strioterebrum plumbeum , common name : the lead-coloured auger , is a species of sea snail , a marine gastropod mollusk in the family terebridae , the auger snails .

strioterebrum plumbeum

strioterebrum sacco , f . , 1891 type species : strioterebrum basteroti nyst , p . - h . , 1843
myurella joserosadoi myurella kilburni myurella nathaliae myurella nebulosa myurella parkinsoni myurella paucistriata myurella torquata myurella undulata myurella wellsilviae oxymeris areolata oxymeris areolatus cf . oxymeris caledonicus oxymeris chlorata oxymeris costelliferus oxymeris crenulatus oxymeris dillwynii oxymeris dimidiatus oxymeris fatuus oxymeris felinus oxymeris gouldi oxymeris maculatus oxymeris senegalensis oxymeris strigatus oxymeris trochlea oxymeris troendlei perirhoe cerithina perirhoe eburnea pristiterebra glauca pristiterebra petiveriana pristiterebra tuberculosa strioterebrum caliginosum strioterebrum japonicum strioterebrum nitidum strioterebrum plumbeum strioterebrum sanjuanensis strioterebrum swainsoni terebra alba terebra amanda terebra argosyia terebra argus terebra argus brachygyra ( f ) terebra argus cf .
clade e is the largest clade and includes the genera myurella , clathroterebra , terenolla , hastulopsis , strioterebrum , and the “terebra” textilis - group ( terryn 2007 ) . myurella itself is polyphyletic , with several species placed as sister groups of other genera . for example , myurella affinis , the type species , is the sister group of terenolla , hastulopsis , some clathroterebra species , and two other myurella species ( pp = 1 , b = 94 ) . clathroterebra is also polyphyletic , with the two representative species used in our analyses , clathroterebra poppei and clathroterebra fortunei , type species of clathroterebra , appearing in separate well - supported clades ( pp = 1 , b = 100 ) for both . the distinctiveness of the monotypic genus terenolla appears to be confirmed in our analysis . hastulopsis and strioterebrum are paraphyletic . the “terebra” textilis - group is dispersed within clade e and constitutes a group that includes a large amount of undescribed diversity , both at the genus and species levels , hence the various types ( textilis iii , iv , v , and vii ) listed in the tree .
( of terebra plumbea quoy & gaimard , 1833 ) quoy j . r . c . & gaimard j . p . ( 1832 - 1835 ) . voyage de découvertes de l '
astrolabe
exécuté par ordre du roi , pendant les années 1826 - 1829 , sous le commandement de m . j . dumont d ' urville . zoologie . paris : tastu . 1 : i - l 1 - 264 ; 2 ( 1 ) : 1 - 321 [ 1832 ] ; 2 ( 2 ) : 321 - 686 [ 1833 ] ; 3 ( 1 ) : 1 - 366 [ 1834 ] ; 3 ( 2 ) : 367 - 954 [ 1835 ] ; atlas ( mollusques ) : pls 1 - 93 [ 1833 ] . , available online at urltoken [ details ]
( of terebra assimilis pease , 1869 ) pease w . h . ( 1869 ) . description of new species of marine gasteropodæ inhabiting polynesia . american journal of conchology . 5 : 64 - 79 . , available online at urltoken page ( s ) : 67 [ details ]
terryn , y . ( 2007 ) . terebridae : a collectors guide . conchbooks & natural art . 59pp + plates . [ details ]
( of hastula plumbea ( quoy & gaimard , 1964 ) ) bratcher t . & cernohorsky w . o . ( 1987 ) . living terebras of the world . a monograph of the recent terebridae of the world . american malacologists , melbourne , florida & burlington , massachusetts . 240pp . [ details ]
( of terebra plumbea quoy & gaimard , 1833 ) bratcher t . & cernohorsky w . o . ( 1987 ) . living terebras of the world . a monograph of the recent terebridae of the world . american malacologists , melbourne , florida & burlington , massachusetts . 240pp . [ details ]
( of terebra plumbea quoy & gaimard , 1833 ) liu j . y . [ ruiyu ] ( ed . ) . ( 2008 ) . checklist of marine biota of china seas . china science press . 1267 pp . ( look up in imis ) [ details ] available for editors [ request ]
( of terebra assimilis pease , 1869 ) bratcher t . & cernohorsky w . o . ( 1987 ) . living terebras of the world . a monograph of the recent terebridae of the world . american malacologists , melbourne , florida & burlington , massachusetts . 240pp . [ details ]
( of terebra bourguignati deshayes , 1859 ) bratcher t . & cernohorsky w . o . ( 1987 ) . living terebras of the world . a monograph of the recent terebridae of the world . american malacologists , melbourne , florida & burlington , massachusetts . 240pp . [ details ]
( of terebra castaneofusca thiele , 1925 ) bratcher t . & cernohorsky w . o . ( 1987 ) . living terebras of the world . a monograph of the recent terebridae of the world . american malacologists , melbourne , florida & burlington , massachusetts . 240pp . [ details ]
( of terebra clappi pilsbry , 1921 ) bratcher t . & cernohorsky w . o . ( 1987 ) . living terebras of the world . a monograph of the recent terebridae of the world . american malacologists , melbourne , florida & burlington , massachusetts . 240pp . [ details ]
( of terebra contigua pease , 1871 ) bratcher t . & cernohorsky w . o . ( 1987 ) . living terebras of the world . a monograph of the recent terebridae of the world . american malacologists , melbourne , florida & burlington , massachusetts . 240pp . [ details ]
( of terebra hoffmeyeri abbott , 1952 ) bratcher t . & cernohorsky w . o . ( 1987 ) . living terebras of the world . a monograph of the recent terebridae of the world . american malacologists , melbourne , florida & burlington , massachusetts . 240pp . [ details ]
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terebra assimilis pease , w . h . , 1871 ( preoccupied , renamed )
terebra clappi pilsbry , h . a . , 1921 ,
1920
: hawaii
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terebridae terebridae are not variable in shape : they are all slender and pointed . the variability in sculpture and pattern is impressive . their determination is a challenge and we are fortunate with the existence of the work of bratcher and cernohorsky ( 1987 ) . there are about 350 species .
