Scaphopod mollusks (Scaphopoda) Jan M. Strugnella,* and A. Louise Allcockb (Baltodentialiidae and Prodentaliidae), whereas four aDepartment of Zoology, University of Cambridge, Downing St, others contain at least one fossil genus each, along Cambridge, CB2 3EJ, UK; with genera containing living species (Dentaliidae, b The Martin Ryan Marine Science Institute, National University of Gadilinidae, Laevidentaliidae, and Gadilidae). 7 e orders Ireland Galway, University Road, Galway, Ireland. of Scaphopoda diB er in the shape of the foot. 7 e den- *To whom correspondence should be addressed (jan.strugnell@ gmail.com) taliidans have a conical foot whereas gadilidans have a worm-shaped foot with a terminal disk capable of expan- sion. Additional distinguishing features are provided by Abstract Steiner (2). 7 e monophyly of the two orders has been supported by morphological data (3) and by molecu- The tusk shells (~500 sp.) are grouped into 14 families lar analyses based on the nuclear gene for 18S riboso- and two orders within the molluscan Class Scaphopoda. mal RNA (rRNA) (4) and the mitochondrial cytochrome Only two molecular studies have focused on phylogen- o x i d a s e I gene (COI) (5). etic relationships within scaphopods. Estimates of diver- 7 e Order Gadilida comprises four recent families. gence times among families are estimated here. The Entalinidae is placed within the Suborder Entalimorpha, initial divergence among scaphopods, separating Gadilida distinguished by a ribbed shell and by a smooth rachis and Dentaliida, is estimated to have occurred near the in the radula. 7 e remaining three families— Pulsellidae, Devonian–Carboniferous boundary, ~359 million years Wemersoniellidae, and Gadilidae—are placed within ago (Ma), with the Fustiariidae, Rhabdidae, and Dentaliidae the Suborder Gadilimorpha, distinguished by a smooth diverging in the Carboniferous (359–299 Ma). In contrast, shell and by a cuspid rachis. Support for these suborders the families included in the study from the Order Gadilida has been provided by morphological data (3, 6–9) and were estimated to have diverged from one another in the by molecular analyses based on 18S rRNA (4), although Cretaceous, 139–96 Ma. molecular analyses based on COI have suggested that the Gadilimorpha is paraphyletic (5). Analyses 7 e scaphopods (Phylum Mollusca, Class Scaphopoda) using 18S rRNA did not support the monophyly of the are known as tusk shells because of their curved shape Gadilidae (4). (resembling elephant tusks), open at both ends (Fig. 1). 7 ey are relatively small, usually 3–6 cm in length. Scaphopods burrow into sediments with the wider (anterior) end of the shell oriented downward. Both the head and foot (used for burrowing) have an anter- ior location, whereas the viscera are posterior. 7 ere are ~500 valid species of recent scaphopods and about 800 valid fossil species. 7 ere is some argument as to when the lineage originated. Scaphopod fossils have been described from the Ordovician, Silurian, and Devonian, but many of these specimens have been reclassiA ed as belonging to other groups. Yochelson (1) and others have suggested that scaphopods most likely evolved in the early Carboniferous. Here we review the evolution- ary relationships and divergence times of the members Fig. 1 Two scaphopod shells (Pictodentalium vernedei) from of the Class Scaphopoda. Taiwan (right) and two shells of an undescribed species 7 e Class Scaphopoda consists of 14 families and two (Pictodentalium sp.) from Broome, Australia. Credit: orders. Two of the families contain only fossil genera B. Sahlmann. J. M. Strugnell and A. L. Allcock. Scaphopod mollusks (Scaphopoda). Pp. 239–241 in e Timetree of Life, S. B. Hedges and S. Kumar, Eds. (Oxford University Press, 2009). HHedges.indbedges.indb 223939 11/28/2009/28/2009 11:27:01:27:01 PPMM 240 THE TIMETREE OF LIFE Gadilidae-2 6 Pulsellidae 5 Gadilidae-1 4 Gadilida Gadilimorpha Entalinidae 1 Dentaliidae 3 Rhabdidae 2 Fustiariidae Dentaliida C P Tr JKPg Ng PALEOZOIC MESOZOIC CZ 350 300 250 200 150 100 50 0 Million years ago Fig. 2 A timetree of Scaphopoda. Divergence times are shown in Table 1. Gadilidae-1 contains the Subfamily Siphonodentaliinae and Gadilidae-2 contains the Subfamily Gadilinae of the classical Gadilidae. Abbreviations: C (Carboniferous), CZ (Cenozoic), J (Jurassic), K (Cretaceous), Ng (Neogene), P (Permian), Pg (Paleogene), and Tr (Triassic). 7 e Order Dentaliida comprises eight recent families each relevant taxon. We included the following fossils: whose interrelationships are not well resolved. DiB erent Prodentalium fredericae, Dentalium acutoides, Antalis taxon sampling within morphological studies makes torquatus, Fissidentalium pukaea, Fustiaria glabellum, comparisons di1 cult, and authors have expressed pref- Rhabdus paralelum, Entalina curvum, Cadulus groen- erences for diB erent character sets which have yielded landicus, Polyschides arnoensis, and Pulsellum infun- conP icting results. Taxon sampling within molecular dibulum. Where the speciA c age of a fossil was not given, studies is particularly poor. Representatives from three the midpoint of the epoch/age of the fossil was used as dentaliid families were sequenced for 18S rRNA (4). a minimum constraint. Fossil dates used for calibration Fustiariidae was basal to a clade composed of Dentaliidae are as follows: minimum of 329 Ma for the divergence and Rhabdidae. 