Downloaded from http://rsbl.royalsocietypublishing.org/ on June 16, 2017
Palaeontology
rsbl.royalsocietypublishing.org
Research
Cite this article: Tapanila L, Pruitt J, Pradel
A, Wilga CD, Ramsay JB, Schlader R, Didier DA.
2013 Jaws for a spiral-tooth whorl: CT images
reveal novel adaptation and phylogeny in fossil
Helicoprion. Biol Lett 9: 20130057.
http://dx.doi.org/10.1098/rsbl.2013.0057
Received: 18 January 2013
Accepted: 6 February 2013
Subject Areas:
palaeontology, evolution
Keywords:
mandibular arch, autodiastyly, Phosphoria,
Chondrichthyes, Euchondrocephali, Permian
Jaws for a spiral-tooth whorl: CT images
reveal novel adaptation and phylogeny in
fossil Helicoprion
Leif Tapanila1,2, Jesse Pruitt2,3, Alan Pradel4, Cheryl D. Wilga5,
Jason B. Ramsay5, Robert Schlader3 and Dominique A. Didier6
1
Department of Geosciences, Idaho State University, Pocatello, ID 83209, USA
Division of Earth Sciences, and 3Idaho Virtualization Lab, Idaho Museum of Natural History, Pocatello,
ID 83209, USA
4
Department of Vertebrate Paleontology, American Museum of Natural History, New York, NY 10024, USA
5
Department of Biological Sciences, University of Rhode Island, Kingston, RI 02881, USA
6
Department of Biology, Millersville University, Millersville, PA 17551, USA
2
New CT scans of the spiral-tooth fossil, Helicoprion, resolve a longstanding
mystery concerning the form and phylogeny of this ancient cartilaginous
fish. We present the first three-dimensional images that show the tooth
whorl occupying the entire mandibular arch, and which is supported along
the midline of the lower jaw. Several characters of the upper jaw show that
it articulated with the neurocranium in two places and that the hyomandibula
was not part of the jaw suspension. These features identify Helicoprion as a
member of the stem holocephalan group Euchondrocephali. Our reconstruction illustrates novel adaptations, such as lateral cartilage to buttress the
tooth whorl, which accommodated the unusual trait of continuous addition
and retention of teeth in a predatory chondrichthyan. Helicoprion exemplifies
the climax of stem holocephalan diversification and body size in Late
Palaeozoic seas, a role dominated today by sharks and rays.
1. Introduction
Author for correspondence:
Leif Tapanila
e-mail: [email protected]
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rslb.2013.0057 or
via http://rsbl.royalsocietypublishing.org.
The iconic spiral-tooth whorl of Helicoprion is one of the most unusual evolutionary novelties among ancient chondrichthyans. For more than a century,
palaeobiologists have puzzled over its form and function in the absence of fossilized cranial or postcranial elements, leading to numerous creative but largely
untested reconstructions ([1 –12]; figure 1a–i). Bendix-Almgreen [5] described
the only known Helicoprion specimen (IMNH 37899) that preserves endoskeletal
elements in association with the whorl. The fossil is imbedded in a slab of phosphatic limestone from the Early Permian (270 Ma) Phosphoria Formation of
Idaho, USA. With limited exposure, Bendix-Almgreen interpreted calcified
layers of cartilage as the jaws and anterior portion of the neurocranium. His
reconstruction placed the tooth whorl at the front midline of elongate lower
jaws (figure 1j; [5,13]), and his interpretation of a neurocranial capsule and rostrum led to his assessment that Helicoprion belonged to the Elasmobranchii, an
ill-defined group of sharks and rays. Bendix-Almgreen’s ‘symphyseal’ reconstruction ([6,14]; figure 1j –k) has not been challenged by new physical
evidence in the intervening decades. Phylogenetic interpretations of Helicoprion
and its spiral-tooth relatives have been less stable; however, most recent
analyses based on dental characters have placed Helicoprion among the
Euchondrocephali, which include modern chimaera and ratfish [15,16].
