Zoologica Scripta
Speciation and dietary specialization in Drupa, a genus of
predatory marine snails (Gastropoda: Muricidae)
MARTINE CLAREMONT, DAVID G. REID & SUZANNE T. WILLIAMS
Submitted: 8 November 2011
Accepted: 11 December 2011
doi:10.1111/j.1463-6409.2011.00512.x
Introduction
A fundamental question in evolutionary biology concerns
the generation of diversity in lineages with wide dispersal
and potentially high gene flow among populations. Under
an allopatric model of speciation, gene flow is the main
process opposing population differentiation; theory pre-
dicts that sister species are at first allopatric, but that the
likelihood of range overlap should increase with age since
divergence (often estimated by genetic distance; Mayr
1954; reviewed by Coyne & Orr 2004). In a marine sys-
tem, geographical barriers to dispersal (and gene flow) are
not immediately obvious, and it might be expected that
speciation in the sea should therefore be rare and slow
(Palumbi 1992). This is clearly not the case: many marine
groups are highly diverse in areas smaller than would be
ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters, 41, 2, March 2012, pp 137–149
Claremont, M., Reid, D.G. & Williams, S.T. (2012). Speciation and dietary specialization
in Drupa, a genus of predatory marine snails (Gastropoda: Muricidae). —Zoologica Scripta,
41, 137–149.
We test the competing predictions of allopatric speciation and of ecological speciation by
dietary specialization in Drupa, an Indo-Pacific genus of carnivorous marine gastropods in
the family Muricidae. We use a well-resolved molecular phylogeny (reconstructed from
one nuclear and two mitochondrial genes) to show the validity of the traditional species
D. elegans, D. rubusidaeus, D. clathrata, D. morum and D. speciosa. ‘Drupa ricinus’ is shown to
consist of three species: D. ricinus s. s., D. albolabris and a new species, possibly endemic to
Japan. ‘Purpura’ aperta is transferred to Drupa. Despite potential widespread dispersal and
a high degree of range overlap among sister species, range sizes between sister species are
highly asymmetric, suggesting that speciation has been predominately peripatric. The
exception is the sister pair D. ricinus s. s. and D. albolabris, which have symmetric range sizes
and are sympatric over broad Indo-Pacific ranges. Such symmetry and extensive sympatry
are contrary to the predictions of the (peripatric) allopatric model of speciation. Neverthe-
less, contrary to the predictions of an ecological speciation model based upon dietary spe-
cialization, broad dietary range appears to be identical between the species. Small
differences in microhabitat preferences (or hypothetical dietary specialization at a fine taxo-
nomic scale) may have been significant in the speciation process or, if initial divergence
was allopatric, in permitting subsequent sympatry. Broad dietary shifts appear to have
accompanied more ancient divergences within the genus Drupa.
Corresponding author: Martine Claremont, Department of Zoology, Natural History Museum,
Cromwell Rd., London, SW7 5BD, UK & Division of Biology, Imperial College London, Silwood
Park Campus, Ascot SL5 7PY, UK. E-mail: m.claremont@nhm.ac.uk
David G. Reid & Suzanne T. Williams, Department of Zoology, Natural History Museum,
Cromwell Rd., London SW7 5BD, UK. E-mails: d.reid@nhm.ac.uk, s.williams@nhm.ac.uk
predicted based on potential dispersal ability (Williams &
Reid 2004; Lee & Ó Foighil 2005; Rocha et al. 2005; Ayre
et al. 2009; Claremont et al. 2011b). This apparent contra-
diction has led to the recognition of many factors limiting
dispersal including historical and current physical barriers,
larval behaviour and the availability of suitable settlement
habitat (Cowen & Sponaugle 2009). As a result, a primar-
ily allopatric mode of speciation among marine organisms
is widely accepted (see e.g. Williams & Reid 2004; Reid
2007; Frey 2010; Claremont et al. 2011b).
Nonetheless, there are indications that speciation in the
face of gene flow (‘sympatric speciation’) may be common
in the sea. In several marine gastropod radiations, some
young sister species are broadly sympatric at a geographical
scale, contrary to the predictions of allopatric speciation
137
Speciation and dietary specialization in Drupa d M. Claremont et al.
(reviewed by Krug 2011). There is increasing evidence
that, in these cases, ecological specialization may play a
role in the speciation process, promoting differentiation in
the face of gene flow. The theory of ecological speciation
suggests that reproductive isolation evolves via disruptive
selection acting on populations that occupy contrasting
environments or use different resources (reviewed by
Schluter 2001; Coyne & Orr 2004). This may result in
sister species that are sympatric but differ in ecological
characters; examples have been identified in fish (Rocha
2003; Rocha et al. 2005, 2008) and molluscs (Williams &
Reid 2004; Meyer et al. 2005; Reid et al. 2006; Frey 2010).
Although ecological factors limit distributions in some
marine organisms, their role in speciation is uncertain,
because ecological divergence may follow (rather than pre-
cede) speciation, perhaps as a result of adaptation or com-
petition (reviewed by Coyne & Orr 2004; see also
Claremont et al. 2011b).
Some of the best evidence for an ecological role in spe-
ciation has been found in groups with specialized diets. In
terrestrial systems, host preference and local adaptation
have long been a focus of speciation research (reviewed by
Coyne & Orr 2004). Although fewer such studies have
been performed on marine organisms, examples of local
adaptation and possible ecological speciation are found
among crustaceans, polychaetes and molluscs, despite
potential gene flow between sisters in some of these
groups (reviewed by Sotka 2005). However, few studies
have tested the predictions of ecological speciation in a
phylogenetic context. Two exceptions are found in work
performed on the parasitic gastropod genera Leptoconchus
(Gittenberger 2006; Gittenberger & Gittenberger 2011)
and Phestilla (Faucci et al. 2007). Both genera have free-
swimming larvae and include examples of sister species
that feed upon different hosts (Faucci et al. 2007;
Gittenberger & Gittenberger 2011), consistent with eco-
logical speciation mediated by diet, even in the face of
gene flow (see also Sotka 2005).
Species in the gastropod genus Conus are also widely
dispersed and specialized predators, but are not parasitic.
Phylogenetic analyses in the group show that sister species
are often geographically sympatric, while still sharing the
same broad prey type (e.g. worms, fish or molluscs; Duda
et al. 2001; Duda & Palumbi 2004; Duda & Kohn 2005;
reviewed by Krug 2011). This appears to contradict the
predictions of both the allopatric and the ecological speci-
ation models. However, because it is known that Conus
can exhibit specialization within broad prey groups (Kohn
1968, 1980; Kohn & Nybakken 1975), it could be argued
that prey choice may yet prove to be significant in an eco-
logical speciation process. Indeed, Duda et al. (2001) men-
tioned one case of contrasting diets in a sister–species pair
138 ª 2012 The Authors
of molluscivorous Conus. Alternatively, some sympatric sis-
ter species of Conus may be differentiated by microhabitat
(Vallejo 2005), suggesting that ecological speciation may
be promoted by differentiation along ecological gradients
unrelated to diet.
To test the competing predictions of allopatric specia-
tion and of ecological speciation mediated by diet, we use
another group of carnivorous marine gastropods, the
genus Drupa in the family Muricidae. Although most mu-
ricids feed by drilling holes in slow-moving or sessile prey,
including other molluscs and barnacles (Taylor 1976,
Taylor 1978; Vermeij & Carlson 2000), species of Drupa
are not known to drill (Taylor 1976). Instead, some species
of Drupa feed upon more active prey such as errant poly-
chaetes and fish by trapping them in holes and using an
extensible proboscis (Taylor 1976, 1982). The range of
diet across the genus is known in some detail (Taylor
1976, 1978, 1983, 1984). The 12 morphospecies (and sub-
species) were recently revised by Monsecour & Wuyts
(2007); distributions and anatomical characters were
described by Emerson & Cernohorsky (1973). Drupa spe-
cies can be presumed to have the potential for wide dis-
persal, because some are known to have large (and
probably long-lived) planktotrophic larvae (Taylor 1975)
and both Drupa morum and Drupa ricinus s. l. have dispersed
across the 5000 km of the Eastern Pacific Barrier to colonize
remote islands of the Eastern Pacific (Emerson & Cerno-
horsky 1973; Monsecour & Wuyts 2007). We aim to
(1) produce a well-resolved molecular phylogeny to delin-
eate species and reconstruct their relationships in Drupa;
(2) estimate ages of species divergences; and (3) map diet
and range onto the phylogeny to compare dietary special-
ization and range overlap between sister species. The allo-
patric speciation model predicts that sister species will be
allopatric; it makes no prediction about ecology. Alterna-
tively, if the prevailing mode of speciation is ecological
and mediated by diet, it is predicted that sister species will
not share the same dietary niche, regardless of range overlap.
Materials and methods
Specimen identification and outgroup selection
The type species of Drupa, D. morum, is a member of the
Rapaninae, a subfamily of the Muricidae (Kool 1993;
Vermeij & Carlson 2000; Claremont et al. 2008; Houart
2008; Barco et al. 2010). The most recent revision of the
genus (Monsecour & Wuyts 2007) recognized 12 species
and subspecies in three subgenera: Drupina, Ricinella and
Drupa s. s. (Table 1); note that the familiar subspecies
D. ricinus hadari Emerson & Cernohorsky 1973 is a junior
synonym of D. ricinus lischkei Hidalgo, 1904 (Monsecour
& Wuyts 2007). The subspecies of D. morum and Drupa
clathrata are geographical variants distinguished by small
d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters, 41, 2, March 2012, pp 137–149
 M. Claremont et al. d Speciation and dietary specialization in Drupa

