Journal o f
The Malacological Society of London
Molluscan Studies
Journal o f Molluscan Studies (2013) 79: 1 9 -2 9 . d o i:10.1093/m ollus/eys028
A d v a n ce Access p u b lic a tio n d a te : 29 N o v e m b e r 2012
A M O L E C U L A R PH Y LO G EN ETIC FR A M E W O R K FOR THE
ERGALATAXINAE (NEO G ASTRO POD A : M U R IC ID A E )
M A R T I N E C L A R E M O N T 12, R O L A N D H O U A R T 3, SU ZA NN E T. W I L L I A M S 1
AND DAVID G. R E I D 1
d e p a rtm e n t o f foology, .Natural History M useum , London S [ I 7 5 B D , U K ;
^Division o f Biology. Imperial College London, Si.lwood Park Campus, Ascot S L 5 7P T , U K ; and
fn s titu t Royal des Sciences .Naturelles de Belgique, Rue Vautier, Brussels, Belgium
(R e ce iv e d 2 A p ril 2012; a c c e p te d 28 S e p te m b e r 2012)
ABSTRACT
T h e v a lid ity o f th e m u ric id su b fam ily E rg a la ta x in a e has re ce n tly b e en co n firm ed w ith m o le c u la r
d a ta , b u t its c o m p o sitio n a n d th e re la tio n sh ip s a m o n g its c o n stitu e n t g e n e ra re m a in u n c le ar. In o rd e r
to investigate this, we use fo u r genes (28S rR N A , 12S rR N A , 16S rR N A a n d c y to c h ro m e c oxidase
su b u n it I ) to c o n stru c t a B ayesian p h y lo g e n y o f 52 e rg a la ta x in e species in 18 g e n era , re p re se n tin g c.
4 0 % o f th e c u rre n tly a cc ep te d species a n d 8 6% o f th e g e n era . T h is is th e m ost co m p lete p h y lo g en y
o f this ta x o n o m ic a lly confusing su b fam ily yet p ro d u c e d . O u r results in d ic a te th e p o ly p h y ly o f m a n y
tra d itio n a l g en era, in c lu d in g Morula, Pascula a n d Orania. I n o rd e r to im p ro v e th e co rre sp o n d e n c e
b etw ee n classification a n d phy lo g en y , we restrict th e d e fin itio n o f M orula, re su rrec t Tenguella a n d
elevate Oppomorus to full genus, b u t d escrib e no new g e n era . Several species in this analysis co u ld not
be id en tifie d a n d m ay be new , b u t we d o n o t d escrib e th em . F u rth e r m o le c u la r a n d m o rp h o lo g ic al
analyses, in th e c o n te x t o f this fram ew o rk , sh o u ld h e lp to resolve th e re m a in in g a m b ig u itie s in the
classification o f this subfam ily. T h e oldest fossil m e m b e r o f th e E rg a la ta x in a e k n o w n to us is o f E a rly
O lig o cen e age.
INTRODUCTION
T h e M u ric id a e a re a larg e, tax o n o m ic a lly com plex fam ily o f
n eo g astro p o d s. M a n y species in this fam ily are well k n o w n for
th e ir c h arism atic shells (M urex, Chicoreus), as p re d a to rs
( Ocenebra, Urosalpinx) o f c o m m ercially im p o rta n t oysters, as a n
a n c ie n t source o f p u rp le dye (Bolinus, Plicopurpura) o r as food
item s (Concholepas, M urex). H ow ever, u n til recently, th e p h y l­
o geny o f th e fam ily w as p o o rly know n; subfam ilies h a v e been
e rec te d b a se d larg e ly on superficial shell a n d ra d u la r resem ­
blan ces r a th e r th a n o n rigorous p h y lo g en e tic analyses. O n e
su ch su b fam ily is th e E rg a la ta x in a e , th e diagnosis o f w h ic h was
b a se d o n so m ew h at v a g u e c h a ra c te rs o f th e shell, o p e rcu lu m ,
ra d u la a n d egg c apsule (K u ro d a & H a b e , 1971). I t h a s been
criticised as “ th e least w ell-defined [subfam ily] in th e e n tire
fam ily M u ric id a e " (Vokes, 1996a, 27). E v er since its in tr o d u c ­
tion, th e ta x o n o m y o f th e g ro u p a n d its re la tio n sh ip to a n o th e r
m u ric id subfam ily, th e R a p a n in a e ( = T h a id in a e o f a u th o rs ),
h a s b e e n controversial. Som e w orkers c o n te n d e d th a t th ere
w as little m o rp h o lo g ic al s u p p o rt for th e se p a ra tio n o f the
R a p a n in a e a n d E rg a la ta x in a e (T a n , 1995, 2000). O th e rs
d e sc rib e d new e rg a la ta x in e g e n e ra a n d tra n sfe rre d existing
g e n e ra to th e su b fam ily (e.g. H o u a rt, 1995a, b, 1997; Vokes,
1996a, b ). R e c e n t m o le c u la r p h y lo g en e tic analyses h a v e tested
these o p p o sin g views, estab lish in g th e m o n o p h y ly o f the
E rg a la ta x in a e a n d su p p o rtin g its re co g n itio n as a subfam ily
(C la re m o n t, R e id & W illiam s, 2008; B arco et al., 2010;
C la re m o n t et ed., in press).
Like th e rest o f th e M u ric id a e , e rg a la ta x in e s are carn iv o ro u s,
p re y in g u p o n a w ide v a rie ty o f org an ism s in c lu d in g corals,
p o ly ch aetes, b a rn ac le s a n d o th e r m olluscs (e.g. T a y lo r, 1980;
T a n , 1995; Ish id a , 2004; C la re m o n t, R e id & W illiam s, 2011a).
E rg a la ta x in e s are m ain ly fo u n d in th e tro p ic a l In d o -W e st
Pacific a n d o c cu p y a w ide ra n g e o f h a b ita ts , w ith som e species
c o m m o n in th e h ig h in te rtid a l, w hile o th ers live m ore th a n
500 m d e ep (K u ro d a & H a b e , 1971; H o u a rt, 1995b; T a n ,
1995). T h e su b fam ily w as in itially estab lish ed for only th ree
g e n e ra (Ergalatax, Bedevina a n d Cytharomorula), b u t m a n y t r a d ­
itio n a lly ‘th a id id ’ g e n e ra h ave b e e n tran sferre d to it subse­
q u e n tly (e.g. Morula, Spinidrupa, Cronia, Drupella; T rö n d lé &
H o u a rt, 1992; K o o l, 1993; V okes, 1996a; T a n , 2000; V erm eij
& C a rlso n , 2000; H o u a rt, 2004; C la re m o n t et al., 2 011a). N ew
e rg a la ta x in e g e n e ra h a v e also b e e n d e scrib ed , based o n c h a ra c ­
ters o f th e shell a n d ra d u la (e.g. Habromorula', H o u a rt, 1995a).
C h a ra c te rs o f th e shell, in te rn a l a n a to m y a n d ra d u la h ave
also b e en used to suggest affinities b e tw ee n v a rio u s g e n e ra (e.g.
F u jio k a, 1985; H o u a rt, 1995a, b, 2004), b u t cases o f p lasticity,
iC) 77íe Author 2012. Published by Oxford Uniiersity Press on behalf o f The Malacological Society o f London, all rights reseroed
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Correspondence: A I. Claremont; e-mail: m .elaremontidnhm.ae.uk
M. C L A R E M O N T E T A L .
p o ly m o rp h ism a n d o f p a ra lle l a n d co n v erg e n t ev o lu tio n w ith in
th e E rg a la ta x in a e h ave m a d e p h y lo g en e tic re co n stru c tio n
based o n m o rp h o lo g y difficult. F o r exam ple, r a d u la r m o rp h ­
ology has b e en show n to v a ry w ith in species a cc o rd in g to
sex, g ro w th ra te a n d season (F ujioka, 1985; K o o l, 1993; T a n ,
1995). S u c h is th e p re v alen c e o f h o m o p la sy in m o rp h o lo g ic al
c h a ra c te r tran sfo rm a tio n s th a t e arly cladistic analyses d id not
even find su p p o rt for th e m o n o p h y ly o f th e E rg a la ta x in a e
(K ool, 1993; V erm eij & C arlso n , 2000). A lth o u g h m o le c u la r
studies h a v e c o n firm ed its m o n o p h y ly (see a bove), so far th ey
h ave suffered from lim ite d tax o n o m ic sam p lin g . A c o m p re h e n ­
sive m o le c u la r analysis o f this im p o rta n t su b fam ily rem ain s to
be do n e.
