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Helicoprionadaptation and phylogeny in fossilJaws for a spiral-tooth whorl: CT images reveal novel

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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

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.

Palaeontology

Jaws for a spiral-tooth whorl: CT imagesreveal novel adaptation and phylogeny in

fossil HelicoprionLeif Tapanila1,2, Jesse Pruitt2,3, Alan Pradel4, Cheryl D. Wilga5,

Jason B. Ramsay5, Robert Schlader3 and Dominique A. Didier6

1Department of Geosciences, Idaho State University, Pocatello, ID 83209, USA2Division of Earth Sciences, and 3Idaho Virtualization Lab, Idaho Museum of Natural History, Pocatello,

ID 83209, USA4Department of Vertebrate Paleontology, American Museum of Natural History, New York, NY 10024, USA5Department of Biological Sciences, University of Rhode Island, Kingston, RI 02881, USA6Department of Biology, Millersville University, Millersville, PA 17551, USA

New CT scans of the spiral-tooth fossil, Helicoprion, resolve a longstandingmystery 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 reconstruc-

tion 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. IntroductionThe iconic spiral-tooth whorl of Helicoprion is one of the most unusual evol-

utionary novelties among ancient chondrichthyans. For more than a century,

palaeobiologists have puzzled over its form and function in the absence of fos-

silized 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 phos-

phatic limestone from the Early Permian (270 Ma) Phosphoria Formation ofIdaho, 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 ros-

trum led to his assessment that Helicoprion belonged to the Elasmobranchii, an

ill-defined group of sharks and rays. Bendix-Almgreens symphyseal recon-

struction ([6,14]; figure 1jk) 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 tomographicscans to describe the cranial anatomy of Helicoprion. Our reassessment of the

anatomy partly confirms Bendix-Almgreens symphyseal reconstruction, but

& 2013 The Author(s) Published by the Royal Society. All rights reserved.

mailto:[email protected]://dx.doi.org/10.1098/rslb.2013.0057http://rsbl.royalsocietypublishing.org/http://rsbl.royalsocietypublishing.org/http://rsbl.royalsocietypublishing.org/http://rsbl.royalsocietypublishing.org/http://rsbl.royalsocietypublishing.org/http://rsbl.royalsocietypublishing.org/http://rsbl.royalsocietypublishing.org/http://dx.doi.org/10.1098/rslb.2013.0057http://dx.doi.org/10.1098/rslb.2013.0057mailto:[email protected]://crossmark.crossref.org/dialog/?doi=10.1098/rsbl.2013.0057&domain=pdf&date_stamp=2013-02-27


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reveals unseen features of the jaw that inform a new recon-

struction of the mandibular arch (figure 1l ). It also confirms

the phylogenetic placement of Helicoprion among the

Euchondrocephali.

2. Material and methodsThe 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 (Univer-

sity of Texas High-Resolution X-ray CT Facility) with voxel

resolution of 0.295 mm in the x- and y-planes, and 1 mm resol-

ution in the z-plane. Volume data were reconstructed usingMIMICS v. 14.11, GEOMAGIC STUDIO 2012 and BLENDER v. 2.64a.

Surface roughness of the model is an artefact of scanning resol-

ution. The whorl and teeth of IMNH 37899 are preserved

mostly as external impressions, so a model of the whorl was

generated for figure 2. This computer generated model was

produced by scanning fig. 12 of [5], and sculpting a three-dimen-

sional 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-con-

tact laser scanner at the Idaho Virtualization Lab of IMNH.

3. DescriptionIMNH 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 cal-

cified 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 2ch 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 palatoqua-

drate. 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 dome-shaped 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 hyoman-

dibula, 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 later-

ally 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 pala-

toquadrate (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 synch-

ondrosis with the dorsal surface of the Meckelian cartilagea

unique articulation found only in Helicoprion. Widened por-

tions 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 carti-

lages (figure 2f ). From the surface view of the imbedded fossil,

(a)

(c)

(b)

(d)

(e)

(f)

(g)

(i)(j)

(k)

(l)

(h)

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].


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these thin cartilage layers are restricted to the ventral and cen-

tral 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-Almgreens [5] contention that the fossil was severelycrushed 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 carti-

lage 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 obser-vation 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.

(a)

(c)

(b)

(d)

(e)

(f) (g)

(h)

5cm

pf

qmf

qf

ep

c

*

*

bp

bf

qp

pp

lj

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 oflabial 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 ( fg).


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5. DiscussionOur 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 pre-

vious symphyseal reconstructions (figure 1j,k; [5,6]) which

place the whorl at the anterior end of an elongate jaw, creat-

ing 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 continu-ous 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

toothroot 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 buttres-sing 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 sli-

cing 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 break-

age is rare in Helicoprion [5,6]. This may be a result of rapid

tooth productionsome whorls exceed 150along 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 two-

point 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 pre-

vious 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.

We thank R. Troll for artistic renderings. Funding for CT scan pro-vided by IMNH-Earth Science (L.T.) and National ScienceFoundation grant no. ATOL1036505 (D.A.D.). Post-scan analysis sup-ported by IMNH (H. Maschner), ISU-Undergraduate ResearchCommittee (J.P.), H.R. & E. Axelrod Research Chain in Paleoichthyol-ogy, AMNH (A.P.) and NSF ARC1023321 (H. Maschner). M. Colbert(U Texas) provided technical assistance with CT scanning.