Table 1 Classification of Drupa according to Monsecour & Wuyts domains D1–D6), 700 bp of COI (completely contained
(2007) compared with the revision proposed herein. Type species within the standard bar-coding region) and 650 bp of 12S
of each (sub)genus shown in bold. Drupa aperta was previously (corresponding to domains II and III). Primers and PCR
usually placed in Purpura (e.g. Kay 1979)
conditions for all genes were those used by Barco et al.
(2010), except for some COI sequences that were obtained
Classification of Monsecour & Wuyts (2007) Classification proposed herein
using primers COIF and COI-MUR (Claremont et al.
Drupa (Drupa) Röding, 1798 Drupa 2011a). PCR products were sequenced using a BigDye Ter-
morum morum Röding, 1798 morum
minator v1.1 Cycle Sequencing Kit (Applied Biosystems,
morum iodostoma (Lesson, 1840) albolabris (Blainville, 1832)
denticulata Houart & Vilvens, 1997 aperta (Blainville, 1832) Carlsbad, CA, USA) and run on an Applied Biosystems
elegans (Broderip & Sowerby, 1829) clathrata 3730 DNA Analyzer automated capillary sequencer.
ricinus ricinus (Linnaeus, 1758) denticulata Sequences were assembled and edited with SEQUENCHER
ricinus lischkei Hidalgo, 1904 elegans (v4.8; GeneCodes Corporation, Ann Arbor, MI, USA).
Drupa (Ricinella) Schumacher, 1817 ricinus s. s.
Clear heterozygous peaks in both the forward and reverse
rubusidaeus Röding, 1798 rubusidaeus
clathrata clathrata (Lamarck, 1816) speciosa sequence of 28S were coded as polymorphisms.
clathrata miticula (Lamarck, 1822) n. sp. Sequences for ribosomal genes (28S rRNA and 12S
speciosa (Dunker, 1867) rRNA) were aligned using the G-INS-i method of MA-
Drupa (Drupina) Dall, 1923 Drupina FFT (Multiple Alignment using Fast Fourier Transform,
grossularia Röding, 1798 grossularia
v6.847b; Katoh & Toh 2008) as sequences were not
lobata (Blainville, 1832) lobata
expected to be highly divergent. Long gaps in the align-
ment were also not expected, so the offset value was set to
0.1. The resulting alignments were adjusted by eye in
differences in shell shape and colour; their status is not MACCLADE (v4.06 OSX; Maddison & Maddison 2003).
evaluated here. GBLOCKS (v0.91beta; Castresana 2000) was then used to
Of the nine species recognized by Monsecour & Wuyts remove poorly aligned sites (minimum number of
(2007) in Drupa s. l., 46 samples from seven species were sequences for a conserved position: 70%; minimum num-
obtained (see Table S1). Identifications were from the ber of sequences for a flanking position: 90%; maximum
descriptions of Monsecour & Wuyts (2007) and Emerson number of contiguous non-conserved positions: 3; mini-
& Cernohorsky (1973). Preliminary molecular analyses of mum length of a block: 5; all gap positions allowed). COI
the Rapaninae (M. Claremont et al. unpublished data) sequences were aligned by eye in MACCLADE (v4.06 OSX;
indicated that an additional species, ‘Purpura’ aperta, Maddison & Maddison 2003). For each gene partition, 24
should be assigned to Drupa and three samples were there- different models of nucleotide substitution were tested
fore also included; identification was based on Kay (1979). with MRMODELTEST (v2.2; Nylander 2004).
As outgroups, we used seven species confirmed with A three-gene concatenated alignment was constructed,
molecular analysis to be members of the Rapaninae consisting only of specimens for which all three genes were
(Claremont et al. 2008; Barco et al. 2010), as well as Cymia available. Before combining gene partitions, we compared
tectum of the Rapaninae sensu Vermeij & Carlson (2000; posterior probabilities (PP) of all clades among individual
Table S1). gene Bayesian trees. Conflict among strongly supported
A total of 66 specimens and 181 sequences were used in clades (PP > 95%) is evidence of genetic incongruence that
this study (Table S1). Sequences for some or all genes of suggests divergent phylogenetic histories of loci, while con-
8 species (24 sequences) have previously been published flict among weakly supported clades (PP < 95%) may be
(Table S1; Claremont et al. 2008; Barco et al. 2010). due to stochastic error (Wiens 1998; Erixon et al. 2003;
Reeder 2003; Williams & Reid 2004; Williams & Ozawa
DNA sequencing and alignment 2006). Lack of resolution does not indicate conflict.
For all samples, regions of two mitochondrial genes (cyto-
chrome c oxidase subunit I (COI), 12S rRNA) and one Molecular species delimitation
nuclear gene (28S rRNA) known to be informative for phy- All alignments were analysed using Bayesian inference and
logenetic analysis in the Muricidae (Claremont et al. 2008; the Markov chain Monte Carlo (MCMC) method
Barco et al. 2010) were sequenced, following the protocols (MRBAYES v3.1, Huelsenbeck & Ronquist 2001). Model
of Claremont et al. (2011a). DNA was extracted with the parameters for each gene were set according to the model
Qiagen QIAamp DNA mini kit (Qiagen Ltd., Crawley, selected by MRMODELTEST and were free to vary among
West Sussex, UK). Polymerase chain reactions (PCR) gene partitions. The MCMC analysis ran twice for each
amplified approximately 1500 bp of 28S (corresponding to alignment: five million generations for each individual

ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters, 41, 2, March 2012, pp 137–149 139
Speciation and dietary specialization in Drupa d M. Claremont et al.
gene and 50 million generations for the combined align-
ment. Analyses were sampled every 5000 and 50 000 gen-
erations, respectively, to generate 10 000 trees each.
Convergence between runs was tested by examining the
average deviations of split frequencies and the potential
scale reduction factor (PSRF). A 10% burn-in for all anal-
yses was used, based on the traces in TRACER (v1.5;
Drummond & Rambaut 2007). Branches in consensus
trees with PP < 50% were collapsed.
We used BEAST (v1.6.1, Drummond & Rambaut
2007) to generate an ultrametric tree for use in species
delimitation tests. Site models were again set based on
the models chosen by MRMODELTEST. In this analysis,
we were only interested in relative clade ages, so we used
a relaxed clock model (uncorrelated log normal;
Drummond et al. 2006) without calibration for time. The
starting tree was random and the coalescent tree prior
was set to a constant population size. Priors were
adjusted based on preliminary analyses in order to
improve effective sample size (ESS) values. Three analyses
of 25 million generations were sampled every 2500 gener-
ations to generate 10 000 trees each. Length of burn-in
(10%) was determined by examination of traces in TRA-
CER (v1.5; Drummond & Rambaut 2007). Tree files were
combined with LOGCOMBINER (v1.6.1, part of the BEAST
package; Drummond & Rambaut 2007). The final tree
was calculated with maximum clade credibility and med-
ian node heights using TREEANNOTATOR (v1.6.1, part of
the BEAST package; Drummond & Rambaut 2007).
In order to find significant clusters within the BEAST
tree, we applied the GMYC function from the SPLITS pack-
age (Ezard et al. 2009) in R (R Development Core Team
2009). This function optimizes the likelihood of genetic
clusters, where branching rates between species follow a
Yule model, but branching rates within species follow a
neutral coalescent model (Pons et al. 2006; Fontaneto
et al. 2007). This method has been shown to help identify
phylogenetic species and cryptic taxa in other muricids
(Claremont et al. 2011a,b). We also estimated the uncor-
rected pairwise distance over all pairs of COI sequences
among and within clusters using MEGA5 (Tamura et al.
2011). Where possible, we re-examined the shell morphol-
ogy of all specimens in each cluster.
Time of diversification of Drupa
Fossil evidence suggests that the subfamily to which Drupa
belongs (Rapaninae) dates from the Late Cretaceous
(Vermeij 1996); the earliest fossil rapanine is Cymia berryi
from the Mancora Formation (late Eocene) of Peru
(Vermeij & Carlson 2000). A member of this genus,
C. tectum, was included in the analysis, so a fossil prior
with a maximum of 99.6 Ma (the beginning of the Late
140 ª 2012 The Authors
Cretaceous) and a minimum of 33.9 Ma (the end of the
Eocene) was used for the divergence of C. tectum.
We estimated the timing of diversification with BEAST
(v1.6.1; Drummond & Rambaut 2007). Site models were
initially set based on MRMODELTEST, but reduced in com-
plexity based on preliminary results observed in TRACER
(v1.5; Drummond & Rambaut 2007). We used a relaxed,
uncorrelated lognormal molecular clock, estimating all
rates, and the Yule process for the species-tree prior. The
Yule model estimates species-level branching rates, so single
exemplars were used for each species of Drupa (as defined
by the GMYC analysis) for which sequences of all three
genes were available. All outgroup sequences were removed
except for C. tectum, which was used to calibrate the analy-
sis. A single analysis (100 million generations) was sampled
every 10 000 generations to generate 10 001 trees. A 10%
burnin was used, as determined by examination of traces in
TRACER (v1.5; Drummond & Rambaut 2007).
Mode of speciation
In order to test hypotheses about mode of speciation, the
phylogenetic position of Drupa denticulata, the only species
of Drupa s. s. missing from this analysis (Table 1), was
plotted onto a cladogram of all analysed species, based on
predictions from morphological examination, the original
description (Houart & Vilvens 1997) and the revision of
Monsecour & Wuyts (2007).
Range overlap and range-size symmetry in the four sis-
ter pairs were calculated based on the distribution maps of
Emerson & Cernohorsky (1973). Because white and yellow
colour forms were distinguished on these maps, ranges of
D. ricinus s. s. and Drupa albolabris could be differentiated.
The range size of Drupa aperta was extrapolated from Kay
(1979) and D. denticulata from Houart & Vilvens (1997),
following the methods of Barraclough & Vogler (2000).
Specifically, range overlap (degree of sympatry) is defined
as the percentage of the more restricted clade’s range that
is overlapped by its more widespread sister, while range-
size symmetry is defined as the range size of the clade with
the smaller range divided by the sum of the range sizes of
each clade (Barraclough & Vogler 2000).
Dietary information was based primarily on gut contents
analyses by Taylor (1976, 1978, 1982, 1983, 1984). For
D. aperta, gut contents analysis was not available, but this
species has been observed to feed upon other gastropods
and barnacles (Kay & Magruder 1977; Bird 2011; C. Bird,
personal communication).
Results
Sequence results
The three-gene alignment consisted of 55 sequences, while
the 28S alignment had 57 sequences, the 12S alignment
d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters, 41, 2, March 2012, pp 137–149