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hastula imitatrix hastula knockeri hastula lanceata hastula lepida hastula matheroniana hastula penicillata hastula philippiana hastula rufopunctata hastula solida hastula species indonesia ( from ) hastula species thailand ( from ) hastula strigilata hastula strigilata nipponensis ( f ) hastula strigilata verreauxi ( f ) hastula strigillata cf . hastulopsis alveolata hastulopsis amoena hastulopsis burchi hastulopsis conspersa hastulopsis conspersa cf . hastulopsis loisae hastulopsis pertusa hastulopsis pseudopertusa impages aciculina impages anomala impages bacillus impages cinerea impages cinerea luctuosa impages escondida impages hectica impages inconstans impages marqueti impages maryleeae impages nassoides impages salleana impages stylata myurella affinis myurella affinis peasii ( f ) myurella affinis cf . myurella columellaris myurella flavofasciata myurella hiscocki
the basic data of this taxon were not entered consulting the original description , but from secondary sources .
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pilsbry , h . a . 1921 ,
marine mollusks of hawaii viii - xiii
, proceedings of the academy of natural sciences , philadelphia , vol . 72 , pp . 296 - 328
pease , w . h . 1871 ,
notes on the synonymy and distribution of marine gastropoda
, american journal of conchology , vol . 7 , pp . 20 - 25
deshayes , g . p . 1859 ,
a general review of the genus terebra and a description of new species
, proceedings of the zoological society of london , vol . 27 , pp . 270 - 321
abbott , r . t . 1952 ,
a new terebra ( hoffmeyeri ) from the philippines
, nautilus , vol . 65 , no . 3 , pp . 77 - 80 , pl . 5
thiele , j . 1925 ,
gastropoda der deutschen tiefsee - expedition . theil 2
, wissenschaftliche ergebnisse der deutschen tiefsee - expedition auf dem dampfer
valdivia
1898–1899 , vol . 17 , no . 2 , pp . 35 - 382 , pls 313 - 346
urn : lsid : biodiversity . org . au : afd . taxon : 58186065 - d13c - 444a - 90d9 - 8e10795e4bb2
urn : lsid : biodiversity . org . au : afd . name : 512226
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terebra bruguière , j . g . , 1789 type species : terebra subulata linnaeus , c . , 1758
terebra ( amanda - group ) type species : terebra ( amanda - group ) amanda hinds , r . b . , 1844
terebra ( panamensis - group ) type species : terebra ( panamensis - group ) panamensis dall , w . h . , 1908
terebra ( picta - group ) type species : terebra ( picta - group ) picta hinds , r . b . , 1844
terebra ( textilis - group ) type species : terebra ( textilis - group ) textilis hinds , r . b . , 1844
terebra ( textilis - group ) textilis roseata ( var . ) ( 4 )
terebra ( variegata - group ) type species : terebra ( variegata - group ) variegata gray , j . e . , 1834
terebra ( variegata - group ) specillata balaenorum ( var . ) ( 1 )
terebra ( bathyrhaphe - group ) type species : granuliterebra bathyrhaphe smith , e . a . , 1875
terebra ( bathyrhaphe - group ) bridgesi dushaneae ( var . ) ( 4 )
terebra ( alba - group ) type species : terebra ( alba - group ) alba gray , j . e . , 1834
terebra ( elata - group ) type species : terebra ( elata - group ) elata hinds , r . b . , 1844
terebra ( elata - group ) elata montijoensis ( var . ) ( 2 )
cinguloterebra oyama , k . , 1961 type species : terebra hedleyana pilsbry , h . a . , 1905
clathroterebra oyama , k . , 1961 type species : clathroterebra fortunei deshayes , g . p . , 1857
duplicaria dall , w . h . , 1908 type species : duplicaria duplicata linnaeus , c . , 1758
euterebra cotton , b . c . & f . k . godfrey , 1932 type species : euterebra tristis tristis deshayes , g . p . , 1859
granuliterebra oyama , k . , 1961 type species : granuliterebra bathyrhaphe smith , e . a . , 1875
hastula adams , h . g . & a . adams , 1853 type species : hastula strigilata linnaeus , c . , 1758
hastulopsis oyama , k . , 1961 type species : hastulopsis melanacme smith , e . a . , 1873
impages smith , e . a . , 1873 type species : terebra caerulescens lamarck , j . b . p . a . de , 1822
myurella hinds , r . b . , 1844 type species : myurella affinis gray , j . e . , 1834
oxymeris dall , w . h . , 1903 type species : oxymeris maculatus linnaeus , c . , 1758
pellifronia terryn , y . & m . holford , 2008 type species : pellifronia jungi lai , k . y . , 2001
perirhoe dall , w . h . , 1908 type species : perirhoe circumcincta deshayes , g . p . , 1857
pristiterebra taki , i . & k . oyama , 1954 type species : terebra tsuboiana yokoyama , m . , 1922
triplostephanus dall , w . h . , 1908 type species : triplostephanus triseriatus gray , j . e . , 1834
terenolla iredale , t . , 1929 type species : terenolla pygmaea hinds , r . b . , 1844
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hastula is a genus of sea snails , marine gastropod mollusks in the family terebridae , the auger snails .
