblidia (Recent monoplacophorans) (Haszprunar & Schaefer
1997), with the signicant difference that they have preoral
cephalic tentacles like Gastropoda and Cephalopoda. The
assumption of a ScaphopodaCephalopoda clade requires a
de-differentiation of the head region in Scaphopoda and the
complete reduction of the (cerebral) eyes which are considered
a potential synapomorphy of Gastropoda and Cephalopoda. The latter argument is, however, weakened by the
presence of cerebrally innervated eyes on the rst ctenidial
laments of several pteriomorph Bivalvia (e.g. Rosen et al.
1978). Such a de-differentiation of the head and loss of
photoreceptors can, again, be correlated with the acquisition
of an infaunal life style and the anterior elongation of the
mantle/shell. However, as the de-differentiation of the head
region can occur from any level, this character is not very
informative.
Relationships within Scaphopoda
The taxon sampling of the Scaphopoda in this study is not
sufcient to allow denitive conclusions to be drawn on all
relationships of its higher taxa. We have no molecular data
on the dentaliid families Calliodentaliidae, Gadilinidae,
Laevidentaliidae and Omniglyptidae, or on the gadilid deep-sea
family Wemersoniellidae. Moreover, some of the family taxa
are represented by a single species only. Nevertheless, it is
possible to address several important questions and demonstrate problematic points.
The monophyletic status of the orders Dentaliida and
Gadilida is fully supported, as is that of the Entalimorpha and
Gadilimorpha in the latter taxon. The diphyletic origin of the
353

Molecular phylogeny of Scaphopoda G. Steiner & H. Dreyer

Gadilidae was unexpected but is consistent with the analyses

and comparatively well supported. The morphological
character setting Siphonodentaliinae and Gadilinae apart from
all other scaphopods is the anterior constriction of the shell.
Steiner (1992, 1998) noted that not all species of Siphonodentalium show this constriction. In the light of the present
results, the possibility that this trait evolved independently in
the two groups becomes likely.
The internal branches of the dentaliid clade are generally
shorter than those of the Gadilida but show a similar level of
support. Together with the short-terminal branches in this
subtree, this indicates low substitution rates and/or a recent
series of cladogenetic events. For further phylogenetic
studies on lower systematic levels it seems appropriate to use
faster evolving markers since the genetic distances in the 18S
rDNA become too small within the Dentaliidae. Dentaliidae
itself is at least paraphyletic, with Rhabdus rectius (Rhabdidae)
being part of the quite recent radiation mentioned above.
The addition of more species of the smooth-shelled taxa like
Laevidentaliidae or Calliodentaliidae is likely to make this
even more apparent. The only morphological synapomorphy
of the Dentaliidae is the longitudinally ribbed shell, but
several species of the genus Antalis show this feature transiently
in the juvenile shell only. Moreover, Lamprell & Healy
(1998) demonstrated longitudinal sculpture also in some
Laevidentaliidae. The rather clear separation of Antalis
vulgaris and A. inaequicostata from the other dentaliids could
point to multiple development and/or reduction of shell ribbing. The present results on dentaliid molecular phylogeny
clearly demonstrate the urgent need of a revision of this
group based on additional morphological and molecular
data.
The position of Fustiaria rubescens (Fustiariidae) at the base
of the Dentaliida is in accordance with the morphological
analyses in Steiner (1998, 1999a). Fustiariidae and Gadilinidae
share a simple anatomy of the posterior mantle edge compared
to the other Dentaliida (Steiner 1991, 1998). However, conrmation of this character state being plesiomorphic depends
on future analyses including species of the Gadilinidae.

Acknowledgements
We are greatly indebted to the institutions involved in the
BIOICE program, the University of Iceland, the Icelandic
Marine Research Institute, and the Icelandic Institute of
Natural History, and Jon-Arne Sneli (Trondheim Biological
Station, Norway) and Torleiv Brattegard (University of Bergen,
Norway) for the opportunity to join the summer 2000 cruise
where most of the species for this study were collected. We
also wish to thank John Taylor and Emily Glover (Natural
History Museum London), and Kurt Schaefer and Christiane
Todt (University of Vienna) for providing us with specimens.
We are grateful for the discussions with Luitfried Salvini-Plawen
354

(University of Vienna) and his comments on the manuscript.

The study was partly funded by the Austrian Science Foundation (FWF), projects P11846-GEN and P14356-BIO.

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