J Mammal Evol
DOI 10.1007/s10914-014-9254-9
ORIGINAL PAPER
Comparative Anatomy of the Petrosal Bone of Dichobunoids,
Early Members of Artiodactylamorpha (Mammalia)
M. J. Orliac & M. A. O’Leary
# Springer Science+Business Media New York 2014
Abstract Among Artiodactylamorpha, dichobunoids are
some of the oldest fossil species that have been associated
with Artiodactyla, the crown clade that includes
hippopotamids, camelids, suoids, ruminants, and cetaceans.
These important fossil species are known from early Eocene
rocks of North America, Europe, and Asia, but their phylogenetic position has yet to be well resolved. Before generating
such a phylogeny, it is first critical to document all of the
anatomy of known dichobunoid fossils. Here we use CT scans
to describe previously undescribed anatomy of the petrosal
bone, a complex part of the mammalian skull that contains
many variable and phylogenetically informative features. Results show that these extinct species share a number of features
that are not documented in modern species including a lateral
process of the epitympanic wing constituting the medial border of the piriform fenestra, and a tegmen tympani foramen
that may have given passage to the ramus superior of the
stapedial artery. Future comprehensive phylogenetic studies
may show that many of these characters are plesiomophic for
Artiodactylamopha. Some species (Diacodexis, Homacodon
and ?Helohyus) exhibit a dorsolateral exposure of the mastoid
region of the petrosal on the temporal part of the cranium. This
uncommon feature has, to our knowledge, not been reported
in another euungulate group.
Electronic supplementary material The online version of this article
(doi:10.1007/s10914-014-9254-9) contains supplementary material,
which is available to authorized users.
M. J. Orliac (*)
ISE-M, Université Montpellier2, Place Eugène Bataillon,
34095 Montpellier cedex 05, France
e-mail: maeva.orliac@univ-montp2.fr
M. J. Orliac : M. A. O’Leary
Department of Anatomical Sciences, HSC-T-8 (040), Stony Brook
University, Stony Brook, NY 11794-8081, USA
Keywords Middle ear . Eocene . Euungulata . micro CTscan
Introduction
Dichobunoidea is a paraphyletic assemblage of Eocene fossil
species that has been linked taxonomically to Artiodactyla
(McKenna and Bell 1997; Theodor et al. 2007). Spaulding
et al. (2009) recently defined Artiodactyla as a crown clade
and named Artiodactylamorpha as its associated total clade
(fossil species more closely related to Artiodactyla than to any
other living species, following de Queiroz 2007).
Dichobunoidea is composed of seven families:
Diacodexeidae, Homacodontidae, Dichobunidae, Helohyidae,
Leptochoeridae, Cebochoeridae, and Raoellidae (Theodor
et al. 2007). The relationships of most of these families to
modern artiodactyl clades are still being investigated and
several interesting phylogenetic questions remain to be tested.
These include whether Diacodexis, one of the oldest artiodactyl species documented in the fossil record (Rose 2006;
Theodor et al. 2007), is also one of the most basal branches
within Artiodactylamorpha (e.g., Geisler et al. 2007;
Thewissen et al. 2007, 2009; Geisler and Theodor 2009), or
whether it is a more highly nested species (Spaulding et al.
2009; Orliac and Ducrocq 2011; Gatesy et al. 2012), and
whether dichobunoid taxa are stem taxa to different extant
artiodactyl clades (e.g., Gatesy et al. 2012).
Petrosal bones of the ear region have long been viewed as
highly relevant to mammalian systematics because these complex bones preserve important anatomical variation for comparison (e.g., Mammalia: MacIntyre 1972; Wible et al. 1995,
2001; Metatheria: Ladevèze 2007; Carnivora: Hunt 1974,
2001; primates and insectivorans: MacPhee 1981; Asher
et al. 2002; “condylarths”: Cifelli 1982; and more recently,
Artiodactyla: Geisler and Luo 1998; Theodor 2010; O’Leary
20 10). Yet for many foss il species assigned to
J Mammal Evol
Artiodactylamorpha the petrosal bone has remained undocumented, or only partially described, because few skulls are
known and, of those, the petrosal is preserved in situ in the
skull such that most views are obscured. For example, the
petrosal bone of Diacodexis, and several other dichobunoid
species (Homacodon, ?Helohyus, Gobiohyus), has been described only from its ventrolateral surface (Coombs and
Coombs 1982; Russell et al. 1983; Geisler and Luo 1998).