P revious m o le c u la r p h y lo g en e tic analyses o f th e M u ric id a e
have in c lu d e d only a few re p re se n tativ es o f th e E rg a la ta x in a e
(6 species in C la re m o n t et id., 2008; 10 species in B arco et ed.,
2010; 6 species in C la re m o n t et ed., in press). Elere, we aim to
pro v id e a m o re co m p reh en siv e p h y lo g en e tic fram e w o rk o f th e
E rg a la ta x in a e for fu rth e r tax o n o m ic, ecological a n d phylogeog ra p h ic w ork; to test m o n o p h y ly o f n o m in a l g e n e ra c u rre n tly
d efin ed b y m o rp h o lo g ic al c h a ra c te rs a n d to p ro v id e a new
p h y lo g en e tic classification. T o d o this, w e c o n stru ct a m o le c u ­
la r p h y lo g e n y o f 52 e rg a la ta x in e species using one n u c le a r a n d
th ree m ito c h o n d ria l genes.
W h e re generic assignm ents re m a in u n c le a r (because o f polyp h y ly a n d /o r lack o f ty p e species in th e analysis), we h ave fol­
low ed those o f H o u a r t (e.g. H o u a rt, 1986, 1987, 1991, 1995a,
b, 1996a, b, 1997, 1998, 2000, 2002, 2004, 2008), except for
'T h a is’ castanea (w here we have follow ed S teyn & Lussi, 1998).
Single q u o ta tio n m ark s h ave b e en used to in d ic a te these cases
o f u n c e rta in ty .
D .N A sequencing and alignm ent
M A T E R I A L AND M E T H O D S
T a x on sam pling and identification
A to ta l o f 109 e rg a la ta x in e specim ens w ere o b ta in e d for m o ­
le c u la r analysis (S u p p le m e n ta ry M a te ria l, T a b le S I). T h ese
w ere id en tifie d m o rp h o lo g ic ally b y th e a u th o rs (R .H ., D .G .R .
a n d M .C .) as b e lo n g in g to 52 species in 18 g en era, re p re se n t­
in g 4 0 % o f th e c. 129 a cc ep te d species in th e su b fam ily a n d
all b u t th ree o f th e 21 c u rre n tly a cc ep te d g e n e ra (H o u a rt,
1986, 1987, 1991, 1995a, b, 1996a, b, 1997, 1998, 2000, 2002,
2004, 2008; T rö n d lé & H o u a rt, 1992; T a n , 1995; Vokes,
1996b; V erm eij & C arlso n , 2000; T a b le 1). W e h ave sequenced
th e ty p e species o f 15 g e n e ra (H o u a rt, 1995b; V erm eij &
C arlso n , 2000; T a b le s 1, S u p p le m e n ta ry M a te ria l T a b le S I).
B ased o n m o rp h o lo g y , n in e a d d itio n a l g e n e ra h av e been
in c lu d e d in th e E rg a la ta x in a e by som e a u th o rs (T rö n d lé &
H o u a rt, 1992; H o u a rt, 1995b, 2004; V okes, 1996b). O f these
n in e g e n era , one is u n a v a ila b le ; one is a possible sy n o n y m o f
a n o th e r e rg a la ta x in e genus; th re e h ave b e en rem oved from th e
su b fam ily o n th e basis o f th e ir m o rp h o lo g y (P o n d e r, 1972;
R a d w in & D ’A ttilio, 1976; R . H o u a rt, 2010, u n p u b h ); a n d
one has b e en rem oved based on m o le c u la r analyses (B arco
et al., 2010; see S u p p le m e n ta ry M a te ria l, T a b le S2). T h e th ree
e rg a la ta x in e g e n e ra n o t in c lu d e d in o u r analysis (Daphnellopsis,
Lindapterys, Uttleya) are p o o rly k n o w n a n d lack cle ar m o rp h o ­
logical sim ilarities to o th e r E rg a la ta x in a e , so h ave b e en p laced
in th e E rg a la ta x in a e only te n ta tiv e ly (R . H o u a rt, u n p u b h ;
S u p p le m e n ta ry M a te ria l, T a b le S2). R e p re se n ta tiv e species o f
these g e n e ra should be in c lu d e d in fu tu re m o le c u la r analyses.
W e used 66 prev io u sly p u b lish e d e rg a la ta x in e sequences
(S u p p le m e n ta ry M a te ria l, T a b le S I; C la re m o n t et ed., 2008,
2011a; B arco et ed., 2010). O u tg ro u p species w ere selected front
th e R a p a n in a e , as this is th e sister su b fam ily to th e
E rg a la ta x in a e in som e analyses (C la re m o n t et ed., 2008; b u t see
B arco et ed., 2010). A ll ra p a n in e o u tg ro u p sequences h av e p re ­
viously b e en p u b lish e d (C la re m o n t et ed., 2008; B arco et ed.,
2010).
N ew
sequences
w ere
su b m itte d
to
G enB ank
(S u p p le m e n ta ry M a te ria l, T a b le SI ). L o c a tio n o f v o u c h er m a ­
te ria l is n o te d in S u p p le m e n ta ry M a te ria l, T a b le S I. G en eric
assignm ents in th e follow ing tex t a n d figures a re valid , based
o n th e conclusions o f this stu d y (su m m arize d in T a b le 1).
20
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F o r all sam ples, th re e m ito c h o n d ria l genes [c y to ch ro m e c
oxidase su b u n it I (C O I), 16S rR N A a n d 12S rR N A ] a n d one
n u c le a r g ene (28S rR N A ), k n o w n to be in fo rm a tiv e for p h y lo ­
ge n etic analysis in th e M u ric id a e (C la re m o n t et al., 2008;
B arco et al., 2010), w ere seq u en ced , follow ing th e p ro to co ls o f
C la re m o n t et cd. (2011b). P olym erase c h a in reactions (P C R s)
a m p lifie d c. 1500 b p o f 28S, 750 b p o f 16S, 700 b p o f C O I a n d
650 b p o f 12S. P rim ers a n d P C R co n d itio n s for all genes w ere
as d e sc rib e d by B arco et ed. (2010), except for som e fo rw ard
frag m e n ts o f 16S th a t w ere o b ta in e d using a new in te rn a l
p rim e r, 1 6 S -In t5 6 F (5'-A A C R G C C G C G G T A C T C T G -3 ')
a n d som e C O I sequences th a t w ere o b ta in e d using p rim e rs
C O I F a n d C O I-M L T R (C la re m o n t et ed., 2011b). W e w ere
u n a b le to am p lify all genes for all specim ens. T h u s, th e 12S
a lig n m e n t consisted o f 115 sequences, th e 16S a lig n m e n t o f
106 sequences, th e 28S a lig n m e n t o f 95 sequences a n d th e
C O I a lig n m e n t o f 78 sequences (S u p p le m e n ta ry M a te ria l,
T a b le S I ).
S equences w ere assem bled a n d e d ite d w ith S e q u e n ch e r
(v. 4.8; G en eC o d es C o rp o ra tio n , A n n A rb o r, M I). C le a r h e t­
erozygous peaks in b o th th e fo rw a rd a n d reverse sequence o f
28S w ere cod ed as p o ly m o rp h ism s. A fter rem o v al o f p rim e r
regions, 28S sequences w ere 1497 b p a n d 12S sequences w ere
573 b p . C O I sequences o b ta in e d w ith C O IF /C O I-M L T R w ere
703 b p ; those sequences o b ta in e d using u n iv ersal p rim e rs
(F o lm er et ed., 1994) w ere 658 b p . S equences o f 16S o b ta in e d
w ith C G L e u R (H ay ash i, 2005) a n d 1 6 S -In t5 6 F (this p a p e r)
w ere 705 bp, w hile those o b ta in e d w ith C G L e u R (H ay ash i,
2005) a n d 16SA (P a lu m b i et ed., 1991) w ere 825 bp.