In this study, we re-examine IMNH 37899 using computer tomographic
scans to describe the cranial anatomy of Helicoprion. Our reassessment of the
anatomy partly confirms Bendix-Almgreen’s symphyseal reconstruction, but
& 2013 The Author(s) Published by the Royal Society. All rights reserved.
Downloaded from http://rsbl.royalsocietypublishing.org/ on June 16, 2017
(b)
(c)
(d)
(e)
(g)
(i)
(h)
(k)
( j)
(l)
Figure 1. Reconstructions of Helicoprion since 1899. Earliest models (a – d )
posited the whorl as an external defensive structure, but (e – l ) feeding
reconstructions dominate more recent hypotheses. Credits: (a) Woodward
[2]; (b) Simoens [11]; (c) Karpinsky [12]; (d ) Obruchev [7]; (e) Van den
Berg in Obruchev [7]; (f ) John [8]; (g) Carr [9]; (h) Eaton [4]; (i) Parrish
in Purdy [10]; ( j ) Troll in Matsen & Troll [13] based on Bendix-Almgreen
[5]; (k) Lebedev [6]; (l ) Troll & Ramsay, this study. Configuration of gill
slits and fins based on related fish, e.g. Caseodus and Ornithoprion [14].
reveals unseen features of the jaw that inform a new reconstruction of the mandibular arch (figure 1l ). It also confirms
the phylogenetic placement of Helicoprion among the
Euchondrocephali.
2. Material and methods
The rock slab containing IMNH 37899 (figure 2a), also known as
‘Idaho 4’ [5], is 32.9 30.2 13.1 cm. It was collected in 1950
from the historic Waterloo Mine near Montpelier, Idaho (42.38 N,
111.28 W) and deposited at the Idaho Museum of Natural History.
Bendix-Almgreen [5] diagnosed the specimen as Helicoprion ferrieri.
IMNH 37899 was scanned using an ACTIS scanner (University of Texas High-Resolution X-ray CT Facility) with voxel
resolution of 0.295 mm in the x- and y-planes, and 1 mm resolution in the z-plane. Volume data were reconstructed using
MIMICS v. 14.11, GEOMAGIC STUDIO 2012 and BLENDER v. 2.64a.
Surface roughness of the model is an artefact of scanning resolution. The whorl and teeth of IMNH 37899 are preserved
mostly as external impressions, so a model of the whorl was
IMNH 37899 has a whorl measuring 23 cm in diameter and
bearing 117 serrated tooth crowns (figure 2a), most preserved
as impressions. The series of tooth crowns are anchored to a
continuous osteodentine root and calcified cartilaginous base
that forms a logarithmic spiral of 314 revolutions, with tooth
size increasing outward from the spiral centre. Prismatic calcified cartilage layers of the mandibular arch have lower
density than the rock matrix, and are shown in CT scans to
be largely intact throughout the specimen.
CT scans reveal the complete left upper and lower jaws in
closed articulated position around the medial tooth whorl (see
figure 2c–h and electronic supplementary material, figure S1).
A large wedge of cartilage extends from the lower jaw and
braces against the outermost root of the whorl. Inner parts of
the whorl are surrounded by coarse prismatic tessellated
cartilage. No portion of the neurocranium is preserved.
The upper jaw is composed of a triangular palatoquadrate. Its posterior border flares laterally for its entire
length, and medial to this is a vertical basitrabecular fossa
and basal process. The quadrate process displays dual jointed
articular surfaces that correspond with respective articular
surfaces of the lower jaw (Meckelian cartilage), a primitive
feature of jawed vertebrates. The elongate palatine ramus
tapers anteriorly, with a pronounced medial circular domeshaped ethmoid process. Quadrate and palatine fossae are
located on the lateral surface for quadratomandibular
muscle attachment. There is no evidence of a groove on the
medial surface of the quadrate to accommodate the hyomandibula, and the CT scans provide no evidence for dentition
associated with the palatoquadrate.