had 66 sequences and the COI alignment had 58
sequences (see Table S1 for GenBank accession numbers).
After the removal of primer sequences and regions of
ambiguous alignment, the 28S alignment (originally
1486 bp) was reduced to 1454 bp (3%), while the 12S
alignment (initially 569 bp) was reduced to 486 bp (15%).
COI alignments were 703 bp long; sequences obtained
with COIF and COI-MUR (Claremont et al. 2011a) were
703 bp and those sequences obtained using universal prim-
ers (Folmer et al. 1994) were 658 bp. In the alignment,
43 bp of 28S, 152 bp of 12S and 269 bp of COI were
informative; remaining bases were either constant or phy-
logenetically uninformative. The model chosen by MRMO-
DELTEST was GTR+I+G for 28S and 12S, and HKY+I+G
for COI. Inspection of individual gene trees did not reveal
any well-supported clades (PP > 95%) in conflict. Resolu-
tion in the three-gene analysis was greater than in the
individual gene analyses, so we will primarily discuss the
three-gene analysis (Fig. 1). However, for several speci-
mens, sequence information was only available for 12S, so
this analysis will also be discussed (Fig. S1; individual gene
trees for 28S and COI analyses are given in Fig. S2).
Phylogeny and species delimitation
PSRF values for all MRBAYES analyses were 1.00 and aver-
age deviations of split frequencies were < 0.008 for all
analyses, indicating that all runs had reached stationarity.
All ESS values for the three-gene BEAST run were >200.
Specimens of Drupina grossularia were excluded from
the clade containing the type species D. morum and the
remaining sampled Drupa species (Figs 1A and S1); this
clade is designated Drupa s. s.
Nine significant entities were recovered within Drupa s. s.
by the GMYC analysis (Fig. 1; ML clusters = 7; ML enti-
ties = 9; likelihood of null model = 249.435; likelihood of
GMYC model = 263.437; P < 0.0001). Four entities corre-
sponded to species of Drupa recognized by Monsecour &
Wuyts (2007): D. morum, Drupa rubusidaeus, D. clathrata
and Drupa speciosa, and an additional entity corresponded
to D. aperta (formerly Purpura aperta; Figs 1A and S1;
PP = 96%). Four entities were composed of individuals
identified morphologically as D. ricinus (sensu Monsecour
& Wuyts 2007; hereafter D. ricinus s. l.; see Discussion
for identifications of these entities). An additional species
of Drupa recognized by Monsecour & Wuyts (2007),
Drupa elegans, was present only in the 12S analysis
(Fig. S1).
Average uncorrected pairwise distances among all
GYMC entities within Drupa ranged from 12.5 to 31.8%,
except for the distance between the entity identified as
D. ricinus lischkei and its sister entity, D. ricinus s. s., which
was 3.5%. Average uncorrected pairwise distance within
ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters, 41, 2, March 2012, pp 137–149
M. Claremont et al. d Speciation and dietary specialization in Drupa
GYMC clusters was <1.5%. In addition, there were several
fixed differences in the nuclear gene among most clades
(Table S2). The only exception was the nuclear sequence
of the entity D. ricinus lischkei, which was identical to that
of D. ricinus s. s. (Table S2).
Age of Drupa
Based on preliminary results, site models were reduced in
complexity to HKY for 12S and COI, and HKY+I+G for
28S for the age estimation analysis. All ESS values for the
BEAST analyses were >500. The median age estimated for
the diversification of Drupa was 25.5 Ma (13.6–38.2;
Fig. 2). Relationships among species of Drupa were well
resolved and the three pairs of sister species diverged at
approximately the same time, in the Late Miocene (5.5–
6.2 Ma; Fig. 2; PP = 100% for all sister relationships).
Patterns of endemism and dietary specialization
Based on morphological similarity, the only species of
Drupa s. s. missing from the molecular analysis, D. denticu-
lata, was placed as sister to D. morum (Fig. 3). In three of
the four sister–species relationships in Drupa, a species
with a wide range was sister to a narrowly restricted ende-
mic (Fig. 3). Of these, only one sister pair (D. clathrata–
D. aperta) is allopatric (Emerson & Cernohorsky 1973;
Kay 1979).
Range overlap among sister–species pairs was calculated
to be 100% for D. morum–D. denticulata, 96% for D. ricinus
s. s.–D. albolabris, 67% for D. rubusidaeus–D. speciosa, and
0% for D. clathrata–D. aperta (Table 2). The degree of
range-size symmetry for the sister pairs D. morum–
D. denticulata, D. rubusidaeus–D. speciosa and D. clathrata–
D. aperta was <0.05 (highly asymmetric) in all cases, while
the degree of range-size symmetry for D. ricinus s. s.–
D. albolabris was 0.49 (highly symmetric; Table 2).
In the two sister pairs where diet is known from gut
contents analysis and observation (D. clathrata–D. aperta,
D. ricinus s. s.–D. albolabris; Kay & Magruder 1977; Taylor
1982, 1983; Bird 2011; C. Bird, personal communication),
prey items were similar between the sisters (Fig. 3). In the
other two sister pairs (D. rubusidaeus–D. speciosa, D. morum–
D. denticulata), diet is only known for the more wide-rang-
ing sister (i.e. D. rubusidaeus, D. morum; Taylor 1976,
1978, 1982, 1983, 1984; Fig. 3). We reconstruct missing
dietary information for the restricted endemics based on
the assumption that diet is a conserved character (Fig. 3).
Clearly, this assumption needs to be tested in future work.
Discussion
Phylogeny and species delimitation
The genus Drupa, as defined by Monsecour & Wuyts
(2007), is polyphyletic, because its subgenus Drupina did
141
Speciation and dietary specialization in Drupa d M. Claremont et al.