species in this genus can be found in the indo - pacific region , australia and tasmania .
these are sand - dwelling snails that burrow into the sand no deeper than their length . these are carnivorous snails , feeding on polychaete worms .
the shell is smooth and glossy . it is very high and turreted with impressed sutures . the shell shows axial sculpturing of crenulations below the slender ribs . there is often no spiral sculpture ; some species show very weak spiral lines .
hastula apicitincta ( sowerby iii , 1900 ) : synonym of impages apicitincta ( g . b . sowerby iii , 1900 )
hastula diversa ( e . a . smith , 1901 ) : synonym of hastula rufopunctata ( e . a . smith , 1877 )
hastula maryleeae r . d . burch , 1965 : synonym of impages maryleeae ( r . d . burch , 1965 )
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1 department of biology and biotechnology “c . darwin” , sapienza university of rome , roma , italy ,
competing interests : the authors confirm that co - author mandë holford is a plos one editorial board member . this does not alter the authors’ adherence to plos one editorial policies and criteria . the authors also confirm that co - author yu zhang is employed by ernst & young ( 5 time square , new york , ny , ny 10036 , ny 10036 , usa ) . this does not alter the authors’ adherence to plos one policies on sharing data and materials .
conceived and designed the experiments : mvm np . performed the experiments : mvm np mc . analyzed the data : mvm np mc yz . contributed reagents / materials / analysis tools : mh . wrote the paper : mvm np mc mh yz . conducted fieldwork to collected specimens : mvm mh mc np .
this is an open - access article distributed under the terms of the creative commons attribution license , which permits unrestricted use , distribution , and reproduction in any medium , provided the original author and source are properly credited .
. in order to validate the abgd / klee approach with another group , a similar analysis has been carried out here on the terebridae . the terebridae was chosen as it is a well - characterized family of conoidea that includes ∼350 described species , with an estimated total number of 450 extant species ( worms–
, which constitutes an exception for the conoideans , making terebrids a good model to test the ability of the abgd / klee approach to accurately delimit pshs .
species delimitation is shown as a function of time and robustness . abgd / klee allows for a fast and relatively accurate first assessment of species diversity . a sampling of biodiverse taxa is first analyzed by bioinformatics species delimitation tool abgd ( automated barcode gap discovery ) using the coi gene and visualized by klee diagrams generated from indicator vectors of coi allowing primary species hypotheses ( pshs ) to be made . further analyses using integrative taxonomy in which additional characters ( genes , morphology , geography ) and criteria ( similarity , phylogeny ) will generate secondary species hypotheses ( sshs ) , but this involves a significant increase in time to produce a definitive robust species hypothesis ( rsh ) .
the three predatory marine mollusk groups of conoidea are illustrated with representative shells . conidae ( cone snails ) in red , terebridae ( auger snails ) in green , and the 14 remaining families , referred to as turrids , in yellow . the inner dark colors refer to known diversity and the outer light colors refer to estimated diversity .
collection permits were provided by the smithsonian tropical research institute permit office ( stri - spo ) and the panama aquatic resources authority ( arap ) for east pacific localities and by the muséum national d’histoire naturelle , paris for all the other localities . specific locations of collection sites are recorded in table s1 . our study did not involve endangered or protected species .