The Meckelian cartilage of the lower jaw is incomplete in
its posteroventral region. Its anteroventral surface flares laterally to border the quadratomandibular fossa ventrally. On
the Meckelian cartilage anterior to the jaw joint, a process
projects dorsally and abuts a descending process of the palatoquadrate (figure 2g). These processes may serve to restrict
closure of the lower jaw, and consequently prevent the
tooth whorl from puncturing the neurocranium.
The labial cartilage is a distinct element that forms a synchondrosis with the dorsal surface of the Meckelian cartilage—a
unique articulation found only in Helicoprion. Widened portions of the blade-shaped labial cartilage match the dorsal
position of successive roots in the whorl, suggesting a gliding
articulation with the base of the root (figure 2d,g). The posterior
region of the labial cartilages forms a cup-shaped structure that
surrounds the developing root of the last volution. This is the
only structure that was reoriented in producing the CT
model, shifting three collapsed fragments of the posterior
margin approximately 1 cm in a medial-anterior direction.
Part of the tessellated cartilages that surround the inner
parts of the whorl are visible in scans and do not appear to
articulate directly with either the lower jaw or the labial cartilages (figure 2f ). From the surface view of the imbedded fossil,
Biol Lett 9: 20130057
( f)
3. Description
2
rsbl.royalsocietypublishing.org
(a)
generated for figure 2. This computer generated model was
produced by scanning fig. 12 of [5], and sculpting a three-dimensional whorl using BLENDER v. 2.64a software. Fig. 24b of [5] was
used to accurately model the thickness of teeth and root. The
model whorl was then scaled to match a surface scan of IMNH
37899 (figure 2b), made using a KonicaMinolta Vivid9i non-contact laser scanner at the Idaho Virtualization Lab of IMNH.
Downloaded from http://rsbl.royalsocietypublishing.org/ on June 16, 2017
3
5 cm
(a)
(b)
rsbl.royalsocietypublishing.org
bp
pf
ep
c
*
*
(e)
(h)
bf
qmf
(f)
(g)
lj
qp
pp
Figure 2. Helicoprion specimen IMNH 37899, preserving cartilages of the mandibular arch and tooth whorl. (a) Photograph and (b) surface scan of fossil, positioned
anterior to the right, imbedded in limestone slab. (c) CT model of specimen in lateral, (d ) medial, (e) posterior, (f ) oblique lateral, (g) oblique medial and
(h) ventral views. Modelled tooth whorl (grey, black outline) surrounded by palatoquadrate (green), Meckelian (blue) and labial (red) cartilages. (d ) Asterisks
mark widened part of labial cartilage corresponding to successive root volutions. (f ) Palatoquadrate removed to show scanned portion of root (dark yellow),
tooth crowns ( pale yellow) and tessellated cartilages of the inner whorl ( purple). Arrow indicates direction of root growth and advancement to form spiral.
(h) Right side of image mirrored to show paired jaw elements surrounding the whorl. bf, basitrabecular fossa; bp, basal process; c, cup-shaped portion of
labial cartilage; ep, ethmoid process; lj, labial joint with base of root; pf, lateral palatine fossa; pp, process limiting jaw closure; qf, lateral quadrate fossa;
qmf, quadratomandibular fossa; qp, quadrate process. Scale bar applies to all but oblique views (f– g).
these thin cartilage layers are restricted to the ventral and central parts of the whorl. Only the outermost eight tooth crowns
and a short arc of root appear in the scan (figure 2f ).
4. Comparison
Bendix-Almgreen’s [5] contention that the fossil was severely
crushed and disarticulated from burial largely explains why
our interpretations of the fossil differ. Our most substantial
anatomical revision concerns the upper jaw. The anterior
part, which we interpret as the palatine region, was interpreted
by Bendix-Almgreen as the neurocranial cavity and rostrum,
but CT evidence demonstrates continuity of the calcified cartilage through the palatine and quadrate regions of the upper
jaw. Scans also show that the anterior part of the lower jaw
does not include a projection beyond the whorl, as suggested
by Bendix-Almgreen, nor do we find CT evidence for a tooth
pavement associated with the upper jaw. Finally, identification
of labial cartilages concealed by the rock matrix is a new observation afforded by CT imaging. Although, its articulation with
the Meckelian cartilage is unique to Helicoprion, designating
them as labial cartilage is conservative because these elements
are common to chondrichthyans.