Cymia tectum
NewCaledonia
Vanuatu-65 Drupina
100
Vanuatu-58 grossularia
Guam-52
Japan-88
Thalessa aculeata
100 Menathais intermedia
Thais nodosa
100 68 Concholepas concholepas
100 Dicathais orbita
99 Rapana bezoar
Guam-63
100 Tahiti-11 Drupa clathrata
100 Hawaii-61
96 Drupa aperta
96 Hawaii-79
Hawaii-60
Tuamotu-37 Drupa speciosa
Guam-61
100 Hawaii-72
Hawaii-71
Hawaii-70 Drupa rubusidaeus
100
94
Japan-84
100 Japan-10
Vanuatu-66
Guam-74.2
100 Vanuatu-51
Hawaii-69
Guam-74.1 Drupa morum
Philippines
Mozambique-41
100 Hawaii-75
Japan-65.1
100 Japan-64.3 Drupa n. sp.
Japan-65.2
Japan-64.4
Egypt Drupa ricinus lischkei
Guam-28.1
100 Japan-78
100
Taiwan Drupa ricinus s.s.
Vanuatu-69
Mozambique-42.2
Tuamotu-48
Tuamotu-62
87
Mozambique-42.1
Guam-28.2
Guam-29.2
Tahiti-15
Hawaii-81.3
100 Hawaii-81.1 Drupa albolabris
Japan-63.1
Guam-29.1
Hawaii-81.4
Hawaii-81.2
A 28S rRNA +12S rRNA + COI Japan-17 B 28S rRNA +12S rRNA + COI
0.1 substitutions/site

Fig. 1 Phylogeny of Drupa and rapanine outgroups based on concatenated analysis of 28S, 12S and cytochrome c oxidase subunit I (COI).
—A. MRBAYES analysis support values are posterior probabilities. Intraspecific support values are not shown for the sake of clarity. Codes
indicate general localities; detailed information can be found in Table S1. —B. Simplified ultrametric tree generated by a BEAST
molecular phylogeny of Drupa based on concatenated analysis of 28S, 12S and COI, indicating the entities supported by GMYC analysis;
topology is identical to that of the MRBAYES analysis.

not form a clade with other Drupa including the type spe-
cies D. morum (Figs 1A and S1). We therefore recognize
Drupina as a full genus. Although a few previous authors
have also used it in this way (e.g. Vermeij & Carlson
2000), this is the first formal demonstration that Drupa and
Drupina do not form a clade. The two remaining subgener-
a of Monsecour & Wuyts (2007), Drupa and Ricinella, are
not monophyletic either (Figs 1A and S1; Table 1), but we
refrain from subgeneric division of Drupa.
The GMYC analysis recognizes nine entities within
Drupa (seven clusters and two single terminals; Fig. 1).
Four of these entities correspond to the morphological
species D. morum, D. clathrata, D. rubusidaeus and D. speci-
osa (Figs 1 and S1). Drupa aperta was not recognized as a
member of this genus by Monsecour & Wuyts (2007),
but this assignment has previously been suggested on
morphological grounds (Iredale 1937; Vermeij 2001a).
Recognition of these GMYC clades as species is further

142 ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters, 41, 2, March 2012, pp 137–149
 M. Claremont et al. d Speciation and dietary specialization in Drupa

Cymia tectum

D. clathrata
D. clathrata (IWP)
6.3
32.6 100
D. aperta

D. aperta
D. speciosa (Hawaii)
25.5 6.4
100 100
11.5 D. rubusidaeus
100
D. rubusidaeus
D. morum
(IWP)
18.8
100
Drupa n. sp.
8.3 ?? ? D. speciosa
100 D. ricinus s.s. (Tuamotu/Pitcairn)
5.5
100
D. albolabris

Oligocene Miocene Pliocene/ D. morum

Pleistocene (IP)
33.9 23.8 5.3
35 30 25 20 15 10 5 0

Fig. 2 BEAST phylogeny of Drupa with outgroup Cymia tectum,

? D. denticulata
based on combined analysis of 28S, 12S and cytochrome c oxidase (Mascarene Is)
subunit I (COI). Values above the branch are node ages; values
below are BEAST posterior probabilities. Grey bars indicate 95% ? ?
highest posterior density intervals on nodes with more than 50% ? ? D. elegans
? (French Polynesia)
support.

