Table Of Content—
THE NAUTILUS 123(1):9-13, 2009 Page 9
Phylogenetic position of the bivalve family Cyrenoididae
removal from (and further dismantling of) the superfamily
Lncinoidea
John D. Taylor
EmilyA. Glover
Suzanne T. Williams
Department of Zoology
The Natural History Miiseuiir
London, SWT 5BD UNITF,D KINGDOM
[email protected]
[email protected]
s.\[email protected]
ABSTRACT wdth Lucinidae species, wdth no support for separate
lamilial status, and the nominal family w'as syuonymized
A molecularanalysis usingsequences from I8S and 28S rKNA accordingly. Apart from the Lucinidae, the only other
genes of the brackisli and freshwater bivalve Cijrenoida flori- family wdth living species still classified wdthin Luciuoi-
dana, in conjunction wdth a wide range of other heterodont
biwilves, demonstrated a close I'elationship with the families dea is the Cvrenoididae, but lack of suitably presen’ed
Corbiculidae and Glauconomidae and distant from the laici- material has precluded inclusion in molecular analyses.
noidea, wliere the Cyi'enoididae liad been usually classified. From morphological exidence, Williams etah (2004) and
Based on this result it is proposed that the Cyrenoididae be Taylor and Glover (2006) thought a relationship to the
removed from the Lucinoidea, which, for lixing taxa, now Lucinidae unlikely, Cijrenoida havdng medium to long
includes onlytire family Lucinidae. fused siphons, well developed labial palps and ctenidia
wdth two demibrauchs. These statements led Bieler and
Additional Kci/words: Bixalvia, fleterodonta,
Cijrenoida floridana, 18S rKNA, 28S rRNA Alikkelsen (2006) toplaceCyrenoididae as incciiaescdis.
The Cyrenoididae Adams and Adams, 1857 (= Cyre-
nellidae Gray, 1853) comprise a small group of around
ten nominal species of little-studied bixalves inhabiting
brackish to freshwaters, classified into a single genus,
INTRODUCTION Cijrenoida (txq^e species C. diiponfia joannis, 1835)
(Figures 1-3), distributed in western Africa, eastern
Until recently, most classifications of bivalve mollusks and w^esteru Americas and some islands of the Garibbe-
'
included within the snperfamily Lucinoidea several an. The West African species inhabit brackish mangrove
component families (Lucinidae, Fimbriidae, Thyasiri- habitats (Pilsbiy and Bequaert, 1927). In the eastern
dae, Ungulinidae Cyrenoididae, and fossil iVIactrom)-!- USA, Cijrenoida floridana Dali, 1901 (Figures 4-7)
dae) (e.g. Dali, 1901; Chavan, 1969; Boss, 1982, Vaught, ranges from Dehuvare to the coast of the Gulf of
1989; Amler, 1999). The Lucinidae and some Thyasiri- Mexico, maybe as far west as Yucatan (\"okes and Wkes,
dae are notable for the chemosvmbiosis wdth sulphide- 1983), w'here it inhabits fresh and brackish water habi-
oxidizing bacteria housetl in the ctenidia (Southward, tats (Leathern, Kinuer, and Maurer, 1976; Kat, 1982;
1986; Taylor and Glover, 2006). Molecular analyses of Bishop and Hackney, 1987).
tlie Lucinoidea, compared wdth a wdde range of other Dali (1895) was the first to place the Gyrenoididae
heterodont bivalves, demonstrated that superfamily within the Lucinoidea, .stating (p. 545) “These are estua-
was not monophyletic, wdth the Thyasiridae and Uugiili- rine Lucinacea.” Later (Dali, 1901: 817) stated “. . .shells
nidae notcloselyrelatedtothe Lucinidae (Williams, Tay- ol this group with a Luciuoid animal and Diplodonta-
lor, and Glover, 2004; Taylor, Williams, and Glover, 2007; like shell, exhibit a hinge .structure w'hich is w'holly
Taylor et ah, 2007). The Ungulinidae group near families distinct from any other of the Lucinacea.” Many later
such as the Veueridae, Corbiculidae, and Mactridae, classifications, inciudiug the iulluential Treatise ofInver-
while the Thyasiridae form a basal clade within the tebrate Paleontology (Ghavau, 1969), lollow^ed Dali in
Euheterodon—ta and are considered as a distinct placing the Gyrenoididae within the Lucinoidea (e.g.
snperfamily Thyasiroidea. Fimbria fimhriata, one of Yokes, 1980; Boss, 1982, Vaught, 1989, Skelton and Ben-
the two living species of Fimbriidae, nested together ton, 1993; Amler, 1999).
:
Page 10 THE NAUTILUS, Vol. 123, No. 1
Figures 1-7. Ci/reuoida (hipcnitid (1-3) and C. flohdana (4-7). 1. Cijrenoida dnpoiitia Joannis, left valve, Senegal (BMNH
200810.5.5). Scale bar = 10 nun. 2-3. Hinge teeth ol Ci/rcnoida dupontia. right \-alve (2) and left valve (3). Scale bar = 2 nun.