) and stored in the malacology collection of the muséum national d’histoire naturelle ( paris , france ) .
dna sequences were aligned with muscle 3 . 8 . 31 [ 34 ] and accuracy of the alignment was confirmed by eye .
a total of 454 specimens of terebridae were sequenced for a 658 - bp fragment of the coi gene , while a portion of the 28s rdna ranging from 696 to 742 bp was sequenced in a subset of 195 specimens and used to build a 758 - bp alignment ( data s1 and s2 ) . the coi alignment was analyzed with abgd to propose partitions with variable numbers of pshs , depending on the prior threshold and initial or recursive analyses . the more inclusive ( lumper ) partition provided by abgd included 98 clusters , and the least inclusive ( splitter ) partition contained 125 clusters . based on the coi gene only , gmyc and ptp analyses contained a variable number of clusters , mostly overlapping with abgd : 110 in the gmyc single threshold , 130 in the gmyc multiple threshold and 112 in the ptp ( fig . s1 – s3 ) . sixty - three pshs are found identical in the five partitions . if the partitions obtained with the gmyc multiple threshold method are excluded , the number of identical pshs raises to 83 .
and 17 were assigned only to a genus name ( designated by “sp . ” ) (
klee diagram for the coi gene showing the correlation amongst indicator vectors for the less inclusive ( splitter ) dataset obtained with the abgd method and including 125 pshs . color gradation in red indicates high correlation values . arrows indicate the conflicting pshs between the more inclusive and the less inclusive partitions discussed in the text and listed in table s1 .
additionally , ten pshs defined in the lumper partition were split in several psh in the splitter partitions . incongruence between the lumper and splitter abgd partitions can be easily visualized and evaluated when sequence data corresponding to the splitter partition are transformed in indicator vectors and used to build a klee diagram with the indicator vector method
phylogenies for the pshs groups in the splitter partition vs . the lumper partition (
gene sequences were paraphyletic between members of each splitter psh . on the basis of these results 13a–b , 24a–d , 71a–c , 81a–c and 98a–c pshs were rejected and not considered candidate species . however , three groups of pshs from the same partition as those rejected , 3a–d , 12a–b , 30a–b , were clearly recognized in the klee diagram (
phylogeny , with support values comparable or only slightly lower than the lumper partition . additionally , results obtained from the gmyc and ptp are congruent and support the splitting of partitions . for 3a–d , 12a–b , 30a–b psh groups , 28s gene results either confirmed the monophyly of the group ( e . g . for 30a–b ) or were inconclusive . these results substantially reflect a geographical differentiation . specifically ,
with psh 30a from vanuatu and 30b from east africa . as a result , 3a–d , 12a–b , 30a–b pshs , referring to
bayesian phylogenetic tree estimated with the coi gene alignment . clades including several specimens identified as a single morphospecies are compressed in triangles . green circles indicate pp = 100 ; blue upward triangles indicate pp > 80 ; black downward triangles indicate pp > 50 .
sp . 3 ( psh 33 ) . pshs 16 and 33 were split respectively in three ( pshs 16a–c ) and ten ( pshs 33a–j ) partitions in the abgd splitter analysis . inspection of the klee diagram for psh 16 and 33 clearly shows that correlation values of indicator vectors are lower than 90 % only between two clusters internal to each psh (
) . this result , although not congruent with abgd analyses , is supported by gmyc analyses and , in case of psh 33 , by ptp analysis as well . pshs 16a–b and 16c and 33a and 33b–j were thus accepted as candidate species .
in summary a partition of 104 primary species hypotheses are proposed that are congruent based on different characters ( coi , 28s ) , criteria ( similarity , phylogeny ) and species delimitation methods ( abgd / klee , gmyc , ptp ) .
in other instances , the identification of two or more pshs in single morphospecies of our sample correlated with a disjunct geographic distribution , e . g . in
) . for these putative allopatric species pairs , a more complete integrative approach taking into account evidence such as dispersal abilities is needed to rule out the possibility that genetic differentiation is due to an intraspecific geographic structure for psh pairs . in disjoint populations , reduced dispersal abilities are generally linked to higher levels of interpopulation genetic divergence
. in marine environment , dispersal ability of benthic organisms is frequently influenced by the duration of their larval stage . this can be extremely variable , even in closely related species , ranging from remarkably long ( species with teleplanic planktotrophic larvae ) , to short ( species with lecitotrophic pelagic larvae ) , or even absent ( species with intracapsular development or brooding )
remarkably , there are no cases in which two morphological distinct species are joined in a single psh using abgd / klee approach , suggesting that the use of morphological characters in terebridae is not likely to lead to alpha errors in biodiversity estimate ( e . g . overestimation of the number of species ) , due to a general lack of informativeness of shell characters .
list of terebridae specimens analyzed . table indicates morphospecies identification and collection data , together with psh assignment ( abgd lumper and splitter partitions , gmyc single and multiple thresholds and ptp ) , statistical support ( bootstraps and posterior probabilities ) for both coi and 28s loci for each defined psh and klee results .
all material analyzed are from various expeditions organized in collaboration with the smithsonian tropical research institute , muséum national d’histoire naturelle ( mnhn ) , the institut de recherché pour le développement ( ird ) and pro - natura international ( see castelin et al . [ 32 ] for details ) . the authors acknowledge support from p . bouchet , b . buge , j . brisset and j . utge for access to , processing , and curation of the specimens used in this study . m . oliverio is acknowledged for discussion on larval development and microevolution . the phylogenetic analyses were partly performed on the cipres science gateway ( urltoken ) .
funding for this work was provided by nsf ( grant 1247550 ) and the alfred p . sloan foundation ( grant b2010 - 37 ) grants to m . h . this work was also supported by the “consortium national de recherche en génomique” and the “service de systématique moléculaire” ( ums 2700b cnrs - mnhn ) as part of agreement 2005 / 67 between genoscope and mnhn for the project “macrophylogeny of life” directed by g . lecointre . the funders had no role in study design , data collection and analysis , decision to publish or preparation of the manuscript .