R ib o so m a l (28S, 16S a n d 12S ) sequences w ere a lig n e d using
th e Q T N S -i m e th o d o f M A F F T (M u ltip le A lig n m e n t using
Fast F o u rie r T ra n sfo rm ; v. 6.847b; K a to h & T o li, 2008). Based
o n p re lim in a ry analyses, we d id n o t expect long gaps in o u r
a lig n m en ts, so th e offset v a lu e was set to 0.1. T h e resu ltin g
a lig n m en ts w ere a d ju ste d by eye in M a c C la d e (v. 4.06 O S X ;
M a d d iso n & M a d d iso n , 2003). G blocks (v. 0.91 b eta;
C a stresan a , 2000) w as th e n used to rem ove p o o rly a lig n ed
sites (m in im u m n u m b e r o f sequences for a conserved position:
7 0 % ; m in im u m n u m b e r o f sequences for a flan k in g p o s­
ition: 9 0 % ; m a x im u m n u m b e r o f c o n tig u o u s no n -co n serv ed
positions: 3; m in im u m le n g th o f a block: 5; all g a p p ositions
allow ed). E lim in a tio n o f a m b ig u o u s regions re d u ce d th e 28S
a lig n m e n t by 5% to 1432 b p , th e 12S a lig n m e n t b y 10% to
518 b p a n d th e 16S a lig n m e n t by 14% to 620 bp. C O I
sequences w ere a lig n e d by eye in M a c C la d e . T h e re w ere 91
p h y lo g en e tic ally in fo rm a tiv e base p a irs in 28S, 232 b p in 12S,
173 b p in 16S a n d 272 b p in C O I.
F o r eac h g ene p a rtitio n , 24 different m odels o f n u c le o tid e
su b s titu tio n w ere tested w ith M rM o d e lT e s t (v. 2.2; N y la n d e r,
2004). A d d itio n a lly , w e tested a site-specific m o d el o f evo lu tio n
o f C O I using PALTP* (v. 4 .0 b l0 ; Sw offord, 2002). T h e m odel
chosen b y b o th th e h ie ra rc h ic a l ra tio test a n d A k a ik e ’s
In fo rm a tio n C rite rio n in M rM o d e lT e s t w as G T R + I + G for
28S, 16S a n d 12S, a n d H K Y + I + G for C O I. C o m p a riso n o f
log-likelihood values in d ic a te d th a t H K Y + I + G w as a
significantly b e tte r fit to th e d a ta th a n a m o d el th a t allow ed
site-specific ra te v a ria tio n across c o d o n p a rtitio n s .
M O L E C U L A R PH Y L O G E N Y O F E R G A L A T A X IN A E
T a b le 1. S ta tu s o f g e n e ra o f E r g a la ta x in a e in c lu d e d in th is study.
G enus
Type species
First placed in
Type species
Ergalataxinae by
analysed herein
Validity
Bedevina Habe, 1946
Trophon birileffi Lishke, 1871
Kuroda & Habe, 1971
Y es
Valid; could include Spinidrupa
Cronia H. & A. Adams,
Purpura amygdala Kiener, 1835
Tröndlé & Houart, 1992
Y es
Valid; could include Maculotriton and
Cytharomorula vexillum Kuroda,
Kuroda & Habe, 1971
Y es
U ncertain; not m onophyletic in any analysis
C larem ont e ta /., 2011a
Y es
Valid
Kuroda & Habe, 1971
No (although included
Uncertain; not m onophyletic in any
Ergalatax
1853
Cytharomorula
Kuroda, 1953
Drupella Thiele, 1925
1953
Purpura elata Blainville, 1832
[=D rupa cornus Röding,
1798]
Ergalatax I redale,
1931
Ergalatax recurrens Iredale,
1931 [ = Murex pauper
E. contracta is
analysis. In clade with Cronia and
W atson, 1883]
possible synonym ;
Maculotriton ; potential synonym of Cronia
Houart, 2008)
Habromorula H ouart,
Purpura biconica Blainville, 1832
H ouart, 2004
Y es
Not a valid genus; w ithin Morula clade;
m onophyly of Habromorula not strongly
1995
contradicted, so potentially valid
Jousseaum e, 1883
Lataxiena lataxiena
H ouart, 1995b
Y es
Valid; com position unclear due to
uncertainty surrounding Orania
Jousseaum e, 1883
[ = Trophon fimbriata Hinds,
1844]
Maculotriton Dali, 1904
Triton bracteata Hinds, 1844
Tröndlé & Houart, 1992
Y es
Valid; potential synonym of Cronia
H ouart, 2004
Y es
Valid; definition restricted (cf. H ouart, 2002,
[ = Buccinum serriale
Deshayes, 1834]
Morula Schum acher,
1817
Morula papillosa Schum acher,
1917 [=D rupa uva Röding,
2004)
1798]
Muricodrupa Iredale,
1918
Oppomorus Iredale,
Purpura fenestrata Blainville,
Tröndlé & Houart, 1992
Y es
Valid; definition restricted (M. fiscella
Morula nodulifera M enke, 1829
H ouart, 2004
Y es
Valid genus (subgenus o f H ouart, 2004)
Pseudomurex spadae Libassi,
H ouart, 1995b
No
Uncertain; type species not included;
1832
excluded)
1937
Orania Pallary, 1900
1859 [= M urex fusulus
species previously assigned to Orania
Brocchi, 1814]
form clades with m em bers of Lataxiena,
Usilla, Cytharomorula and Pascula.
Pascula Dali, 1908
Trophon citricus Dali, 1908
Tröndlé & Houart, 1992
No
Uncertain; type species not included;
Phrygiomurex Dali,
Triton sculptilis Reeve, 1844
Tröndlé & Houart, 1992
Y es
Valid
Murex euracantha A. Adams,
H ouart, 1995a
Y es
Uncertain; som e species in clade with
Purpura granulata Duelos, 1832
T his study
Y es
Valid; synonym ized with Morula by Fujioka
Trachypollia sclera W oodring,
Vokes, 1996a
No
Probably valid, although sam pling lim ited
Vokes, 1996b
Y es
Valid, but type in clade with type of
paraphyletic as currently defined
1904
Spinidrupa Habe &
Kosuge, 1966
Tenguella Arakawa,
Bedevina, which has priority
1851
(1985), but shown here to be distinct
1965
Trachypollia W oodring,
1928
Usilla H. Adam s, 1861
and type species not included
1928
Vexilla nigrofusca Pease, 1860
[ = Vexilla fusconigra Pease,
Lataxiena and som e Orania-, retained as
1860 = Purpura avenacea
genus because m orphologically distinct
Lesson, 1842]
(follow ing Vokes, 1996b; H ouart &
Tröndlé, 2008)
S ee Supplem entary m aterial, Table S2 fo r status o f unsam pled, excluded and doubtful genera. Valid genera are those confirm ed as m onophyletic, with type
species included. Potential synonym y and other uncertainties should be resolved by fu rth e r sam pling and analysis.
p a ra m e te rs for each gene w ere set a cc o rd in g to th e m odel
selected b y M r M o d e l T est a n d w ere free to v a ry a m o n g gene
p a rtitio n s . T h e re w ere tw o in d e p e n d e n t ru n s o f th e M C M C
analysis, eac h using fo u r chains. C o n v erg en ce b e tw ee n th e in ­
d e p e n d e n t M C M C ru n s was tested b y e x am in in g th e average
P hylogenetic analysis ( single gene)
A ll single-gene a lig n m en ts w ere a n aly se d using B ayesian in fe r­
ence a n d th e M a rk o v C h a in M o n te -C a rlo M e th o d (M C M C ;
M rB ayes v. 3.1; H u e lse n b ec k & R o n q u ist, 2001). M o d e l
21
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subgenus
Lataxiena
M. C L A R E M O N T E T A L .
d e v ia tio n s o f split frequencies a n d th e p o te n tia l sc a le -red u c tio n
fa cto r (P S R F ), as w ell as th e traces in T ra c e r (v. 1.5;
D ru m m o n d & R a m b a u t, 2007). T h e M C M C analysis w as ru n
for five m illio n g e n era tio n s u n til th e M C M C ru n s converged.
I n all cases, we used a sam p le freq u e n c y o f 1,000 a n d a
b u rn -in o f 1,501; o th e r p a ra m e te rs w ere d e fa u lt v alues. C lades
w ith p o ste rio r p ro b a b ility (P P ) > 9 5 % w ere considered well
su p p o rte d , w hile P P o f 9 0 - 9 5 % w as ta k e n as m a rg in a l
su p p o rt. B ranches in th e consensus tree s u p p o rte d b y P P
< 5 0 % w ere collapsed. A ll P S R F values for M rB ayes analyses
w ere 1.00, w hile a v erag e d e v ia tio n s o f split frequencies
co n v erg ed on zero, in d ic a tin g th a t all trees h a d reach ed
sta tio n a rity .