Here we describe the entire petrosal of representatives of five
of seven dichobunoid families: Diacodexis (Diacodexeidae),
Homacodon (Homacodontidae), Dichobune (Dichobunidae),
?Helohyus (Helohyidae), Gobiohyus (Helohyidae?), and
Acotherulum (Cebochoeridae) using CT scans of in situ petrosals
that permit visualization of surfaces that could not be seen
previously. Our survey of petrosal morphology from this broad
sample of putative basal artiodactylamorphans provides important primary data for future phylogenetic analyses that are even
more taxonomically comprehensive than those mentioned above.
We propose some hypotheses of character evolution based on the
patterns we observe.
Abbreviations
AMNH – VP
MNHN Qu
UM2
USNM
American Museum of Natural History,
Vertebrate Paleontology collection
Museum Nationale d’Histoire Naturelle,
Paris, Quercy collection
Université Montpellier2, France
United States Museum of Natural History,
Vertebrate Paleontology collection.
Material and Methods
In situ petrosals of Diacodexis ilicis (Diacodexeidae),
Homacodon vagans (Homacodontidae), Dichobune leporina
(Dichobunidae), ?Helohyus plicodon (Helohyidae),
Gobiohyus orientalis (Helohyidae?), and Acotherulum
saturninum (Cebochoeridae) were documented using virtual
3D extraction. The suprageneric systematics follows that of
Theodor et al. (2007) and Erfurt and Métais (2007). The
familial attribution of Gobiohyus is still problematic (Foss
2007), and this taxon is here attributed to “Helohyidae?.”
The specimens were first scanned using the high resolution
GE phoenix|vtome|x s240 industrial CT scanner at the AMNH
or the Skyscan/1076/in vivo CT scanner at the ISE-M (UM2).
The number, dimensions, and thickness of CT slices varied
depending on the size of the specimen and which machine was
used. The list of specimens and the resolution of their corresponding scans are provided in Appendix 1. We reconstructed
two-dimensional slices from X-rays using VGStudioMax®
(version 1.2; VolumeGraphics GmbH 2004). We extracted
digital endocasts using the segmentation tools of AVIZO 6.3
(Visualization Sciences Group). Paired stereo images of the
petrosals are provided in Electronic Supplementary Material
(Figs. S1-S10, MorphoBank Project 946).
Descriptions
Because the petrosal anatomy of these species is largely
unknown, we first present five new full petrosal descriptions
followed by a comparative discussion. Figure 1 shows the
general orientation of the petrosal bone within the skulls of
these artiodactylamorphans in medial, anterior, and dorsal
views. Note that the bone is tightly wedged into the skull.
Figures 2, 3, 4, 5, 6, 7, 8, and 9 consist of comparative
illustrations showing the petrosals of the different species in
ventrolateral (Figs. 2, 6, and 8), dorsomedial (Figs. 3, 7, and
9), dorsolateral (Fig. 4), and ventromedial (Fig. 5) views.
Figure 10 is a comparative plate showing the external exposure of the mastoid region on the skull. Stereo images of the
petrosals are provided in Electronic Supplementary Material
(Figs. S1-S10, MorphoBank Project 946) as well as illustrations of the ventral views of the basicranium of Homacodon
vegans (Fig. S11), ?Helohyus plicodon (Fig. S12), and
Gobiohyus orientalis (Fig. S13). The tympanic bulla is absent
in all of the specimens described here except Acotherulum
saturninum, where it is only partially preserved.
Terminology (Appendix 2) follows that of Wible (2003),
Giannini et al. (2006), and Luo and Gingerich (1999), which
was applied to, and expanded upon, for Artiodactyla and
relatives in O’Leary (2010:Table 2). Four new terms are
defined here: i) the lateral process of the epitympanic wing,
a prong of bone of variable size protruding laterally and
anteriorly from the epitympanic wing and constituting the
lateral border of the piriform fenestra, it typically terminates
in a point anteriorly (Fig. 1c); ii) the tegmen tympani canal, a
channel that traverses the tegmen tympani vertically creating a
passage between the middle ear and the cranial cavity, its
tympanic opening lies lateral to the fenestra vestibuli and its
endocranial opening on the dorsal aspect of the tegmen (see
Fig. 4); iii) the tegmen tympani fossa, a depression located on
the tegmen tympani, dorsal to the hiatus Fallopii that is directed anteriorly toward the cerebral cavity; and iv) the
anteromedial tuberosity of the petrosal, a structure located
on the lateral edge of the dorsomedial surface of the petrosal
lateral to the foramen acusticum superius (= “knob” of
O’Leary 2010). Inferences about soft tissues hypothesized to
be associated with the osteological structures described here
are briefly discussed in the section “Anatomical Comparisons
and Character States.”