7 e monophyly of Dentaliidae was of Dentalida and Gadilida, minimum of 322 Ma for not supported because of Rhabdus (Rhabdidae) falling the diversiA cation of Dentalidae (Dentalium v. Antalis), within a clade containing Antalis, Fustiaria, Dentalium, minimum 172.5 Ma for the divergence of Rhabdidae and and Fissidentalium (Dentaliidae). A study based on COI Dentalidae, minimum of 123 Ma for the divergence of (5) suggested Dentaliidae to be paraphyletic. In this case, Entalinidae and Gadilidae, minimum of 28.3 Ma for the Rhabdus grouped with Fissidentalium, which was closest divergence of Fustariidae and Dentalidae, minimum of to a clade containing Antalis and Dentalium. 18 Ma for the divergence of Gadilidae and Pulsellidae 7 ere are no previous published studies estimating (Cadulus vs. Pulsellum), a minimum of 88 Ma for the divergence times among scaphopod families. We have diversiA cation of Gadilinae (Gadilidae; Cadulus vs. therefore taken the nuclear 18S rRNA sequences from Cadulus), and a minimum of 45 Ma for the diversiA ca- GenBank (4) and applied a penalized likelihood method tion of Siphonodentaliinae (Gadilidae: Siphonodentalum of Sanderson (10) in the program “r8s” to estimate these vs. Polyschides). divergence times. Cross-validation scores were examined A variety of conP icting hypotheses has been proposed over a range of smoothing parameters to A nd the opti- as to which molluscan crown groups are closest to the mal smoothing parameter for the analysis. ConA dence Scaphopoda. However, recent molecular evidence has intervals were estimated using a bootstrap approach. supported a close relationship between Cephalopoda We selected only those (minimum) fossil constraints and Scaphopoda (4, 14). We have therefore rooted the whose validity has not been questioned to date. For tree with the four cephalopod species used in the previ- example, many authors (1, 4, 11–13) reject claims that ous study (4). Given that potential scaphopod fossil spe- Rhytiodentalium kentuckyensis and other early fos- cies have been described from as early as the Ordovician sils showing “scaphopodization” are true scaphopods (although many are admittedly controversial), we have (12). So, we have not used them. Yet, we have made an again taken a conservative approach and placed a max- attempt to select the earliest fossil representatives for imum age constraint of 488 Ma on the divergence of HHedges.indbedges.indb 224040 11/28/2009/28/2009 11:27:03:27:03 PPMM Eukaryota; Metazoa; Mollusca; Scaphopoda 241 Table 1. Divergence times (Ma) and their confi dence/ 7 e fossil record of scaphopods is extensive and is credibility intervals (CI) among tusk shell mollusks well suited to a molecular dating analysis by taking into based on analyses reported here. account the abundance and distribution of fossil scapho- Timetree pods. However, such an endeavor awaits further progress Node Time CI in molecular sequencing of the Scaphopoda. Additional sequencing of more scaphopod families and a greater 1363.3367–359number of genes would undoubtedly improve the reso- 2329.9354–306lution and information that could be gained from such 3324.0345–303an analysis. 4139.5154–124 5106.2121–91Acknowledgments 6 96.0 110–82 7 is work would not have been possible without the Note: Estimates are based on a penalized likelihood analysis of extensive catalogue of Steiner and Kabat, 2004 and the nuclear 18S rRNA sequences. without the online database of Bernd Sahlmann. J.S. is supported by a Natural Environment Research Council Antarctic Funding Initiative grant awarded to L.A and a Lloyd’s Tercentenary Fellowship. the cephalopods and scaphopods at the Cambrian– Ordovician border. 7 e resulting timetree is shown in Fig. 2. 7 e initial References divergence among scaphopods, separating Gadilida 1. E. L. Yochelson, Ann. Naturhist Mus. Wien, Ser. A 106, and Dentaliida, is estimated to have occurred ~363 13 (2004). Ma, with the Fustiariidae, Rhabdidae, and Dentaliidae 2. G. Steiner, J. Mollus. Stud. 58, 385 (1992). 3. P. D. Reynolds, A. Okusu, Zool. J. Linn. Soc. 126, 131 (1999). diverging in the Carboniferous (359–299 Ma). In con- 4. G. Steiner, H. Dreyer, Zool. Scripta 32, 343 (2003). trast, the families included in the study from the Order 5. G. Steiner, P. D. Reynolds, in Molecular Systematics Gadilida were estimated to have diverged from one and Phylogeography of Mollusks, C. Lydeard, D. L. another in the Cretaceous, 139–96 Ma. 7 e most basal Lindberg, Eds. (Smithsonian Books, Washington, 2003), family, the Entalinidae, was estimated to have diverged pp. 123–139. close to the Jurassic–Cretaceous border, 145 Ma. Steiner 6. P. D. Reynolds, Zool. Scripta 26, 13 (1997). and Dreyer’s (4) sequence data imply the polyphyly of 7.