Genus-level clades
Construction and analysis o f concatenated alignm ents
In sp e c tio n o f in d iv id u a l g ene trees d id n o t reveal a n y wells u p p o rte d clades (P P > 9 5 % ) in conflict. C onflict a m o n g
strongly s u p p o rte d clades (P P > 9 5 % ) c a n be in te rp re te d as
evidence o f g e n etic in c o n g ru e n c e a n d d iv e rg e n t p h y lo g en e tic
histories, w hile conflict a m o n g w eakly su p p o rte d clades (P P <
5 0 % ) m ay be d u e to stochastic e rro r (W iens, 1998; R e e d e r,
2003; W illiam s & O z aw a, 2006). W e therefore c rea te d c o n c a te ­
n a te d d atasets. As m ore sequences w ere a v ailab le for 28S a n d
12S th a n for 16S a n d C O I, we c o n stru c te d tw o data se ts: a
fo u r-g en e d a ta se t (28S + 12S + 16S + C O I) a n d a tw o-gene
d a ta se t ( 2 8 S + 1 2 S ) . T h e tw o-gene d a ta se t consisted o f 94
sequences, w hile th e fou r-g en e a lig n m e n t consisted o f 59
sequences.
B ayesian analysis o f th e tw o-gene a n d fou r-g en e d a ta se ts was
p e rfo rm e d exactly as above; M C M C analyses o f b o th d a ta se ts
w ere ru n u n til sta tio n a rity w as re a c h e d a t nine m illion
g en eratio n s.
RESULTS
I n general, th e single-gene analyses w ere less well resolved
th a n tw o-gene a n d four-gene analyses (Figs 1—3), w ith 28S
being p a rtic u la rly po o rly resolved a t the su p rag en eric level
(S u p p le m e n tary M a te ria l, Fig. S I ). W e fo und th a t the tw o-gene
a n d th e four-gene analyses w ere m ost useful for d e te rm in in g the
relationships am o n g g e n era (Figs 1 a n d 2) w hile, because it h a d
the m ost av ailab le sequences, the 12S analysis was m ost useful for
d e te rm in in g relationships a m o n g species (Fig. 3). F o r this reason,
we will n o t discuss the single-gene trees o th e r th a n 12S in detail;
none o f th e re m a in in g single-gene trees have a n y w ell-supported
b ranches in conflict w ith th e trees discussed (S u p p le m e n tary
M a te ria l Fig. S I ).
Suprageneric relationships
T h re e w e ll-su p p o rte d su p ra g en e ric clades w ere fo u n d (Figs 1
a n d 2; C lades A —C; P P = 1 0 0 % ) , w ith a single lineage
(Trachypollia lugubris) in a n a m b ig u o u s p o sitio n (Figs 1 —3).
R e la tio n sh ip s a m o n g th e m a jo r clades w ere n o t w ell su p p o rte d
in m ost trees, a lth o u g h B a n d C fo rm ed a clad e in th e all-gene
tree (Fig. 1; P P = 9 8 % ).
W ith in clade A, we recovered species th a t h ave b e en previous­
ly assigned to th e g e n era Morula sm.su stricto, Muricodrupa a n d
Tenguella (Figs 1 a n d 2; P P = 100% ). In c lu d e d in clade B were
species th a t have b e en previously assigned to Morula s. s.,
Muricodrupa, Morula (Habromorula) a n d Cytharomorula (Figs 1 - 3 ;
P P = 100% ). W ith in clade C fell species th a t h ave previously
b een assigned to Orania, Cronia s. s., Cronia (U silla), Lataxiena,
Drupella, Ergalatax, Maculotriton, Bedevina, Spinidrupa, Morula s. s.,
Morula (Oppomorus), Pascula, Cytharomorula a n d Phrygiomurex
(Figs 1 - 3 ; P P > 9 5 % ).
Species-level relationships
T h is stu d y w as n o t d esigned to test species b o u n d a rie s o r to
resolve
relatio n sh ip s
b e tw ee n
species
com prehensively.
N evertheless, som e results suggest th e need for fu rth e r investi­
g a tio n . W e fo u n d evidence in d ic a tin g tw o possible new species
(Tenguella n. sp. a n d 'M orula’ n. sp.; Figs 1 - 3 ; a n d
S u p p le m e n ta ry m a te ria l, Fig. S I). S m all g e n etic distan ces are
suggestive o f possible sy n o n y m y o f species; for exam ple, th ere
w as < 1 % d iv erg e n ce a m o n g C O I sequences for th e p a ir
Morula uva a n d M . aspera, a n d sim ilarly for th e p a ir Cronia
amygdala a n d C. aurantiaca. I n tw o cases, m orphospecies
w ere n o t m o n o p h y le tic ('Cytharomorula’ cf. grayi a n d 'Pascula
ochrostoma’; Figs 2 a n d 3B).
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Tenguella granulata, T. ceylonica, T. musiva a n d T. marginalba
fo rm ed a w e ll-su p p o rte d su b c lad e FT w ith in m a jo r clad e A,
to g e th e r w ith a n a p p a re n tly u n d e sc rib e d species ( Tenguella
n. sp.; Figs 1 - 3 A ; P P = 1 0 0 % ) . Muricodrupa fenestrata a n d
'M orula’ anaxares form ed a p o o rly su p p o rte d clad e in th e
tw o -g en e a n d fo u r-g en e analyses (Fig. 1, P P = 9 3 % ; Fig. 2,
P P = 8 5 % ). A sister re la tio n sh ip b etw ee n 'M orula’ nodulosa
a n d all o th e r species in m a jo r clad e A w as w ell su p p o rte d
(Figs 1 -3 A ; P P > 9 8 % ).
W ith in m a jo r clad e B a w e ll-su p p o rte d su b c lad e V consisted
o f Morulauva a n d 10 o th e r Morula species (A í. aspera, M . bene­
dicta, M . biconica, M . chrysostoma, M . coronida, M . japonica,
M . nodicostata, M . spinosa, M . striata a n d M . zebrina', Figs 1 -3 A ;
P P > 9 9 % ). 'M orula’ rumphiusi a n d 'M orula’ fiscella fo rm ed a
w e ll-su p p o rte d clad e in all analyses (Figs 1 -3 A ; P P = 1 00% ).
A n u n id e n tifie d species ('M orula’ n. sp.) fell w ith in m a jo r clade
B, b u t its p o sitio n w as n o t resolved (Figs 1 -3 A ).
F o u r w e ll-su p p o rte d subclades W - Z w ere observed w ith in
m a jo r clad e C (Figs 1, 2 a n d 3B; P P > 9 5 % ; b u t Z u n s u p p o rt­
ed in 12S analysis Fig. 3B). Usilla avenacea, Lataxiena fimbriata,
'Orania’ bimucronata, ' 0 . ’ gaskelli a n d ' 0 . ’ serotina fo rm ed su b ­
clad e W (Figs 1, 2 a n d 3B; P P = 1 0 0 % ). W ith in su b clad e x
Drupella cornus, D . eburnea, D . fragum , D . rugosa, D . margariticola
‘C o n tin e n ta r a n d D . margariticola 'O c e a n ic ' fo rm ed a wells u p p o rte d clad e in th e tw o-gene a n d fou r-g en e analyses (Figs 1
a n d 2; P P > 9 5 % ). A sister re la tio n sh ip b e tw ee n this clade
a n d one consisting o f Ergalatax contracta, 'E .’ junionae, Cronia
amygdala, C. aurantiaca a n d Maculotriton serriale w as well su p ­
p o rte d in th e fou r-g en e analysis (Fig. 1; P P = 1 00% ). W ith in
su b c lad e Y, a clad e o f Oppomorus nodulifera, 0 . purpureocincta a n d
0 . funiculata w as well su p p o rte d in th e fo u r-g en e analysis
(Fig. 1; P P = 1 0 0 % ). Also w ith in su b c lad e Y, a clad e consist­
in g o f 'Spinidrupa’ infans, 'S .’ cf. infans, 'Spinidrupa’ sp. a n d
Bedevina birileffi w as w ell su p p o rte d in b o th th e tw o -g en e a n d
fo u r-g en e analyses (Figs 1 a n d 2; P P > 9 8 % ), b u t th e po sitio n
o f Spinidrupa euracantha w as n o t resolved w ith in su b clad e Y
(Fig. 3B). W ith in su b c lad e Z, a clad e consisting o f
Cytharomorula vexillum, 'C .’ cf. gravi, 'C .’ springsteeni, 'Orania’ orna­
mentata, ' 0 . ’ mixta, ' 0 . ’ pacifica, ' 0 . ’ fischeriana, ' 0 . ’ cf. rosea a n d
'T h a is’ castanea w as w ell s u p p o rte d in th e tw o-gene a n d fourgene analyses (Figs 1 a n d 2; P P = 1 0 0 % ). 'Pascula’ ochrostoma
a n d 'P .’ muricata fo rm ed a clad e (Figs 1 a n d 2; P P = 1 0 0 % ), as
d id 'P .’ darrosensis a n d 'P .’ submissa (Figs 2 a n d 3B; P P =
1 0 0 % ). 'M orula’ parva w as sister to all th e o th e r m em b ers o f
su b c lad e Z in th e tw o -g en e a n d fo u r-g en e analyses (Figs 1 a n d
2; P P > 9 5 % ). T h e p o sitio n o f 'Cytharomorula’ paucimaculata in
su b c lad e Z w as u nresolved (Fig. 3B). T h e p ositions o f
Phrygiomurex sculptilis a n d 'M orula’ echinata (only 12S sequence
a v ailab le for th e la tte r) w ith in m a jo r clad e C w ere n o t resolved
(Figs 1, 2 a n d 3B).