? ?
supported by the pattern of variation in COI: nucleotide ? ? Drupa n. sp.
? ? (Japan)
diversity is higher between clades (minimum 12.5%) than
within them (maximum 1.5%), and the evolutionary dis-
Key to prey items
tances among and within clades are similar to those found molluscs D. albolabris
barnacles ? (IP)
in other species, both in the Rapaninae and other gastro- polychaetes
sponges
pod groups (e.g. Reid 2007, 2009; Claremont et al. sipunculans
other small crustaceans
2011a,b). fish D. ricinus s.s.
(IP)
Although complete sequence data were not available for
a sixth species, D. elegans, it forms a discrete lineage in the Fig. 3 Tree summarizing relationships among species of Drupa
12S analysis (Fig. S1) and is morphologically distinct based on MRBAYES and BEAST analyses. The placement of the
(Monsecour & Wuyts 2007). For these reasons, we con- single species missing from the molecular analysis, Drupa
sider it a valid species. All of the remaining four entities denticulata, was based on its morphological similarity to Drupa
recognized by the GMYC analysis were initially identified morum (Houart & Vilvens 1997; Monsecour & Wuyts 2007). Prey
as a single species, D. ricinus (following Monsecour & items indicated by gut contents analysis or observation (e.g. Kay
& Magruder 1977; Taylor 1982, 1983; Thomas & Kohn 1990;
Wuyts 2007). Three of these entities can now be identified
Bird 2011) are shown in solid boxes. Predicted prey items
as species: D. ricinus s. s., D. albolabris and a new species, indicated with a question mark. Range is shown under species
here referred to as Drupa n. sp. A discussion of the fourth name; IWP: from East Africa to Hawaii and Pitcairn; IP: IWP
entity can be found below. plus Eastern Pacific. Thicker branches indicating the widespread
Sequence divergence among D. ricinus s. s., D. albolabris species (see also Table 2). Branch lengths have no meaning.
and Drupa n. sp. was >16.8% (maximum 1.5% within
clades), and there were several fixed differences in the Table 2 Range overlap and degree of range symmetry among
nuclear gene among these clades (Table S2), supporting sister–species pairs in Drupa
their recognition as species. All three clades are repre-
sented in material from the Amami Islands of southern Degree of range
Sister–species pair Range overlap (%) symmetry (scale of 0.0–0.5)
Japan, suggesting that these are biological species that are
reproductively isolated in sympatry. In addition, morpho- D. ricinus s. s.–D. albolabris 96 0.49
logical re-examination revealed a number of differences in D. morum–D. denticulata 100 0.05
D. rubusidaeus–D. speciosa 67 0.05
shell characters between the sister species D. ricinus s. s.
D. clathrata–D. aperta 0 0.05
and D. albolabris, the most striking of which was a

ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters, 41, 2, March 2012, pp 137–149 143
Speciation and dietary specialization in Drupa d M. Claremont et al.
difference in colouration of the aperture: marked with yel-
low in one clade, but entirely white in the other (Fig. 3).
This colour variation has been the subject of long contro-
versy. Both forms have been named as species: Ricinula
arachnoides Lamarck, 1816 (yellow form; see Dodge 1957)
and Purpura albolabris Blainville, 1832 (white form;
Blainville 1832). Some authors have treated the two forms
as separate species (usually naming the white form D. rici-
nus and the yellow form D. arachnoides, e.g. Bernstein
1974; Thomas & Kohn 1990). However, the two forms
are often found in mixed populations (Hertlein & Allison
1960; Cernohorsky 1969; Emerson & Cernohorsky 1973;
M. Claremont & D.G. Reid, personal observation) and no
differences in anatomical or radular characters (Emerson
& Cernohorsky 1973) or in diet (Taylor 1983) have been
observed between the two forms. Thus, the forms have
usually been regarded as conspecific (Emerson &
Cernohorsky 1973; Taylor 1983; Monsecour & Wuyts
2007). Despite these similarities, the molecular results
show unequivocally that these forms should be recognized
as separate species.
However, it is difficult to determine to which colour
form the name Murex ricinus Linnaeus, 1758 applies,
because apertural colour was not specified in the original
description. We have examined the publications referred
to by Linnaeus in both the 10th and 12th editions of the
Systema Naturae (Linnaeus 1758, 1767), and while the
cited figures are not definitive, yellow colouration is men-
tioned in several places. Linnaeus’ concept of ricinus may
well have included both forms, apparently as well as speci-
mens of what is now D. morum (see Dodge 1957). A speci-
men of the yellow form is in the collection of the Linnean
Society, London, marked with the number ‘540’, the num-
ber of M. ricinus in the 12th edition of the Systema Naturae
(Dodge 1957; Emerson & Cernohorsky 1973). To stabilize
the concept of the species, we designate this specimen as
the lectotype of M. ricinus Linnaeus, 1758. This specimen
was figured by Emerson & Cernohorsky (1973), who also
restricted the type locality to ‘Ceylon’ (Sri Lanka).
The type locality of D. albolabris is Trinquemalay (i.e.
Trincomalee, Sri Lanka; Blainville 1832). Although we
have no samples of the white form from the Indian Ocean
(Fig. 1; Table S1), this form appears to be widespread
throughout the Indo-West Pacific (Emerson & Cernohor-
sky 1973). We suggest, therefore, that the appropriate
name for the white form is D. albolabris, but this requires
confirmation with additional sampling.
Only five specimens of D. n. sp. were available for anal-
ysis. Based on this limited sampling, this species has a
white aperture and appears to be restricted to Japan. It is
possible that the radula of this species was figured by
Fujioka (1985) as ‘D. ricinus hadari Emerson & Cernohorsky,
144 ª 2012 The Authors
1973’. This name is a junior synonym of D. ricinus lischkei
(fide Monsecour & Wuyts 2007) and both were introduced
for the supposed subspecies endemic to the Red Sea, so
are not available for the Japanese species. Available mate-
rial is insufficient for morphological diagnosis or detailed
comparison with D. albolabris, so although no name is
available, we do not describe the new species here.
The fourth entity recognized by the GMYC analysis
within D. ricinus s. l. corresponds in morphology (includ-
ing its white aperture) and locality to the subspecies
D. ricinus lischkei, endemic to the Red Sea (Figs 1 and S1;
Monsecour & Wuyts 2007). Although D. ricinus lischkei
was recognized as a significant entity by the GMYC analy-
sis, COI divergence between this entity and its sister clade,
D. ricinus s. s., is low (3.5%), and there are no fixed differ-
ences between it and D. ricinus s. s. in the nuclear gene
(Table S2). Therefore, we do not elevate it to species sta-
tus, but retain D. ricinus lischkei as a subspecies.
The other two subspecies of Drupa recognized by
Monsecour & Wuyts (2007; D. clathrata miticula and
D. morum iodostoma; Table 1) exhibit similar levels of
morphological divergence from their respective nominal
subspecies to those shown by D. ricinus lischkei (Emerson
& Cernohorsky 1973; Monsecour & Wuyts 2007); their
status remains to be tested. Our revised classification is
summarized in Table 1.
Timing and mode of speciation of Drupa
Drupa is estimated to have diversified in the Late Oligo-
cene (25.5 Ma; Fig. 2); this estimate is older than the avail-
able fossils (Pleistocene; Vermeij & Carlson 2000), but
consistent with ages estimated for other intertidal and reef-
associated gastropod clades, including two within Conus
(late Oligocene to early Miocene; Williams & Duda 2008).
Species divergences are estimated to have taken place in
the Late Miocene (5.5–11.5 Ma; Fig. 2). These diver-
gences may have been stimulated by the considerable
expansion and reorganization of coral reefs in the Miocene
(Wilson & Rosen 1998; Crame & Rosen 2002; Hughes
et al. 2002; Wallace & Rosen 2006), which led to an
increase in available habitat. From the early Miocene, the
Indo-West Pacific fauna appears to have been character-
ized by trophic novelty and dietary specialization across
many taxa (Kohn 1990; Vermeij & Carlson 2000; Vermeij
2001b; Bellwood et al. 2010). Consistent with this pattern,
the genus Drupa includes some dietary specialists (D. clath-
rata, D. aperta, D. morum and D. rubusidaeus; Bernstein
1974; Taylor 1983; Fig. 3). However, it is possible that
Drupa species are less specialized than they at first appear
and may have the ability to feed on other types of prey
when it is available. For example, D. rubusidaeus is known
as a specialized polychaete feeder (Bernstein 1974; Taylor
d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters, 41, 2, March 2012, pp 137–149