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schematic representation of miller ' s foregut anatomy of the terebridae . the three types of foregut anatomy miller used to define feeding strategies within the terebridae are depicted ( types i , ii , and iii ) . anatomical features are labeled and highlighted in color : yellow = salivary glands ( sg ) , red = buccal tube ( bt ) , green = venom bulb ( vb ) and radular sac ( rs ) , and blue = accessory feeding organ ( afo ) . also labeled are the proboscis ( p ) , found only in type ii terebrids , and the labial tube ( lt ) ( after miller 1970 ) .
similar to the majority of shelled mollusks , the taxonomy of the terebridae is not very well characterized ; their taxonomy is primarily based on shell morphology ( oyama 1961 ; bratcher and cernohorsky 1987 ; terryn 2007 ) and relatively few studies describe their anatomy ( rudman 1969 ; miller 1971 ; taylor 1990 ; taylor et al . 1993 ) . this is surprising , given the relative abundance of terebrids and their global tropical distribution and shallow water occurrence . the last classification ( bouchet and rocroi 2005 ) of the gastropoda recognizes two subfamilies , terebridae and pervicaciinae , within the family terebridae , which comprises > 300 known species ( bratcher and cernohorsky 1987 ; terryn 2007 ) and may be another 100 unnamed taxa , especially in deeper waters ( 100–500 m ) .
we used a three - gene data matrix consisting of mitochondrial 12s and 16s rrna and cytochrome oxidase subunit i ( coi ) sequences from 67 species to reconstruct the first molecular phylogeny of the terebridae ( fig . 2 ) . we also assessed the evolution of terebrid feeding strategies by mapping the presence or absence of the venom apparatus on the phylogeny . the results presented here suggest a new hypothesis for understanding terebrid evolution : our findings indicate that the terebridae have independently lost the venom apparatus twice during their evolution .
combined phylogenetic tree . consensus tree of ml analysis and ba using coi , 16s , and 12s data sets . pp and b are specified for each node . miller types , ia , ib , iia , iib , and iii , as described in the text are highlighted in the tree . molecular analyses divide the terebridae into five distinct clades , clades a–e , indicated by the shaded gray areas . representative shells , numbered 1–13 , are shown for each clade . for clarity , multiple samples of the same species are shown only when there is a geographic difference , for example , 30370 and 30389 acus maculatus from panglao 2004 and santo 2006 expeditions , respectively .
ba consisted of six markov chains ( 10 , 000 , 000 generations each with a sampling frequency of one tree each hundred generations ) run in two parallel analyses using mrbayes ( huelsenbeck et al . 2001 ) . the number of swaps that are tried each time the chain stops for swapping was four , and the chain temperature was set at 0 . 08 . when the log - likelihood scores were found to stabilize , a consensus tree was calculated after omitting the first 0 . 25 % of trees as burn - in .
for the combined analyses of the three genes , the same parameters were used for the ml analysis . for the ba , one different model was applied for each gene , each with six substitution categories . for the coi gene , as saturation was found on the third base of the codon , different models were applied for the two partitions ( bases 1 and 2 vs . base 3 ) . finally , we have four unlinked partitions ( coi bases 1 and 2 , coi base 3 , 12s , and 16s ) .
data from cited literature and personal communications from a . sysoev and j . taylor helped to determine the presence or absence of a venom apparatus in the species used for the phylogenetic analysis . the absence or presence of the venom apparatus was then mapped on the tree using mesquite v . 2 . 01 ( maddison w and maddison dr 2007 ) , using the option “tracing character history . ” the parsimony ancestral reconstruction method was used .
one hundred and fifty six samples of terebrids were used to reconstruct the molecular phylogeny of the terebridae . for the coi gene , 658 bp were sequenced . after alignments , we obtained a fragment of 534 and 455 bp for 12s and 16s genes , respectively . trees obtained independently with coi , 12s , and 16s genes were only partly resolved , but no contradictions were found ( results not showed ) . consequently , 12s , 16s , and coi mitochondrial genes , including 131 taxa in the ingroup , were used to produce a combined data set for phylogenetic analyses ( fig . 2 ) .
phylogenetic analyses strongly indicate that the terebridae is monophyletic ( posterior probabilities [ pp ] = 1 , bootstraps [ b ] = 100 ) ( fig . 2 ) . terebra s . l . “ terebra ” jungi appears to be the sister group to all other terebrids ( pp = 1 , b = 92 ) . apart from “ t . ” jungi ( clade a ) , there are four major clades within the tree , designated in figure 2 as clades b–e . clade b is comprised primarily of the genus acus plus one species currently placed in terebra , terebra areolata , which because of its placement in our tree , we tentatively define as acus areolatus ( pp = 1 , b = 100 ) . clade c includes cinguloterebra and additional species currently placed in terebra , including the type species of terebra , terebra subulata ( pp = 1 , b = 76 ) . clade d includes species currently placed in the genera hastula and impages ( pp = 1 , b = 100 ) .