M O L E C U L A R PH Y L O G E N Y O F E R G A L A T A X IN A E
Concholepas concholepas
- Dicathais orbita
Rapana bezoar
Thais nodosa
Thalessa aculeata
Mancinella intermedia
100 'Ergalatax'contracta (Malaysia)
t Ergalatax'junionae (UAE)
ïoo~ 'Ergalatax'junionae (K uwait)
M aculotriton serriale (Japan)
f Cronia am ygdala (A ustralia)
1 Cronia aurantiaca (A ustralia)
'Spinidrupa ' infans ( Ma d a g a sc a r)
Bedevina birileffi (Japan)
'Spinidrupa'cf infans (M o z a m b iq u e )
— Spinidrupa sp. (M o z a m b iq u e )
Oppomorus nodulifera (A u stra lia /! 25 7 )
t Oppomorus purpureocincta (Japan)
looi Oppomorus purpureocincta (M alaysia)
r Oppomorus funiculata (J a p a n /0 1 40)
Oppomorus funiculata (J a p a n /0 3 5 5 )
93 Oppomorus funiculata (J a p a n /0 3 4 0 )
'Morula'parva (P h ilip p in es)
- ‘Pascula’ submissa (M o z a m b iq u e /5 4 4 0 )
'Pascula'ochrostoma (P h ilip p in es)
'Pascula' muricata ( M o z a m b iq u e /0 9 5 0 )
— 'Cytharomorula'springsteeni (P h ilip p in es)
'Cytharomorula' cf grayi {New C a le d o n ia /8 2 2 5 )
Cytharom orula vexillum (N e w C a le d o n ia /8 1 74)
loo1—
'Orania'ornamentata (M o z a m b iq u e )
1 QÛ1—
'Orania'fischeriana (M ad agascar)
I ’
Thais'castanea (S o u th Africa)
'Orania'pacifica (P h ilip p in es)
'Orania mixta (P h ilip p in e s /8 2 0 1 )
28S rRNA + 12S rRNA + 16S rRNA + COI
0 .0 5 s u b s tit u tio n s /s ite
F ig u re 1. Bayesian phylogeny of the Ergalataxinae and rapanine outgroups, based on the four-gene analysis of 28S rRNA , 12S rRNA , 16S rR N A
and cytochrome c oxidase subunit I (GOI) sequences. Posterior probabilities > 50 are shown at the nodes. Generic assignments are based on our
revised classification (Table 1); uncertain assignments are indicated by single quotation marks. Type species of valid genera are indicated in bold.
Locality is shown in parentheses after species name; when more than one sample of a species is from a given location, the last four digits of the
voucher numbers are given (see Supplementary material T able SI). M ajor clades are indicated by letters A —C and subclades by U —Z.
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Trachypollia lugubris (C osta Rica)
io o l Trachypollia lugubris (P an am a)
'Morula'nodulosa (C osta Rica)
—
'Morula'anaxares (M o z a m b iq u e )
r Muricodrupa fenestrata (M o z a m b iq u e )
T Muricodrupa fenestrata (N e w C a le d o n ia )
Tenguella musiva (M alaysia)
Tenguella g ra n u la ta (N e w C a led o n ia )
- Tenguella n. sp . (G uam )
Tenguella ceylonica (M alaysia)
Tenguella marginalba (A ustralia)
'Muricodrupa' fiscella (N e w C a led o n ia )
r 'Morula rumphiusi (Japan)
1—
'Morula' rumphiusi (M alaysia)
'Morula' n. sp . (P h ilip p in e s /8 8 2 8 )
Morula coronata (M o z a m b iq u e )
Morula japonica (Japan)
Morula nodicostata (G uam )
Morula spinosa (J a p a n /0 1 4 8 )
lo o 1 Morula spinosa (J a p a n /0 3 5 1 )
98l
r Morula striata (Japan/YK)
100 Morula striata (J a p a n /0 3 4 6 )
M o ru la uva (G u a m /0 7 7 5 )
Tööjr M orula uva (Japan)
8 4 Morula aspera (E gypt)
82 M o ru la uva (G u a m /0 8 3 1 )
Phrygiom urex sculptilis (V an uatu )
'Orania' bimucronata (M alaysia)
r Usilla avenacea (H aw aii)
Usilla avenacea (Japan)
Lataxiena fim briata (A ustralia)
‘Orania'gaskelli (V an uatu )
‘Orania'serotina (P h ilip p in es)
- Drupella fragum (Japan)
Drupella cornus (N e w C a led o n ia )
Drupella margariticola 'C o n tin e n ta l' (H o n g K ong)
— Drupella margariticola 'O cea n ic' (M o z a m b iq u e )
—
Drupella rugosa (H o n g K ong)
'Ergalatax'contracta (Japan)
M. C L A R E M O N T E T A L .
F ig u r e 2. B ay e sia n p h y lo g e n y o f th e E rg a la ta x in a e , b a se d o n th e tw o -g e n e analysis o f 28S a n d 12S rR N A . R a p a n in e o u tg ro u p s n o t show n.
C o n v e n tio n s as in F ig u re 1.
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2 8 S rRNA + 1 2 S rRNA
0.1 substitutions/site
r Trachypollia lugubris (Costa Rica)
i1 Trachypollia lugubris (Panama)
arula' nodulosa (Costa Rica)
'Morula'anaxares (Mozambique)
r Muricodrupa fenestrata (Mozambique)
L Muricodrupa fenestrata (New Caledonia)
Tenguella ceylonica (Malaysia)
Tenguella marginalba (Australia)
(
Tenguella musiva (Malaysia)
J
<ftrTenguella granulata (New Caledonia)
I ! — Tenguella granulata (Seychelles)
iooI
r Tenguella n. sp. (Vanuatu)
loo1- Tenguella n. sp. (Guam)
i- 'Muricodrupa' fiscella (Australia)
raoi- 'Muricodrupa' fiscella (New Caledonia)
i - 'Morula' rumphiusi (Japan)
1— 'Morula'rumphiusi (Malaysia)
■'Morula'n. sp. (Philippines/8828)
Morula benedicta (Hawaii)
— Morula coronata (Mozambique)
------------- Morula japonica (Japan)
- Morula nodicostata (Guam)
Morula uva (Guam/0831 )
Morula uva (Japan)
Morula aspera (Egypt)
85l Morula uva (Guam/0775)
r Morula spinosa (Vanuatu)
loolr Morula spinosa (Japan/0148)
50 Morula spinosa (Japan/0351)
r Morula zebrina (Moorea)
lôa r Morula striata (Japan/YK)
94 ] Morula striata (Japan/0346)
Morula biconica (Philippines)
'Orania'gaskelli (Vanuatu)
Lataxiena fimbriata (Australia)
'Orania'serotina (Philippines)
'Orania'bimucronata (Malaysia)
j Usilla avenacea (Hawaii)
1001- Usilla avenacea (Japan)
'Morula'parva (Philippines)
'Pascula'darrosensis (Philippines)
__r 'Pascula'submissa (Mozambique/5440)
100 L 'Pascula' submissa (Mozambique/5609)
— ‘Pascula'ochrostoma (Japan)
9*Lr 'Pascula'muricata (Mozambique/0435)
I L'Pascula'muricata (Mozambique/0950)
100 |
p ‘Pascula' ochrostoma (Tahiti)
îooLr 'Pascula'ochrostoma (Guam)