1983), but nevertheless feeds mostly upon sponges at Addu
Atoll (Taylor 1983). Perhaps, where prey are abundant or
competition intense, diets are specialized, but in marginal
habitats, species are more opportunistic.
Unfortunately, dietary information is not available for
all species of Drupa, leading to uncertainty in the
attempted reconstruction of dietary evolution across the
genus (Fig. 3). In this reconstruction, we have assumed
that broad dietary range is a conserved character,
although this is known only in the case of two species
pairs. If future studies support this prediction, clades
within Drupa appear to be characterized by dietary
adaptations. While D. aperta and D. clathrata retain the
plesiomorphic muricid diet of slow-moving or sedentary
hard-shelled prey (Taylor 1978, 1983; Vermeij & Carlson
2000), the other two clades of Drupa species prey mainly
upon more mobile organisms. Both D. morum and
D. rubusidaeus are known to feed upon errant eunicid and
nereid polychaetes (Taylor 1983; Thomas & Kohn 1990;
J. D. Taylor, personal communication), while species
within D. ricinus s. l. use entrapment behaviours to feed
upon fish and nereid polychaetes (Taylor 1982, 1983;
J. D. Taylor, personal communication). Such adaptations
suggest that major shifts in feeding behaviour accompa-
nied the early diversification of the genus (see also Taylor
1978). A similar phylogenetic pattern of dietary special-
ization of entire clades has been described in the much
more diverse cone snails (Duda et al. 2001) and labrid fish
(Cowman et al. 2009).
In the marine realm, diversification of invertebrates with
widespread larval dispersal has repeatedly been interpreted
as the result of primarily allopatric speciation (see e.g.
Williams & Reid 2004; Reid 2007; Frey 2010; Claremont
et al. 2011b). This pattern could also be expected in
Drupa, in which the combination of planktotrophic (and
probably long-lived) larvae (Taylor 1975) and effective
long-distance colonization (Emerson & Cernohorsky
1973; Monsecour & Wuyts 2007) suggest that gene flow
is high. However, in Drupa, the allopatric signal is not
strong, because only one sister–species pair is entirely allo-
patric (D. aperta–D. clathrata; Fig. 3; Table 2). Neverthe-
less, an additional two species pairs have highly
asymmetrical ranges, with the more narrowly distributed
sister in a peripheral position (D. denticulata from the
Mascarene Islands; D. speciosa from the Tuamotus and Pit-
cairn; Fig. 3; Table 2). Similar patterns in other marine
invertebrates have been interpreted as indicative of periph-
eral (peripatric) allopatric speciation, with range overlap
being the result of subsequent range expansion (Barrac-
lough & Nee 2001; Frey 2010; Malay & Paulay 2010).
The pattern in the sister–species pair D. ricinus s. s.–
D. albolabris is different. The ranges of these sister species
ª 2012 The Authors d Zoologica Scripta ª 2012 The Norwegian Academy of Science and Letters, 41, 2, March 2012, pp 137–149
M. Claremont et al. d Speciation and dietary specialization in Drupa
are highly symmetric as well as broadly sympatric across
the entire Indo-West Pacific (Fig. 3; Table 2). Symmetry
and extensive sympatry are contrary to the predictions of
the (peripatric) allopatric model of speciation (although
this signature can of course be removed by range shift fol-
lowing initial allopatry). In addition, diet appears to be
similar between the two species, contrary to the expecta-
tions of a dietary ecological model. For example, Taylor
(1983) found no significant difference in the broad taxo-
nomic composition of the diets of D. ricinus s. s. and
D. albolabris from Kenya and Guam (species from both
localities consumed crustaceans, vermetid gastropods, chi-
tons and polychaetes). Thomas & Kohn (1990) compared
the diets of D. ricinus s. s. and D. albolabris (as D. arachnoides
and D. ricinus, respectively) collected in different habitats
at Enewetak Atoll and showed that while the diet of
D. albolabris was different in more exposed locations
(D. ricinus s. s. was not present in exposed locations), die-
tary composition did not differ significantly between the
species when collected from the same locality (Taylor
1983). The dietary similarity in this pair of sympatric sis-
ter species, combined with possible opportunism in other
supposedly specialist Drupa species, suggests that dietary
shifts have not played a major role in the most recent spe-
ciation of Drupa. Nevertheless, it remains a possibility that
diet is specialized at a finer taxonomic scale, which has not
been revealed by existing studies that have recorded broad
prey categories. Fine-scale dietary preferences have been
found in Conus (Kohn 1968, 1980; Kohn & Nybakken
1975), indicating that future analyses of dietary composi-
tion in carnivorous snails must take into account prey
preferences at the species level.
While there is yet no evidence for dietary differences
between D. ricinus s. s. and D. albolabris, some differences
in microhabitat have been reported. Although these spe-
cies may occur together, even occupying the same rock
(Emerson & Cernohorsky 1973; Taylor 1983; M.
Claremont & D.G. Reid, personal observation), D. albola-
bris is more abundant in sites of high wave action, such as
reef edges and algal-ridge habitats (Bernstein 1974; Taylor
1983; Kohn 1987; Thomas & Kohn 1990). In both Hawaii