4. Cipvnoida floiidaiui Dali, left valve. Blue Hole, Big Pine Key, Florida (BMNH 200S1054). Scale bar = 2 niin, .5-6. Hinge teeth
(SEM images) ol Ci/rcnoida floridtma, right \alve (.5) and left \'alve (6) (BMNH 20081054). Scale Irar = 500 [.nn. 7. Ciirenoida
lloiidnna. livingspecimen with short, fused sijrhons. Blue Hole, Big Pine Key, Florida. (Photo R. Bieler, September2007).
Nevertheless, dillerent opinions were expressed hy placed along with Lncinoidea in the order Astartida.
other authors, I'ischer (1887: 1096), for exainple, placed Alternatively, and rather hizarrely, Starohogatov (1992)
Cyrenoididae (as Cyrenellidae) into a suborder Concha- placed Cyrenoidoidea within the infraorder Eiycinoinei
cea,near[oCorhicuInandUngnlinidaehutapartfromthe along witli Cyainioidea, Galeonnnatoidea and Leptonoi-
Lncinoidea. W'hile Thiele (1934) included Cyrenoididae tlea, all containedwithintheorderLncinifornies.
with other Iresh and brackish water bivalves in the.s7/rp,s' Clearly, there e.xists ninch uncertainty concerning the
Sphaeriaceahut notpositionedcloselyto laicinoidea.The pliylogenetic position of Cyrenoididae amongst the het-
lainilywaselevatedtosiiperlaniilystatusbyOlsson 1961 erodont bivalves hut this has never been tested hy either
(
227) hut placed near to Lncinoidea, a decision also lol- morphological or molecular analyses. In 2007, we
lowed hy Keen (1971). The snperlaniily Cyrenoidoidea obtained samples of Ci/reiioida floridana suitable for
was also recognized hy Nevesskaya et al. (1971) and molecular analysis and in this paper we present 18S and
D. Taylor et al„ 2009 Page 11
J.
28S rRNA sequences for the species that enable ns to DISCUSSION
establisli the phylogenetic position ol the lainily in rela-
tion to a wade range ol heterodont bivalve taxa previous- It would have been desirable to have included the t\pe
ly analysed (Taylor et ah, 2007) and specilically address species of Cifrenoida. namely, Cifrenoida diipontia [oan-
the question of whether the Lncinidae and Cyrenoidi- nis, 1835, from West Africa, in the molecular analysis
dae form a monophyletic group. but no suitably presei'ved material wais a\’ailable. Al-
though a much smaller species, C. floridana is similar
to C. diipontia in shell characters, notably the unusual
MATERIALS AND AIETHODS hinge dentition, and we feel confident that they are
members of the same group, Cifrenoida dii))onlia has
The sample ol Cifrenoida floriclaiia, presen-ed in 100% three cardinal teeth in the riglit valve, the anterior of
ethanol (BAINH 20081053), wars collected (18 Septem- these is tliin and elongate and tlie central tooth larger
ber 2007) from Bine Hole (24°42.4' N, 81°22.8' W) a and sliglitly bifid (Eigures 2-3) wdiile the left \alve has
freshwater pond on Big Pine Key, Monroe County, Elor- two cardinals, the posterior tooth smaller and bilid and
ida Keys, Elorida, USA, from slioreline mnd up to 0.5 m the anteriortooth elongate. Lateralteeth are absent. The
depth among roots of marginal reeds. Other material dentition of C. floridana is veiw similar (Eigures 4-6)
from the same site is lodged at the Eield Mnsenm ol w'ith three cardinal teeth in the right valve, the central
(EMNH
Natural History 314434; 317667). being larger and two caixlinal teetli in the left wilve watli
DNA
Eor tlie molecular analysis, methods of e.xtrac- the posterior tooth Ihfid and the anterior tooth elongate.
tion, amplification anti sequencingfollowed bysequence We have also e.xamined the gross anatomy of Cifrenoida
analysis and phylogenetic reconstruction are as rosea (d'Aillv, 1896) from Nigeria (National Mnsenm of
described in Taylor et al. (2007). Sequences for Ci/re- Wales specimen NMW.Z.2()03.029.()2()4f and this has
)
noicla florichina were analysed togetherwath the data set ctenidia with hvo demibranchs, with the inner demi-
ofheterodonts listed in Taylor et al. (2007, Table 1), with branch larger, paired triangular labial palps, and ftised
the addition of new 18S and 28S sequences for Mi/a medinm-length posterior siphons. Cifrenoida floridana
arenaria Linnaeus, 1758 (family Myidae) from Gydnia, is similar, wath small outer demibranchs, triangular labial
Poland. The new^setjnences for Cifrenoida floridana anti palps andshort Iusedposteriorsiphons, the inlialantwith
Mija arenaria are lodged in GenBank (Accession nnm- papillae (Eigure 7), Despite the presence of siphons,
bers: C. floridana F’M999789, EAI999790; M. arenaria there is no pallial sinus in any Cifrenoida .species.