w1- 'Pascula'ochrostoma (Philippines)
j- Cytharomorula vexillum (New Caledonia/8174)
'Oö1— 'Orania'ornamentata (Mozambique)
88]— 'Cytharomorula'c f grayi (New Caledonia/8225)
1— 'r "tharomorula'springsteeni (Philippines)
tharomorula'cr grayi (New Caledonia/8205)
r 'Orania' mixta (Pnilippines/8708)
100Lf 'Orania'mixta (Philippines/8209)
7? 'Orania'mixta (Philippines/8201 )
'Orania' fischeriana (Madagascar)
— Thais'castanea (South Africa)
'Orania rosea' (Philippines)
loo Lr 'Orania' pacifica (Australia)
53 'Orania'pacifica (Philippines)
— Phrygiomurex sculptilis (Vanuatu)
Drupella eburnea (Japan)
Drupella cornus (New Caledonia)
- Drupella fragum (Japan)
Drupella rugosa (Hong Kong)
Drupella margariticola 'Oceanic' (Hong Kong)
- Drupella margariticola 'Continental' (Mozambique)
'Ergalatax'junionae ((JAE)
'Ergalatax'junionae (Kuwait)
69j- 'Ergalatax'contracta i Japan)
C- 'Ergalatax' contracta (Malaysia)
I Cronia amygdala (Australia)
rao1 Cronia aurantiaca (Australia)
Maculotriton serriale (Japan)
Maculotriton serriale (Philippines)
Bedevina birileffi (Japan)
' oinidrupa' infans (Madagascar)
'Spinidrupa' cf infans (Mozambique)
'Spinidrupa'sp. (Mozambique)
Oppomorus nodulifera (Australia/1257)
r Oppomorus funiculata (Japan/0355)
îol; Oppomorus funiculata (Japan/0140)
73L Oppomorus funiculata (Japan/0340)
r Oppomorus purpureocincta (Guam)
lööLr Oppomorus purpureocincta, (Japan)
941 Oppomorus purpureocincta (Malaysia)
M O L E C U L A R PH Y L O G E N Y O F E R G A L A T A X IN A E
58
j Trachypollia lugubris (Costa Rica)
L Trachypollia lugubris (Panama)
r 'Morula' nodulosa (Costa Rica)
ÍL 'Morula' nodulosa (Senegal)
1001
¡- 'Morula'anaxares (M ozam bique)
1001 'Morula'anaxares (Vanuatu)
Muricodrupa fenestrata (M ozam bique)
1 oo1 Muricodrupa fenestrata (N ew Caledonia)
— Tenguella ceylonica (Malaysia)
98
56
— Tenguella marginalba (Australia)
Tenguella m usiva (Malaysia)
r Tenguella n. sp. (Vanuatu)
100
100 Tenguella n. sp. (Guam)
841 i
Tenguella granulata (Seychelles)
9 9 |j Tenguella granulata (M ozam bique)
9 ? Tenguella granulata (N ew Caledonia)
r 'Morula' rum phiusi (Japan)
100 1— 'Morula' rumphiusi (Malaysia)
100
— 'Muricodrupa' fiscella (Philippines)
'Muricodrupa' fiscella (Australia)
100
'Muricodrupa' fiscella (New Caledonia)
_________ r'Morula' n. sp. (Philippines/8828)
100
’Sol 'M orula' n. sp. (Philippines/8827)
— Morula nodicosta (Guam)
________ Morula benedicta (Hawaii)
Morula chrystosoma (UAE)
— Morula coronata (M ozam bique)
67
\
Morula spinosa (Japan/0148)
100
Morula spinosa (Japan/0351 )
L Morula spinosa (Vanuatu)
99
100 r Morula striata (Japan/YK)
Morula striata (Japan/0346)
100 Morula biconica (Philippines)
L Morula zebrina (Moorea)
Morula japonica (Japan)
Morula uva (G uam /0780)
65
Morula aspera (Egypt)
91 Morula uva (M ozam bique)
Morula uva (G uam /0762)
64 Morula uva (G uam /0775)
Morula uva (Japan)
Morula uva (G uam /0821)
Morula uva (Guam /0831 )
B
96
12S rRNA
—
<
m ajor clade C
0.05 su b stitu tion s/site
F ig u re 3. Bayesian phylogeny of the Ergalataxinae, based on single-gene analysis of 12S rRNA. R apanine outgroups not shown. Conventions as in
Figure 1. A. M ajor clades A and B, with subclades U and V. B. M ajor clade C, with subclades W and Z. Note that subclade Z includes ‘Morula?
parva in Figures 1 and 2.
DISCUSSION
re m a in subjective. W h e n m a k in g su ch decisions, we h av e p re ­
served c u rre n t usage (based on m o rp h o lo g ic al d e finitions o f
g e n era ) w h ere possible. W e e m p h asize th a t o u r stu d y provides
o nly a n in itia l fram e w o rk w h ic h sh o u ld be refined a n d tested
b y fu rth e r m o le c u la r a n d m o rp h o lo g ic al analyses a n d conse­
q u e n tly we n a m e n o new g e n e ra a t this stage.
T h e genus Trachypollia is here re p re se n ted b y only one o f its
fo u r c u rre n tly recognized m em b ers, all o f w h ic h o c cu r in the
e aste rn Pacific a n d A tla n tic O c ea n s (E PA ) (Figs 1 - 3 , T a b le 1;
V okes, 1996a; H o u a rt, 1997). F u rth e r species, in c lu d in g the
ty p e, should be in v estig a te d w ith m o le c u la r tec h n iq u es, n o t
o nly to test th e m o n o p h y ly o f th e genus, b u t also to resolve its
p o sitio n w ith in th e E rg a la ta x in a e . I f th e in c lu d e d species
T. lugubris is re p re se n tativ e o f th e genus, it is c le ar th a t the
P hylogenetic relationships and classification o f the ergalataxine
genera
O u r results in d ic a te p o ly p h y ly in n e a rly all th e e rg a la ta x in e
g e n era , as h ith e rto d efin ed b y m o rp h o lo g ic al c h ara cte rs. F o r
exam ple, species prev io u sly assigned to M orula are fo u n d in
eac h o f th e th ree m a jo r clades, w hile species o f Orania are
fo u n d in eac h su b c lad e w ith in m a jo r clad e C. H ere, we use a
m o le c u la r d a ta se t to c o n stru c t a new p h y lo g en e tic classification
th a t reflects e v o lu tio n a ry re la tio n sh ip s r a th e r th a n superficial
sim ilarities in shell m o rp h o lo g y . A p h y lo g en e tic classification
req u ires th a t g e n e ra are clades th a t c o n ta in th e ir d e sig n ated
ty p e species, b u t som e decisions a b o u t n a m in g a n d ra n k in g
25
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100
M. C L A R E M O N T E T A L .
B
S
'Pascula'ochrostom a (Philippines)
F ig u r e 3. Continued
A tla n tic 'M orula’ nodulosa m ust be e x clu d ed front th e genus, in
a g re e m e n t w ith V okes ( 1996a).