in order to efficiently characterize toxins from various terebrid species , it is essential to first identify those species that have a venom apparatus . shown in figure 3 is the mapping of the presence or absence of a venom apparatus in the terebrid species used to construct the molecular phylogeny in figure 2 . the map clearly indicates that terebrids have lost the venom apparatus twice during their evolution , see clades b and e . “ t . ” jungi , and the members of clades c and d , use the typical toxoglossate venom apparatus to hunt prey .
possession of venom apparatus mapped onto terebrid phylogeny . the presence or absence of a venom apparatus was mapped onto the molecular phylogeny of the terebridae shown in figure 1 . terebrid species with a venom apparatus are indicated by a white box ( □ ) , whereas terebrid species without a venom apparatus are indicated by a black box ( ▪ ) . the map indicates that terebrids have independently lost the venom apparatus twice during their evolution .
evolutionary trends in the toxoglossa have been reconstructed primarily through studies involving radular formation and anatomy of the digestive system ( mills 1979 ; shimek and kohn 1981 ; kantor and sysoev 1989 ; taylor 1990 ; simone 1999 ; kantor and taylor 2000 ) . the molecular phylogeny presented here paints a plausible picture of how terebrids evolved such a diversity of feeding strategies . our findings suggest that all terebrids appear to be derived from a common ancestor with a venom apparatus of the miller type iib ( fig . 3 ) . furthermore , mapping of the venom apparatus indicates that two lineages of terebrids independently lost their ability to hunt prey using toxins , clades b and e .
there is a considerable correlation between our molecular phylogeny , miller ' s anatomical groupings , and the ecological distribution of the terebrid species used in this study . miller separated terebrids with a venom apparatus , type ii feeders , into two distinct groups , iia and iib . type iia and iib terebrids differ in the shape of the buccal tube and shell morphology ( miller 1970 ) . type iia terebrids have a long and slender buccal tube and small shiny shells , with 7–10 whorls and a flared aperture . terebrids of type iib have a short , thick buccal tube , and the shells are large , long , and slender , with 15 or more whorls and a constricted aperture . our phylogenetic analysis supports this separation . the species in clade c , terebra , have slender and multiwhorled shells , whereas those of clade d , hastula , are shiny with fewer whorls . the separation of the two clades is further supported by the ecological differences in their habitats . terebra species of clade c live buried in sandy or muddy subtidal flats , whereas hastula species of clade d live predominantly on surf beaches or in sand in reef pockets ( miller 1970 , 1979 ) . similarly , terebrids that feed without the use of a venom apparatus , types i and iii feeders , are represented by two different clades in the molecular phylogeny , clades b and e , respectively . our analysis clarifies that the two clades without venom apparatus , clades b and e , are not sister groups .
the terebridae phylogeny in figure 2 sets the stage for efficient characterization of terebrid toxins and identification of the gene superfamilies that encode their toxins using the biodiversity first , exogenomic strategy recently applied to cone snails ( olivera 2006 ; olivera and teichert 2007 ) . the exogenomic strategy was used to characterize cone snail toxins that target nicotinic receptors . in this strategy , phylogeny and molecular biology techniques are used to identify “exogenes , ” genes of the toxins expressed in the venom duct . exogenes rapidly evolve to respond to cues in their biotic environment and are thus a powerful marker for differentiating ecological or evolutionarily distinct organisms .
clades c and d are the two major terebrid groups most suitable to investigate toxins for biochemical characterization ( fig . 4 ) . furthermore , as clades c and d are not sister clades , they may produce divergent toxins that could result in varied functional activity upon further characterization .
terebrids with venom apparatus : representative shell images of the terebrid species in clades c and d that have a venom apparatus . the species from left to right are clade c : terebra subulata , terebra guttata , cinguloterebra jenningsi , cinguloterebra anilis , terebra babylonia , terebra laevigata and clade d : hastula strigilata , hastula solida , and hastula hectica .
the biochemical and genetic characterization of terebrid toxins , while identifying novel compounds useful for investigating cell communication in the nervous system , will also provide additional characters to further clarify the phylogeny and evolutionary biology of these organisms . for toxoglossate gastropods , the dual analysis of molecular phylogeny and venom function is an instructive combination for unraveling the bigger question of evolutionary diversification . this work is a first attempt to address these issues for the terebridae .
the authors thank yuri kantor for processing many of the terebrid specimens in the field , virginie heros and philippe maestrati for assistance throughout from the field to curating samples at mnhn , the staff of mnhn ' s “service de systématique moléculaire” for technical facilities , and john taylor and alexander sysoev for providing unpublished anatomical information on terebrid taxa used in this study . the panglao 2004 and santo 2006 expeditions , which were the source of many specimens , were supported among others by the total foundation . joint funding from national science foundation chemistry division and office of international science and engineering postdoctoral fellowship ( 0610202 ) for m . h . also supported this work .