In Fig. 1 we identify an opening in the skull as the piriform
fenestra using the topological definition from O’Leary et al.
(2013) that the piriform fenestra is a “gap between petrosal
and sphenoid on basicranium, anterolateral to the
J Mammal Evol
Fig. 1 Orientation of left petrosal
in skull, CT scan of Homacodon
vagans (USNM 482369) showing
petrosal in situ in, with the skull
cut virtually through a), sagittal b)
coronal, and c) and d) transverse
sections; a) shows the
dorsomedial petrosal surface,
which faces the cerebellum, b)
shows the petrosal in anterior
view with the outline of the
dorsolateral surface that abuts
other skull bones (e.g., the
squamosal), c) and d) show the
relationships of the petrosal to the
surrounding bones, in dorsal and
ventral views of the skull,
respectively. The view shown in
(d) indicates that the medial edge
of the petrosal approximates the
basioccipital/basisphenoid.
Scale=10 mm
promontorium; typically medial or posteromedial to foramen
ovale (…) also distinguished positionally from carotid foramen, which is anteromedial to promontorium versus anterolateral for piriform fenestra” (Character 564, MorphoBank
project 773). Our definition of the promontorium includes
all flanges extending from it combined with its central, bulging portion. Dichobunoid artiodactyls described in this work
all present one single gap anterolateral to the promontorium,
identified here as the piriform fenestra. There is no separate
carotid foramen, and soft tissue structures such as the internal
carotid artery and nerve may be reconstructed as passing
through the piriform fenestra (see prior work on artiodactyl
basicranial anatomy by Geisler and Luo 1998).
Diacodexeidae: Diacodexis ilicis (Figs. 2a, 3a, 4a, 5a, and
10c; Fig. S1)
The specimen consists of the right petrosal of a nearly
complete skull and partial dentition of Diacodexis ilicis
(AMNH 16141; Willwood Formation (“Sand Coulee beds,
Clarks Fork Basin, Wyoming, expedition 1912). Based on
subsequent biostratigraphic work in this area, the locality
yielding the specimen is likely of the earliest Wasatchian age
(approximately 55 Ma; Coombs and Coombs 1982; Gingerich
1989), making it one of the oldest fossils ever attributed to
Artiodactyla. Only the ventrolateral view of the petrosal of this
rare specimen has been described previously (Coombs and
Coombs 1982; Geisler and Luo 1998). The reconstructed 3D
model shows that the bone suffered little postmortem damage
other than the minor abrasions visible on the ventral surface,
such as breakage on the promontorium (not previously figured)
anterior to the fenestra cochleae and on its medial border.
On the ventrolateral surface (Fig. 2), the promontorium is
elongate and ellipse-shaped but relatively flat (Fig. 2a). It is
defined medially by a subtle groove that distinguishes the
flanges of the pars cochlearis from the promontorium itself.
There is a distinct epitympanic wing and adjacent to it a
narrow posteromedial flange. These two flanges are contiguous around the promontorium from laterally, anteriorly, and
medially. The epitympanic wing terminates anteriorly as a
point and also has a small lateral process that is pointed and
distinct. The fenestra vestibuli is oval and appears to be
smaller than the oval-shaped fenestra cochleae; however, the
J Mammal Evol
Fig. 2 Ventrolateral views of the petrosals of (a) Diacodexis ilicis (AMNH 16141; reversed from right); and (b) Acotherulum saturninum (MNHM Qu
16366). Grey surfaces indicate broken parts of the specimens. Scale=2 mm
latter is broken making it possible to only estimate its full size.
These fenestrae are separated by a wide crista interfenestralis.
Grooves on the promontorium are very subtle but there appears to be a single transpromontorial sulcus that is broad and
shallow, and a short and shallow sulcus for the stapedial artery
that runs toward the fenestra vestibuli (also noted by Geisler
and Luo 1998). We interpret the fossa for the tensor tympani
muscle to be wider than that figured by Geisler and Luo
(1998) and this depression does not excavate the tegmen
tympani. The secondary facial foramen is directly lateral to
the fenestra vestibuli occupying a relatively anterior position.