W ith in m a jo r clad e A, we p ro p o se th a t th ree o r fo u r g e n e ra
c a n be recognized: Tenguella, Muricodrupa a n d one o r tw o u n d e ­
scrib ed g e n era . S u b c lad e LT (Figs 1—3A) co n ta in s th e type
species o f Tenguella, T. granulata, a n d we therefore assign to
Tenguella all species in su b clad e LT (Figs 1—3A ). Tenguella has
p rev io u sly b e en sy nonyntized w ith Morula (F ujioka, 1985) a n d
its species h a v e n o t p re viously b e e n recognized as a m o rp h o ­
logically d istin ctiv e g ro u p . In c lu d e d in this g ro u p is a n u n id e n ­
tified species (Tenguella n. sp. in Figs 1—3A ); this h a s been
illu stra te d as 'Azumamorula s p f (D h a rn ta , 2005) a n d as 'Morula
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12S rRNA
— 0.05 su b stitu tion s/site
Lataxiena fimbriata (Australia)
W 62 i— 'Orania'gaskelli (Vanuatu)
100
— 'Orania'bim ucronata (Malaysia)
'Orania'serotina (Philippines)
r Usilla avenacea (Hawaii)
57L
100ÖL Usilla avenacea (Japan)
'Morula'parva (Philippines)
Phrygiomurex sculptilis (Vanuatu)
'M orula'echinata (Vanuatu)
Drupella rugosa (Hong Kong)
— Drupella eburnea (Japan)
100 — Drupella cornus (N ew Caledonia)
Drupella margariticola 'Continental' (H ong Kong)
72
— Drupella margariticola 'Oceanic' (M ozam bique)
96
Drupella fragum (Japan)
79
i ‘Ergalatax’junionae (UAE)
'ööl ‘Ergalatax’junionae (Kuwait)
56'
74r 'Ergalatax'contracta (Japan)
99
^ 'Ergalatax'contracta (Malaysia)
Cronia amygdala (Australia)
82
1001 Cronia aurantiaca (Australia)
loo
r Maculotriton serriale (M ozam bique)
i oor Maculotriton serriale (Japan)
53 Maculotriton serriale (Philippines)
Spinidrupa euracantha (M ozam bique)
52
Bedevina birileffi (Japan)
'Spinidrupa' c f infans (M ozam bique)
70
'Spinidrupa'sp. (M ozam bique)
'Spinidrupa'infans (Madagascar)
ngi- Oppomorus purpureocincta (Guam)
Lj Oppomorus purpureocincta (Japan)
85* Oppomorus purpureocincta (Malaysia)
Oppomorus nodulifera (Australia/1257)
89
100 Oppomorus nodulifera (A ustralia/03918.1 )
Oppomorus nodulifera (A ustralia/03918.2)
72
p Oppomorus funiculata (Japan/0140)
100! Oppomorus funiculata (Japan/0355)
Oppomorus funiculata (Japan/0340)
'Pascula' darrosensis (Philippines)
tool
r 'Pascula'subm issa (M ozam biq u e/5440)
z)
lOOL 'Pascula'subm issa (M ozam b iq ue/5609)
loo i— 'Cytharomorula'c f grayii N ew C aled on ia/8225)
H
i— ‘Orania'ornam entata (M ozam bique)
55'
io o L Cytharomorula vexillum (N ew C aled on ia/8174)
98* Cytharomorula vexillum (N ew C aled on ia/8203)
i— 'Cytharomorula' c f grayi (New C aled on ia/8205)
Töo' 'Cytharomorula' springsteeni (Philippines)
r 'Cytharomorula'paucim aculata (Philippines/8202)
56'
Too*- 'Cytharomorula'paucim aculata (Philippines/8204)
r 'Orania'm ixta (Philippines/8708)
0n 'Orania' m ixta (Solom an Islands)
74l ‘Orania’m ixta (Philippines/8209)
'Orania'm ixta (Philippines/8201)
i— ‘Orania' fischeriana (M adagascar)
q
T h a is'castanea (South Africa)
70'
'
'Orania'pacifica (Australia)
75
'Orania'pacifica (Philippines)
97
'Orania rosea' (Philippines)
— 'Pascula'ochrostom a (Japan)
i oor 'Pascula'muricata (M ozam biq u e/0435)
89
89
'Pascula'muricata (M ozam biq u e/0950)
'Pascula'ochrostom a (Tahiti)
'Pascula'ochrostom a (Guam)
M O L E C U L A R PH Y L O G E N Y O F E R G A L A T A X IN A E
S u b c lad e Y (Figs 1—3B) also c o n ta in s m o rp h o lo g ic ally
diverse species. In th e all-gene analysis (Fig. 1), th e type
species o f Oppomorus, O. nodulifera, form s a w e ll-su p p o rte d clade
w ith O . funiculata a n d O. purpureocincta a n d we therefore propose
th a t Oppomorus sh o u ld be a cc o rd ed full g e n eric ra n k (h ith e rto a
su b g en u s o f M orula, e.g. H o u a rt, 2004). O f th e re m a in in g ta x a
in su b c lad e Y, th ree species prev io u sly assigned to Spinidrupa
fo rm a clad e ('S .’ infans, 'S .’ cf. infans a n d 'S .’ sp.), b u t th e ir re ­
la tio n sh ip w ith th e ty p e species, .S’, euracantha, is u nresolved in
th e o nly analysis in w h ic h th e la tte r w as in c lu d e d (Fig. 3B).
F u rth e rm o re , in th e all-gene analysis th e 'Spinidrupa’ clad e also
inclu d es Bedevina birileffi, th e ty p e species o f Bedevina, w h ic h has
p rio rity . P e n d in g th e in clu sio n o f a d d itio n a l species, w e c o n se r­
vativ ely re co m m e n d th e re te n tio n o f b o th Spinidrupa a n d
Bedevina.
S u b c lad e Z (Figs 1—3B) c o n ta in s species o f Pascula, Orania
a n d Cytharomorula, b u t in clu d es th e ty p e species o f o nly th e last
o f these. B ased o n th e in c lu d e d species, all th ree g e n era , as c u r­
re n tly defined, are p o ly p h y le tic . It m ay be th a t th e e n tire
clad e sh o u ld be assigned to one genus. O f these th ree generic
n am es, Orania h a s p rio rity (T a b le 1), b u t its m em b e rs also
a p p e a r in clad e W a n d th e ty p e species w as n o t in clu d e d .
P e n d in g a m ore co m p le te analysis, in c lu d in g th e re le v a n t type
species, we h a v e conserv ativ ely re ta in e d all species in the
g e n e ra to w h ic h th ey h ave b e e n p re viously assigned. Also
in c lu d e d h e re is th e e n ig m a tic S o u th A frica n species 'T h a is’
castanea', clearly, this is n o t a m e m b e r o f th e r a p a n in e genus
Thais, b u t its a p p ro p ria te generic a ssig n m en t re m a in s to be
d e te rm in e d . A te m p o ra ry p la c e m e n t in Orania is suggested. In
th e tw o-gene a n d fou r-g en e analyses (Figs 1 a n d 2), 'M orula’
parva is sister to all o th e r m em b e rs o f su b c lad e Z, suggesting
th a t a new genus m ay be re q u ire d for this species.
F ossil record and age o f the E rgalataxinae
O w in g to sim ila rity a n d c onvergence o f shell form a m o n g e rg a ­
la ta x in e a n d ra p a n in e m u ric id s a n d lack o f u n a m b ig u o u s syna p o m o rp h ie s for m a n y clades (V erm eij & C arlso n , 2000),
u n e q u iv o c a l id e n tific a tio n o f fossils c a n be p ro b lem atic.
V e rm eij & C a rlso n (2000) gave th e earliest occu rren ces o f
several e rg a la ta x in e g e n e ra as L a te M io cen e, w hile L a n d a u ,
H o u a r t & D a Silva (2007) re p o rte d th a t th e g ro u p a p p e a re d
in th e A tla n tic in th e E a rly M io cen e. T h e oldest c e rta in e rg a ­
la ta x in e k n o w n to us is a sp ecim en o f 'Taurasia’ sacyi C o ssm an n
& P eyrot, 1923 from th e E a rly O lig o cen e (G aas, E spibos,
F ra n c e ; R u p e lia n stage, 2 8 .4 -3 3 .9
M a ; C o llectio n o f
R . H o u a rt). T h is fossil resem bles R e c e n t species o f Pascula,
Ergalatax a n d Cytharomorula, im p ly in g a m in im u m age for
m a jo r clad e C. T h is, how ever, is insufficient for a reliab le tim e
c a lib ra tio n o f o u r p h y lo g en y . P a la e o n to lo g ic a l evidence sug­
gests a C re ta ce o u s o rig in for th e M u ric id a e as a w hole
(V erm eij,
1996). Som e recen t m o le c u la r studies h ave
a tte m p te d to estim ate ages o f e rg a la ta x in e clades, g iving
figures o f 5 M a for Drupella (C la re m o n t et al., 2011a) a n d 82
M a for th e se p a ra tio n o f th e E rg a la ta x in a e a n d R a p a n in a e
(C la re m o n t et al., in press). D e ta ile d stu d y o f e rg a la ta x in e
fossils is re q u ire d before these estim ates c a n be refined.
CONCLUSIONS
A lth o u g h this fram e w o rk rep resen ts th e m ost co m p lete p h y l­
o geny o f th e E rg a la ta x in a e y et c o n stru cted , m u c h w o rk rem ain s
to be d o n e to achieve a ro b u st p h y lo g en e tic classification o f this
ta x o n o m ic a lly difficult subfam ily. W e h a v e clarified th e classifi­
c a tio n o f 'M orula’ s. L, d efin in g as d istin c t clades th e g e n e ra
M orula s. s., Tenguella a n d Oppomorus, a n d h av e c o n firm ed the
v a lid ity o f Muricodrupa, Phrygiomurex a n d Drupella. T h e d e fin ­
itio n a n d v a lid ity o f several tra d itio n a l g e n era , in c lu d in g
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mutica’ (W ilson, 1994). T h e shell shows som e sim ilarities to
M . mutica, w h ic h is th e ty p e species o f Azumamorula, a n d it is
th erefore possible th a t this genus m ay pro v e to be a sy nonym
o f Tenguella (T a b le 1). T h e o th e r species in clad e A are m o r­
p h o lo g ic a lly dissim ilar to species o f Tenguella. W e re co m m e n d
th a t Muricodrupa be re ta in e d for its ty p e species, M . fenestrata.