Biol Lett 9: 20130057
(d)
qf
(c)
Downloaded from http://rsbl.royalsocietypublishing.org/ on June 16, 2017
5. Discussion
References
1.
2.
3.
4.
5.
6.
7.
Woodward H. 1886 On a remarkable ichthyodorulite
from the Carboniferous series, Gascoyne, Western
Australia. Geol. Mag. 3, 1– 7. (doi:10.1017/
S0016756800144450)
Karpinsky AP. 1899 On the edestid remains and its new
genus Helicoprion. Zapiski Imperat. Akad. Nauk 7, 1–67.
Hay OP. 1909 On the nature of Edestus and related
genera, with descriptions of one new genus and
three new species. Proc. United States Natl Mus. 37,
43 –61. (doi:10.5479/si.00963801.37-1699.43)
Eaton Jr TH. 1962 Teeth of edestid sharks. Univ.
Kansas Publ. Mus. Nat. Hist. 12, 347–362.
Bendix-Almgreen SE. 1966 New investigations on
Helicoprion from the Phosphoria Formation of
south-east Idaho, USA. Biol. Skrifter udgivet af det
Kongelige Danske Videnskabernes Selskab 14, 1– 54.
Lebedev OA. 2009 A new specimen of Helicoprion
Karpinsky, 1899 from Kazakhstanian Cisurals and a
new reconstruction of its tooth whorl position and
function. Acta Zool. 90, 171– 182. (doi:10.1111/j.
1463-6395.2008.00353.x)
Obruchev DV. 1953 Edestid studies and the works
by A. P. Karpinsky. Trudy Paleontol. Inst. Akad. Nauk
SSSR 45, 1– 85.
8.
9.
10.
11.
12.
13.
14.
John F. 1910 Spiralhai (Helicoprion) und Stachelhai
(Xenacanthus) (Lithograph). Tiere der Urwelt,
series 2, card 9. Hamburg, Germany: Reichardt
Kakao Compagnie.
Carr K. 2012 Helicoprion for Hoff Productions. Silver
City, NM: Karen Carr Studio Inc. See http://www.
karencarr.com/tmpl1.php?CID=519 (accessed 16
January 2013).
Purdy RW. 2008 The orthodonty of Helicoprion.
Washington, DC: Smithsonian National
Museum of Natural History. See http://paleobiology.
si.edu/helicoprion/index.html (accessed 16 January
2013).
Simoens G. 1902 Note sur Helicoprion bessonowi
(Karpinsky). Bull. Soc. Belge Geol. Paleont. Hydr. 13,
1900 –1902.
Karpinsky AP. 1911 Notes on Helicoprion and other
edestids. Izvestiya Imperat. Akad. Nauk 5,
1105 –1122.
Matsen B, Troll R. 1994 Planet ocean: a story of life,
the sea and dancing to the fossil record. Berkeley,
CA: Ten Speed Press.
Zangerl R. 1981 Handbook of palaeoichthyology.
Berlin, Germany: Springer.
15. Lund R, Grogan ED. 1997 Relationships of the
Chimaeriformes and the basal radiation of the
Chondrichthyes. Rev. Fish Biol. Fish. 7, 65 –123.
(doi:10.1023/A:1018471324332)
16. Ginter M, Hampe O, Duffin C. 2010 The
morphology of the dentition in Paleozoic
Elasmobranchii. In Handbook of paleoichthyology
(ed. H-P Schultze), pp. 1–168. Berlin, Germany:
Springer.
17. Maisey JG. 2008 The postorbital palatoquadrate
articulation in elasmobranchs. J. Morphol.