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http://dx.doi.org/10.1017/S0016756800144450http://dx.doi.org/10.1017/S0016756800144450http://dx.doi.org/10.5479/si.00963801.37-1699.43http://dx.doi.org/10.1111/j.1463-6395.2008.00353.xhttp://dx.doi.org/10.1111/j.1463-6395.2008.00353.xhttp://www.karencarr.com/tmpl1.php?CID=519http://www.karencarr.com/tmpl1.php?CID=519http://paleobiology.si.edu/helicoprion/index.htmlhttp://paleobiology.si.edu/helicoprion/index.htmlhttp://dx.doi.org/10.1023/A:1018471324332http://dx.doi.org/10.1002/jmor.10642http://dx.doi.org/10.1002/(SICI)1097-4687(200003)243:3%3C219::AID-JMOR1%3E3.0.CO;2-1http://dx.doi.org/10.1002/(SICI)1097-4687(200003)243:3%3C219::AID-JMOR1%3E3.0.CO;2-1http://dx.doi.org/10.1002/(SICI)1097-4687(200003)243:3%3C219::AID-JMOR1%3E3.0.CO;2-1http://dx.doi.org/10.1002/(SICI)1097-4687(200003)243:3%3C219::AID-JMOR1%3E3.0.CO;2-1http://dx.doi.org/10.1002/(SICI)1097-4687(200003)243:3%3C219::AID-JMOR1%3E3.0.CO;2-1http://dx.doi.org/10.1002/(SICI)1097-4687(200003)243:3%3C219::AID-JMOR1%3E3.0.CO;2-1http://dx.doi.org/10.1002/(SICI)1097-4687(199901)239:1%3C45::AID-JMOR3%3E3.0.CO;2-Shttp://dx.doi.org/10.1002/(SICI)1097-4687(199901)239:1%3C45::AID-JMOR3%3E3.0.CO;2-Shttp://dx.doi.org/10.1002/(SICI)1097-4687(199901)239:1%3C45::AID-JMOR3%3E3.0.CO;2-Shttp://dx.doi.org/10.1002/(SICI)1097-4687(199901)239:1%3C45::AID-JMOR3%3E3.0.CO;2-Shttp://dx.doi.org/10.1002/(SICI)1097-4687(199901)239:1%3C45::AID-JMOR3%3E3.0.CO;2-Shttp://rsbl.royalsocietypublishing.org/http://rsbl.royalsocietypublishing.org/http://rsbl.royalsocietypublishing.org/http://rsbl.royalsocietypublishing.org/http://dx.doi.org/10.1002/(SICI)1097-4687(199901)239:1%3C45::AID-JMOR3%3E3.0.CO;2-Shttp://dx.doi.org/10.1002/(SICI)1097-4687(199901)239:1%3C45::AID-JMOR3%3E3.0.CO;2-Shttp://dx.doi.org/10.1002/(SICI)1097-4687(199901)239:1%3C45::AID-JMOR3%3E3.0.CO;2-Shttp://dx.doi.org/10.1002/(SICI)1097-4687(199901)239:1%3C45::AID-JMOR3%3E3.0.CO;2-Shttp://dx.doi.org/10.1002/(SICI)1097-4687(199901)239:1%3C45::AID-JMOR3%3E3.0.CO;2-Shttp://dx.doi.org/10.1002/(SICI)1097-4687(199901)239:1%3C45::AID-JMOR3%3E3.0.CO;2-Shttp://dx.doi.org/10.1002/(SICI)1097-4687(199901)239:1%3C45::AID-JMOR3%3E3.0.CO;2-Shttp://dx.doi.org/10.1002/(SICI)1097-4687(200003)243:3%3C219::AID-JMOR1%3E3.0.CO;2-1http://dx.doi.org/10.1002/(SICI)1097-4687(200003)243:3%3C219::AID-JMOR1%3E3.0.CO;2-1http://dx.doi.org/10.1002/(SICI)1097-4687(200003)243:3%3C219::AID-JMOR1%3E3.0.CO;2-1http://dx.doi.org/10.1002/(SICI)1097-4687(200003)243:3%3C219::AID-JMOR1%3E3.0.CO;2-1http://dx.doi.org/10.1002/(SICI)1097-4687(200003)243:3%3C219::AID-JMOR1%3E3.0.CO;2-1http://dx.doi.org/10.1002/(SICI)1097-4687(200003)243:3%3C219::AID-JMOR1%3E3.0.CO;2-1http://dx.doi.org/10.1002/(SICI)1097-4687(200003)243:3%3C219::AID-JMOR1%3E3.0.CO;2-1http://dx.doi.org/10.1002/(SICI)1097-4687(200003)243:3%3C219::AID-JMOR1%3E3.0.CO;2-1http://dx.doi.org/10.1002/jmor.10642http://dx.doi.org/10.1023/A:1018471324332http://paleobiology.si.edu/helicoprion/index.htmlhttp://paleobiology.si.edu/helicoprion/index.htmlhttp://paleobiology.si.edu/helicoprion/index.htmlhttp://www.karencarr.com/tmpl1.php?CID=519http://www.karencarr.com/tmpl1.php?CID=519http://www.karencarr.com/tmpl1.php?CID=519http://dx.doi.org/10.1111/j.1463-6395.2008.00353.xhttp://dx.doi.org/10.1111/j.1463-6395.2008.00353.xhttp://dx.doi.org/10.5479/si.00963801.37-1699.43http://dx.doi.org/10.1017/S0016756800144450http://dx.doi.org/10.1017/S0016756800144450

biol. lett. 2013 tapanila

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