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most populous animal groups that use venom to capture their prey . these marine animals are generally characterized by
a venom apparatus that consists of a muscular venom bulb and a tubular venom gland . the toxoglossan radula , often
but very little is known about toxins from the other toxoglossa , and the phylogeny of these families is largely in doubt .
apparatus for this group . our ﬁndings indicate that most of the genera of terebrids are polyphyletic , and one species
) is the sister group to all other terebrids . molecular analyses combined with mapping of venom
apparatus morphology indicate that the terebridae have lost the venom apparatus at least twice during their evolution .
all other terebrid species do not . for venomous organisms , the dual analysis of molecular phylogeny and toxin function
an instructive combination for unraveling the larger questions of phylogeny and speciation . the results presented here
( taylor et al . 1993 ; puillandre et al . 2008 ) . a venom appa -
1969 ; miller 1971 ; taylor 1990 ; taylor et al . 1993 ) . this
this is an open access article distributed under the terms of the creative commons attribution non - commercial license ( http : / / creativecommons . or
volume of water , for 1 or 2 h . a piece of tissue ( usual
foot ) was cut and ﬁxed in 95 % ethanol . table 2 lists all ter -
and turridae ( s . l . ) were chosen as closely related outgroups ,
. 1 . —schematic representation of miller’s foregut anatomy of the terebridae . the three types of foregut anatomy miller used to deﬁne feeding
strategies within the terebridae are depicted ( types i , ii , and iii ) . anatomical features are labeled and highlighted in color : yellow
accessory feeding organ ( afo ) . also labeled are the proboscis ( p ) ,
found only in type ii terebrids , and the labial tube ( lt ) ( after miller 1970 ) .
. 2 . —combined phylogenetic tree . consensus tree of ml analysis and ba using coi , 16s , and 12s data sets . pp and b are speciﬁed for each
node . miller types , ia , ib , iia , iib , and iii , as described in the text are highlighted in the tree . molecular analyses divide the terebridae into ﬁve
distinct clades , clades a–e , indicated by the shaded gray areas . representative shells , numbered 1–13 , are shown for each clade .
dae . for the coi gene , 658 bp were sequenced . after align -
. 3 . —possession of venom apparatus mapped onto terebrid phylogeny . the presence or absence of a venom apparatus was mapped onto the
molecular phylogeny of the terebridae shown in ﬁgure 1 . terebrid species with a venom apparatus are indicated by a white box (
. 4 . —terebrids with venom apparatus : representative shell images of the terebrid species in clades c and d that have a venom apparatus . the
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taxonomy . new york : springer - verlag . h57 . p . 329–355 .
. . . besides conus , a subset of the closely related family terebridae ( terebrids ) also possesses a specialized radula , used as a spear or harpoon to deliver potent neurotoxins . these ~ 300 known species fall into three feeding types [ 18 ] : type i species have salivary glands , an eversible labile tube , short buccal tube , and lack venom apparatus ; type ii species , the most similar to conus , have true venom glands and a delivery apparatus in the form of a specialized radula ; and type iii lack a venom apparatus , but have an accessory proboscis that other terebrids lack [ 11 , 19 ] . several type ii species have a venom that exhibits similarities to conopeptides . . . .
. . . in this symposium , gorson and holford ( 2016 ) provide a perspective on the ways in which venom differs among gastropods of the family terebridae . specifically , the close relationship between these snails and the better - characterized cone snails ( holford et al . 2009 ) allows these comparisons to be extended in phylogenetic and ecological space . phylogenetic and ecological perspective can enhance prospecting for pharmacologically interesting proteins , and may be critical in identifying novel venom genes through comparative analysis ( fry 2005 ; moran et al . 2008 ; whittington et al . 2010 ) . . . .
. . . conoideans subdue their prey using a venom apparatus made up of a proboscis , radular tooth , a radular sac , venom gland , and venom bulb ( fig . 3 ( a ) ; taylor 1990 ; kantor et al . 2000 ; modica and holford 2010 ; kantor and puillandre 2012 ) . cone snails ( conus ) are the most studied in the conoidea ( puillandre et al . 2014 ; puillandre et al . 2015 ) ; however , conus comprises only 5 % of the biodiverse group of venomous marine snails ( olivera et al . 1999 ; holford et al . 2009 ; king 2015 ) . other non - conus conoideans , such as the turridae ( s . l . ) family , which has more recently been divided into seven family groups ( tucker and tenorio 2009 ; bouchet et al . 2011 ) , and the terebridae family , also produce venom ( heralde et al . 2008 ; aguilar et al . 2009 ; gonzales and saloma 2014 ; gorson et al . 2015 ; moon et al . 2016 ) . . . .