269, 1022– 1040. (doi:10.1002/jmor.10642)
18. Grogan ED, Lund R. 2000 Debeerius ellefseni
(Fam. Nov., Gen. Nov., Spec. Nov.), an autodiastylic
chondrichthyan from the Mississippian Bear Gulch
Limestone of Montana (USA), the relationships of the
Chondrichthyes, and comments on gnathostome
evolution. J. Morphol. 243, 219–245. (doi:10.1002/
(SICI)1097-4687(200003)243:3,219::AID-JMOR1.3.
0.CO;2-1)
19. Grogan ED, Lund R, Didier D. 1999 Description of
the chimaerid jaw and its phylogenetic origins.
J. Morphol. 239, 45 –59. (doi:10.1002/(SICI)10974687(199901)239:1,45::AID-JMOR3.3.0.CO;2-S)
Biol Lett 9: 20130057
We thank R. Troll for artistic renderings. Funding for CT scan provided by IMNH-Earth Science (L.T.) and National Science
Foundation grant no. ATOL1036505 (D.A.D.). Post-scan analysis supported by IMNH (H. Maschner), ISU-Undergraduate Research
Committee (J.P.), H.R. & E. Axelrod Research Chain in Paleoichthyology, AMNH (A.P.) and NSF ARC1023321 (H. Maschner). M. Colbert
(U Texas) provided technical assistance with CT scanning.
4
rsbl.royalsocietypublishing.org
Our reconstruction posits that the tooth whorl is a singular,
symphyseal structure of the lower jaw that occupied the
full length of the mandibular arch. This contrasts with previous symphyseal reconstructions (figure 1j,k; [5,6]) which
place the whorl at the anterior end of an elongate jaw, creating a space between the whorl and the jaw joint. In our
model, the posterior region of the lower jaw is the site
where ever-larger tooth crowns are produced atop a continuous root that is buttressed laterally by the labial cartilage. The
gliding articulation between the root and labial cartilage
serves as the linkage between the left and right lower jaws
(figure 2h). Continual growth of the whorl pushes the
tooth –root complex in a curved direction towards the front
of the jaw, where it eventually spirals to form the base of
the newest root material, and this process continues to form
successive revolutions (figure 2f ). At some time, prior to a
complete 3608 volution of spiral growth, tooth crowns are
concealed within tessellated cartilage.
Retention of teeth in a continuously growing whorl
necessitates specialized morphologies, including the buttressing labial cartilages to maintain rigidity and alignment of
the whorl, as it occludes between the upper jaws. With the
jaw articulation next to the whorl, closure of the lower jaw
rotates the teeth dorsoposteriorly, providing an effective slicing mechanism for the blade-like serrated teeth and
forcing food to the back of the oral cavity.
Accommodating the continuous growth of the logarithmic
whorl required commensurate anterior and dorsal expansion
of the mandibular arch to house the symphyseal structure.
Based on the largest diameter whorls in the IMNH collections,
Helicoprion jaw length and height could exceed 50 cm, nearly
double the size of IMNH 37899. Pre-mortal tooth wear or breakage is rare in Helicoprion [5,6]. This may be a result of rapid
tooth production—some whorls exceed 150—along with prey
selection of soft-bodied animals, such as cephalopods [6] or
poorly armoured fish.
CT scans demonstrate that Helicoprion possessed an
autodiastylic jaw suspension [17] characterized by a twopoint articulation of the upper jaw to the neurocranium via
ethmoid and basal processes, and the absence of a dorsal
extension (otic process) and hyomandibular articulation site
on the upper jaw [18]. An autodiastylic jaw suspension is
diagnostic of euchondrocephalans [19], which confirms previous dentition-based phylogenies placing Helicoprion
among the Euchondrocephali. This result provides new
insight into the evolutionary history of early holocephalans,
including their high degree of specialization and large body
size during the Late Palaeozoic, which may correspond to
the increased diversity and abundance of cephalopod prey
at this time.