and Clipperton Island, D. albolabris is common in the
intertidal zone, but D. ricinus s. s. is found only subtidally
(Hertlein & Allison 1960; Kay 1979; M. Claremont, per-
sonal observation). It is possible that this ecological prefer-
ence for microhabitats differing in exposure to waves may
have promoted speciation at a very small scale, even in the
face of gene flow.
Habitat partitioning has also been implicated in the
diversification of other marine groups, at a variety of dif-
ferent scales. At a broad geographical scale, a preference
for low or high productivity environments limits species
145
Speciation and dietary specialization in Drupa d M. Claremont et al.
distributions, even of species with widespread dispersal;
this preference may have influenced speciation (e.g. Echino-
littorina: Williams & Reid 2004; Stramonita: Claremont
et al. 2011b; reef fishes: Rocha et al. 2005; see also Krug
2011). At the very smallest spatial scale, different ecotypes
of Littorina saxatilis (a viviparous species with no
pelagic dispersal) occupy different microhabitats on the
same shore, within the range of potential gene flow
(Johannesson et al. 1993; Johannesson 2001; Grahame
et al. 2006). This has been used as an example of incipient
non-allopatric or ecological speciation (Rolán-Alvarez
et al. 2004; Butlin et al. 2008). Such a pattern is also seen
in the genus Nucella, where sister species with restricted
dispersal are sympatric in central California, and separated
on the shore by degree of wave exposure (Marko 1998,
2004). In terms of its likely wide gene flow, the ecological
separation between D. ricinus s. s. and D. albolabris is on a
remarkably small scale, even between exposed and
sheltered habitats in the same locality.
In conclusion, peripatric allopatric speciation appears to
have been the primary mode of the most recent diversifi-
cation in the genus Drupa. There is some evidence for
ecological speciation in the sister–species pair D. ricinus
s. s.–D. albolabris but, contrary to expectation, this is
related to microhabitat (or hypothetical dietary preferences
at a fine taxonomic scale) rather than to choice among
broad prey categories. Specialization on broad prey
groups, and associated prey-capture behaviour, may never-
theless have played a role in diversification at deeper levels
in the phylogeny of Drupa.
Acknowledgements
We would particularly like to thank J. D. Taylor for
invaluable discussions and advice during the preparation of
this manuscript. We are very grateful for the assistance
and loans provided by the staff of museums and research
institutions, especially C. Bird of the Hawaii Institute of
Marine Biology, Kane’ohe, Hawaii; R. Kawamoto of the
Bishop Museum, Honolulu, Hawaii; P. Bouchet, V. Héros,
B. Buge and N. Puillandre of Museum nationale d’His-
toire naturelle, Paris (MNHN); G. Paulay, J. Slapcinsky
and M. Bemis of the Florida Museum of Natural History;
J. Harasewych of the National Museum of Natural His-
tory, Smithsonian Institution, Washington DC; M. Olive-
rio and A. Barco of ‘La Sapienza’ University of Rome; and
A. Miller of the Australian Museum, Sydney. We would
also like to thank the many others who provided speci-
mens or who assisted in the field, including C. Bennett,
T. Haga, T. Hamada, G. Herbert, Y. Ito, R. Jones,
Y. Kano, P. Kuklinski, T. Nakano and K.S. Tan. The
MNHN material used in this study was collected during
the following expeditions: the PANGLAO 2004 Marine
146 ª 2012 The Authors
Biodiversity Project [a joint project between University of
San Carlos, Cebu City (USC; co-PI Danilo Largo) and
MNHN (co-PI Philippe Bouchet), funded by the Total
Foundation and the French Ministry of Foreign Affairs];
the AURORA 2007 cruise [M ⁄ V DA-BFAR associated
with the National Museum of the Philippines (NMP,
co-PI Marivene Manuel), MNHN (co-PI Philippe Bou-
chet) and BFAR, funded through a grant from the Louns-
bery Foundation]; the MNHN-IRD-PNI Santo 2006
expedition (funded by grants from, among others, the
Total Foundation and the Stavros Niarchos Foundation);
EBISCO, NORFOLK 2 and CONCALIS cruises [R ⁄ V
Alis deployed from Nouméa by the Institut de Recherche
pour le Développement (IRD)]. M.C. was supported by a
studentship from the Natural History Museum, London
and by an Imperial College Deputy Rector’s studentship.
We thank Thomas Duda Jr. and one anonymous reviewer
for helpful comments on a previous version of this
manuscript.
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Supporting Information
Additional Supporting Information may be found in the
online version of this article:
Fig. S1. MRBAYES Bayesian phylogeny of Drupa and
rapanine outgroups based on single-gene analysis of 12S.
Fig. S2. MRBAYES Bayesian phylogenies of Drupa and
muricid outgroups based on single gene analysis of (A)
28S rRNA and (B) cytochrome c oxidase subunit I (COI).
Table S1. Specimens used in this study with GenBank
numbers, localities and locations of voucher specimens.
Table S2. Positions of fixed differences in the 28S
rRNA gene among Drupa species.
Please note: Wiley-Blackwell are not responsible for the
content or functionality of any supporting materials sup-
plied by the authors. Any queries (other than missing
material) should be directed to the corresponding author
for the article.
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