. . . thus , the advantages of molecular phylogenetics , which allows for the comparison of thousands of homologous characters across species , are of particular interest among the terebridae . the first molecular phylogeny of the terebridae was constructed based on analyses of a three‐ gene matrix ( 12s , 16s , and coi ) to define terebridae lineages and their evolutionary history [ 52 ] . this initial terebridae phylogeny confirmed the monophyly of the group and defined five distinct lineages : acus ( clade b ) , terebra ( clade c ) , hastula ( clade d ) , myurella ( clade e ) , and a previously unidentified fifth sister clade that includes pellifronia jungi ( clade a ) [ 52 ] . . . .
. . . the first molecular phylogeny of the terebridae was constructed based on analyses of a three‐ gene matrix ( 12s , 16s , and coi ) to define terebridae lineages and their evolutionary history [ 52 ] . this initial terebridae phylogeny confirmed the monophyly of the group and defined five distinct lineages : acus ( clade b ) , terebra ( clade c ) , hastula ( clade d ) , myurella ( clade e ) , and a previously unidentified fifth sister clade that includes pellifronia jungi ( clade a ) [ 52 ] . subsequent molecular phylogenetic analysis , including additional taxa from the eastern and western pacific further resolved the terebrid evolutionary relationships , synonymizing acus clade b to oxymeris , recovering a previously unidentified clade f that includes the euterebra and duplicara genera , and subdividing the large myurella clade e into five lineages ( clades e1–5 ) [ 48 ] ( figure 2 ) . . . .
. . . thus , the advantages of molecular phylogenetics , which allows for the comparison of thousands of homologous characters across species , are of particular interest among the terebridae . the first molecular phylogeny of the terebridae was constructed based on analyses of a three - gene matrix ( 12s , 16s , and coi ) to define terebridae lineages and their evolutionary history [ 52 ] . this initial terebridae phylogeny confirmed the monophyly of the group and defined five distinct lineages : acus ( clade b ) , terebra ( clade c ) , hastula ( clade d ) , myurella ( clade e ) , and a previously unidentified fifth sister clade that includes pellifronia jungi ( clade a ) [ 52 ] . . . .
. . . auger snails ( 350–400 described species ) form a clade in the phylogeny of puillandre et al . [ 254 ] which is the sister group to a clade turridae sensu stricto that contains the genus turris . a remarkable aspect of the evolution of terebrids—and in striking contrast to cone snails—is the frequent loss of the venom apparatus261 262 263264 . similarly , hypodermic radular teeth have evolved at least three times in terebrids , and independently of those in cone snails [ 264 ] . . . .
. . . the terebridae was chosen as it is a well - characterized family of conoidea that includes , 350 described species , with an estimated total number of 450 extant species ( worms–www . marinespecies . org ) . recent molecular surveys indicate that most terebrid morphologically defined species are generally congruent with dna - based clusters [ 33 ] , which constitutes an exception for the conoideans , making terebrids a good model to test the ability of the abgd / klee approach to accurately delimit pshs . . . .
. . . tv1 is the first peptide structurally characterized from a terebrid snail . terebrids are part of the conoidean superfamily of predatory mollusks , which includes cone snails and turrids [ 18 , 19 ] . tv1 is a novel twenty - one amino acid teretoxin peptide with a cysteine scaffold similar to the m - superfamily of cone snail neurotoxins , cc - c - c - cc . . . .
. . . the family includes about 400 recent species ( castelin et al . 2012 ) . like other conoidea , terebridae are predators , most of them possessing a venom apparatus ( taylor 1990 , holford et al . 2009 ) and producing toxins , the structure of which is close to that of the toxins of cone snails ( imperial et al . 2003 , puillandre & holford 2010 ) . one of the most prominent features of terebrid evolution is the loss of specialized foregut structures , such as the proboscis , radular apparatus , venom gland and often the salivary glands — which has occurred independently in different lineages of the family ( taylor 1990 , puillandre & holford 2010 , castelin et al . 2012 ) . . . .
central to the discovery of neuroactive compounds produced by predatory marine snails of the superfamily conoidea ( cone snails , terebrids , and turrids ) is identifying those species with a venom apparatus . previous analyses of western pacific terebrid specimens has shown that some terebridae groups have secondarily lost their venom apparatus . in order to efficiently characterize terebrid . . . [ show full abstract ]
the terebridae and teretoxins : combining phylogeny and anatomy for concerted discovery of bioactive . . .
the conoidea superfamily , comprised of cone snails , terebrids , and turrids , is an exceptionally promising group for the discovery of natural peptide toxins . the potential of conoidean toxins has been realized with the distribution of the first conus ( cone snail ) drug , prialt ( ziconotide ) , an analgesic used to alleviate chronic pain in hiv and cancer patients . cone snail toxins ( conotoxins ) are . . . [ show full abstract ]
starting to unravel the toxoglossan knot : molecular phylogeny of the “turrids” ( neogastropoda : conoi . . .
the superfamily conoidea is one of the most speciose groups of marine mollusks , with estimates of about 340 recent valid genera and subgenera , and 4000 named living species . previous classifications were based on shell and anatomical characters , and clades and phylogenetic relationships are far from well assessed . based on a dataset of ca . 100 terminal taxa belonging to 57 genera , information . . . [ show full abstract ]