EM999791, 779792). Voucher specimens t)l both species The inain conclusion ol this study, basedon our results
are housed in the Department of Zoology, The Natural lor Cifrenoida floridana, is that the Cyreuoididae sliould
History Museum, Lt)udon. be removed h'om the Lucinoidea and classified close to,
Phylogenies were constructetl using Bayesian meth- orpossiblywathin, theCorbiculoidea. The status ol Cifre-
ods (MrBayes v3.1.2, Huelsenbeck and Rompiist, 2001) noida in relation to Corbiculidae and Glauconomidae
using a GTR+G+I mt)tlel. The analysis for each data set needs further analysis witli a larger dataset of corbicnlid
was run for 3,500,000 generations, with a sample fre- species. Eorthepresentthe familycan be classifiedwdth-
tjuency of 100. Each analysis wais run twice. The first in a separate superfamily Cyrenoidoidea as proposetl by
15,000 trees from each run were tliscartletl so that the Olsson (1961). Molecular evidence for a liighlv sup-
final cotisensus tree was based ttn the ettmbination of ported relationship betw^eeu Corbiculidae and (ilauco-
accepted trees from each run (a total of 40,000 trees). nomidae was reported by Taylor et al. (2007) although
Support for nodes w'as determinetl usingpttstei'ior prt)b- the elongate shells with deep pallial sinus ami long
abilities (PP, calculatetl by MrBayes). siphons of Glaneonoine are less similar morphologically
to Cyrenoididae and Corbiculidae. Species of Cyreuoidi-
dae and Corbiculidae occur in botli brackish and Iresh-
RESULTS
water habitats while Glauconomidae live intertidally
The combined tree based on concatenated sequences amongmangroves in emironments ol lluctuatingsalinity.
from 18S rRNA and 28S rRNA genes is showm in Eor living taxa, w^e considerthat tlie superfamily Imci-
Eigure 8. The individual trees based on single genes ai'e uoidea should uow' include only the lamily Lncinidae,
very similar in topolog)' to those published previously wath the families Thyasiridae, Ungnlinidae and Cyreuoi-
(Taylor et ak, 2007). In all analyses Cifrenoida floridana didae excluded. The position ol the entirely fossil
nestsinahighlysupportedcladewath Corbiciilafliiininea families Mactromyadae, llionidae, ami Paracyclidae is
(Corbiculidae)andClaiiconoinevirens (Glauconomidae). unresolved althongh the latter two embrace species with
This clade forms part of a major group of heterodonts Incinid characters.
named Neoheterodontei by Taylor et al. (2007). Cifre-
noida is widely separated from both Thyasiridae and
Lncinidae that appear in the more basal parts of the ACKNOWEE CMENTS
tree. The Ungnlinidae, althongh also a member of the 1)
Neoheterodontei, lorm a separate clade distinct from It is pleasure to tliank Riidiger Bieler and Petra Sienvald
Cifrenoida. for generous hospitality and help iu collection ol
Page 12 THE NAUTILUS, Vol. 123, No. 1
100I NeotngoniaMlaarmgaarnctkiuferTaRmiaGrOgaNnltliDfeArEaMARGARITIFERIDAE OUTGROUPS
IUAnnoopdiocnttoarcuymgnea (JNIONIOAE
Card>taleana CARDITIDAE
As/artesulcataASTARTIDAE CRASSATELLOIDEA
EEuuccrraassssaatteellilaadcounianamnganCRASSATELLIOAE
TOO I' ' Thyastrapolygona
THVASIRIDAE
Mendicula/erruginosa
PoromyailtevisPOROMYIDAE
ANOMALODESMATA
LUCINOIDEA
Lunuhcardiumhemicardium
CAROIIDAE
CARDIOIDEA
NEOHETERODONTEI
Chamaasparsa
Chamasenvpurpurata CHAMOIDEA
CHAMiOAE
Figure 8. Molecular phylogeny of heterodont hivalves including Cijrenoida produced by Bayesian analysis for concatenated
se(jiiences from 18S and 28S rHNA genes. The tree was drawn using members ol the palaeoheterodonts Trigoniidae, Unionidae,
and Margaritileridae as outgroups. Support values are posterior probabilities. Nodes with <50% support have been collapsed.
Positions ofLucinoidea, Thyasiroidea, and Ungulinoidea marked bygreybars. Details oft;ixa in Tayloret al. (2007).
C. finridaua. We are grateful to Pat Dyal for assistance Researchonthis exemplarspecies in the BivalveTree-of-
with molecular analysis and to Graham Oliver (National Lifeproject (www.bivatol.org<http://www.bivatol.org/>)
IVlnsemn ol Wales) for making a specimen of Ctireiwida was supported by the U.S. National Science Foundation
rosea available. We thank Professor Idiil Rainbow and AToL program (DEB-()732854/()7329()3/0732860). The
Department of Zoology, NIIM for continuing support. specimens were collected under U.S. Fi.sh and Wildlife
D. T\iylor et al„ 2009 Page 13
J.
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National KeyDeer Refuge. ford University Press, Stanford, 1064 pp.
Leathaem, P. Kinner, and D. Maurer. 1976. Northern
range extension of the Florida marsh clam Ci/rcnnida
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