I n th e all-gene analysis (Fig. 1), 'M orula’ anaxares form s a m a r ­
g in ally significant clad e w ith M . fenestrata, w h ic h is n o t c o n tr a ­
d ic te d in o th e r analyses. LTnworn shells o f b o th species show
sim ila r sc u lp tu re a n d , if fu tu re studies co n firm th e ir sister re la ­
tio n sh ip , 'M orula’ anaxares m ay be tran sferre d to Muricodrupa. A
new gen u s is re q u ire d for 'M orula’ nodulosa, th e sole re p re se n ta ­
tive o f clad e A in th e A tla n tic , w ell s u p p o rte d as sister to the
re m a in in g In d o -W e st Pacific (IW P ) m em b e rs (Figs 1—3A ).
T h e p a tte rn o f one or m ore E P A lineages sister to a m ore
diverse IW P clad e is c o m m o n in tro p ic a l g a stro p o d gro u p s
(e.g. W illiam s & R e id , 2004; C la re m o n t et ed., in press).
E leven species th a t are c o m m o n ly assigned to Morula form a
m o n o p h y le tic g ro u p w ith in m a jo r clad e B. Since this includes
M . uva, th e type species o f M orula, we p ro p o se th a t th e generic
n a m e sh o u ld be re stric te d to this su b c lad e (Figs 1 -3 A : su b clad e
V ). T h is clad e also co n ta in s M . biconica, th e ty p e species o f
Habromorula, b u t species p re viously assigned to this g ro u p [as a
su b g en u s o f Morula'. M . ( H .) biconica, M . ( H .) coronata, M . (H .)
japonica, M . ( H .) spinosa, M . ( H .) striata; H o u a rt, 2004] d o n o t
fo rm a clad e in a n y analysis (Figs 1 —3A ). H ow ever, m o n o p h y ly
o f this m o rp h o lo g ic ally d istinctive g ro u p is n o t strongly c o n tra ­
d icte d , so th a t fu rth e r sa m p lin g a n d analysis co u ld yet su p p o rt
Habromorula as a m o n o p h y le tic su b g en u s o f Morula. B ecause
th ey are m o rp h o lo g ic a lly d issim ilar to species o f Morula s. s.,
o th e r species in clad e B ('M orula’ rumphiusi a n d 'M orula’ fiscella)
sh o u ld be assigned to a new genus. T h e p la c e m e n t o f a n u n id e n ­
tified species ('M orula’ n. sp.) is n o t certain .
M a jo r clad e C is th e larg est a n d m ost m o rp h o lo g ic ally
d isp a ra te o f th e e rg a la ta x in e su b g ro u p s a n d o u r sam p lin g
inclu d es th e ty p e species o f 10 d e sc rib e d g e n era . M o st o f these
a re p o o rly d efin ed m o rp h o lo g ic ally a n d som e (Phrygiomurex,
Usilla, Maculotriton, Bedevina) m ay be m o n o ty p ic . T h e affinities
o f Phrygiomurex sculptilis a n d 'M orula’ echinata are n o t resolved.
Species in su b c lad e W (Figs 1—3B) a re m o rp h o lo g ic ally h e t­
erogeneous, in c lu d in g b o th th e sm ooth-shelled Usilla a n d
foliose Lataxiena, to g e th e r w ith som e Orania species. T h e genus
Orania is stro n g ly p o ly p h y le tic in o u r analyses, w ith m em b ers
in subclades W a n d Z (Figs 1 —3B). Since th e ty p e species o f
Orania (O. fusulus from th e M e d ite rra n e a n ; T a b le 1) w as n o t
in c lu d e d , it is im possible to d e te rm in e to w h ic h o f th e th re e to
five clades o f 'Orania’ th e n a m e sh o u ld be a p p lie d . C lea rly a
revision o f th e g enus is necessary. M e a n w h ile , in view o f the
m o rp h o lo g ic al d isp a rity in this g ro u p , we suggest th a t Orania,
Usilla a n d Lataxiena sh o u ld be re ta in e d a c c o rd in g to th e ir
accu sto m e d usage.
W ith in su b c lad e X (Figs 1 —3B) th e genus-level classification
o f Drupella has b e e n in v estig ated in d e ta il elsew here
(C la re m o n t et al., 2 0 1 1 a). T h e genus is w ell su p p o rte d (Figs 1
a n d 2 ), consisting o f D . cornus, D . fragum , D . eburnea, D . rugosa
a n d tw o c ry p tic species o f D . margariticola sensu lato (D . margari­
ticola 'O c e a n ic ' a n d D . margariticola 'C o n tin e n ta l’). O th e r
species in su b clad e X fo rm a w e ll-su p p o rte d clad e in the
all-g en e analysis (Fig. 1), in c lu d in g th e ty p e species o f Cronia
a n d Maculotriton. T h e ty p e species o f Ergalatax, E. pauper, was
n o t sam p led , b u t th e in c lu d e d E. contracta is p ro b a b ly close to
it a n d has b e en co n sid ered synonym ous (H o u a rt, 2008). O f
these th re e g en eric n am es, Cronia h a s p rio rity (T a b le 1).
A lth o u g h Ergalatax is n o t m o n o p h y le tic in a n y analysis
(Figs 1—3B), o u r sa m p lin g o f this gen u s w as lim ited .
T h ere fo re, we co n servatively suggest th a t all th ree g e n e ra are
re ta in e d u n til relatio n sh ip s a m o n g th e m c a n be m ore th o r­
o u g h ly in v estig a te d w ith in cre ased species-level sam p lin g .
M. C L A R E M O N T E T A L .
Orania, Pascula, Cytharomorula, Cronia, Ergalatax, Maculotriton,
Usilla, Lataxiena, Spinidrupa a n d Bedevina re m a in to be co n firm ed
(see su m m a ry in T a b le 1). A t least th ree new g e n e ra (for
'M orula’ nodulosa', for 'A í.’fiscella a n d 'A Í.’ rumphiusi; a n d for 'A Í .’
parva) a p p e a r to be re q u ire d . S everal liv in g g e n e ra th a t h ave
b e en in c lu d e d in E rg a la ta x in a e b y som e a u th o rs w ere n o t a v a il­
a b le for in clu sio n in o u r analyses a n d th e ir p la c e m e n t should
be tested b y m o le c u la r analysis (Azumamorula, Daphnellopsis,
Lindapterys, Uttleya; S u p p le m e n ta ry m ate ria l: T a b le S2).
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H O U A R T , R . 1996a. O n th e id e n tity o f M orula martensi D a li, 1923
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W e are very g ra te fu l for th e assistance a n d loans p ro v id ed by
th e staff o f m useum s a n d resea rc h in stitu tio n s, especially
P. B ouchet, V. Eléros, B. B uge a n d N . P u illa n d re o f M u seu m
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M éxico: J .E .
M ic h e l-M o rfin a n d V. L a n d a -J a im e
of
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C osta R ic a ; S. S la ck -S m ith a n d C. W hisson o f th e W estern
A u s tra lia n M u seu m , P e rth ; M . O liv erio a n d A. B arco o f ‘L a
S a p ie n z a ’ LTniversity o f R o m e; A. K e rr a n d B. S m ith o f th e
LTniversity o f G u a m M a rin e L a b o ra to ry ; G . W illiam s o f th e
Sw ire M a rin e L a b , Elong K o n g ; a n d I. L o ch a n d A. M ille r o f
th e A u s tra lia n M u seu m , Sydney. W e w o u ld also like to th a n k
m a n y o th ers w h o p ro v id ed specim ens or w h o assisted us in th e
field in c lu d in g L. A lsayegh, C. B e n n ett, C. B ird, C. C arlson,
T . P lag a, T . L la m ad a , G . H e rb e rt, Y. Ito , R . Jo n e s, Y. K a n o ,
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T a n , S .H . T a n , J .D . T ru e , R .C . W illan , a n d Z. Y asin. T h e
M N H N m a te ria l used in this stu d y w as collected d u rin g th e
follow ing expeditions: P A N G L A O 2004 M a rin e B iodiversity
P ro je ct [a jo in t p ro je c t b e tw ee n LTniversity o f S a n C arlos,
C eb u C ity (LTSC; c o -P I D a n ilo L arg o ) a n d M N H N (co-P I
P h ilip p e B o u ch et), fu n d e d by th e T o ta l F o u n d a tio n a n d th e
F re n c h M in istry o f F o reig n A ffairs]; th e A L T R O R A 2007 cruise
[M /V D A -B F A R associated w ith th e N a tio n a l M u s e u m o f th e
P h ilip p in e s (N M P , c o -P I M a riv e n e M a n u e l), M N H N (co-P I
P h ilip p e B ouchet) a n d B F A R , fu n d e d th ro u g h a g ra n t from
th e L o u n sb e ry F o u n d a tio n ]; th e M N H N - I R D - P N I S a n to
2006 e x p e d itio n (fu n d e d by g ra n ts from , a m o n g others, th e
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