It opens onto a distinct and wide facial sulcus that passes
lateral to the stapedial muscle fossa. The latter is a broad,
poorly-defined depression directly posterior to the fenestra
cochleae. Despite breakage to the fenestra cochleae (noted
above) it can be ascertained that that it was directed posteriorly. As described by Coombs and Coombs (1982:225), the
medial part of the mastoid region directly adjacent to the
squamosal bears a small process identified as the
tympanohyal. The stylomastoid notch is a broad trough.
J Mammal Evol
Fig. 3 Dorsomedial views of the petrosals of (a) Diacodexis ilicis (AMNH 16141; reversed from right); and (b) Acotherulum saturninum (MNHM Qu
16366). Scale=2 mm
On the pars canalicularis, the tegmen tympani is narrow,
only moderately inflated, and lacks an anterior process. The
hiatus Fallopii is a long, narrow slit that lies lateral to the
anterior margin of the fossa for the tensor tympani muscle.
The tegmen tympani is perforated by a clear canal that opens
ventrally, directly lateral to the secondary facial foramen, and
posterodorsally on the dorsal surface of the tegmen tympani
(Figs. 2a and 4a). The epitympanic recess is a shallow
depression that lacks a distinct fossa for the head of the
malleus; the fossa incudis cannot be identified. The petrosal
contribution to the external acoustic meatus is wide and deep,
and the ventrolateral tuberosity is a low bump. The
tympanohyal is preserved on the medial extremity of the crista
parotica, which is a very clear ridge extending posterior to the
facial sulcus and stapedial muscle fossa. There is a small
caudal tympanic process directly posterior to the fenestra
J Mammal Evol
Fig. 4 Anterior views of the petrosals of (a) Diacodexis ilicis (AMNH
16141; reversed from right); (b) Acotherulum saturninum (MNHM Qu
16366); (c) Dichobune leporina (MNHN Qu 16586); (d) Homacodon
vagans (USNM 482369; reversed from right); (e) ?Helohyus plicodon
(USNM 13079; reversed from right); and (f) Gobiohyus orientalis
(USNM 26277; reversed from right). Scale=2 mm for a, b, c, f and
scale=5 mm for d and e
cochleae. The mastoid region is a wedge of bone whose
ventral surface is relatively smooth.
The dorsomedial surface of the petrosal (Fig. 3) is smooth
and the mastoid region comprises approximately half the total
size of the bone. The internal acoustic meatus lacks a distinct
border and both the foramina acusticum inferius and superius
are close to the surface of the bone and clearly visible. A wide
crista transversa separates these two openings. The tegmen
tympani meets the dorsomedial surface at a right angle and
there is no prefacial commissure fossa (a fossa located on the
medial surface of the tegmen tympani (O’Leary 2010)=
suprameatal fossa of Luo and Gingerich 1999). The
basicapsular groove is very distinctive and extends
continuously from the anterior extreme of the bone to the
mastoid region. Posteriorly, a sharp ridge separates the internal
acoustic meatus from the subarcuate fossa. This fossa is
extremely deep and large, almost equal in size to the internal
acoustic meatus. The opening into the fossa is oval with the
long axis oriented mediolaterally. The petromastoid canal is
absent and the subarcuate fossa is distinguished by the presence of a large, wide groove on its anterior border. A sharp and
long crista petrosa is present anterior to the subarcuate fossa
(Fig. 3a). It delineates a wide fossa on the tegmen tympani,
dorsal to the hiatus Fallopii (Fig. 4a). The roughened bone of
the mastoid region and some of the cancellous bone internal to
it are visible in this view, as well as in ventromedial view
J Mammal Evol
Fig. 5 Ventromedial views of the petrosals of (a) Diacodexis ilicis
(AMNH 16141 reversed from right); (b) Acotherulum saturninum
(MNHM Qu 16366); (c) Dichobune leporina (MNHN Qu 16586); (d)
Homacodon vagans (USNM 482369; reversed from right); (e) ?Helohyus
plicodon (USNM 13079; reversed from right); and (f) Gobiohyus
orientalis (USNM 26277; reversed from right). Scale=2 mm for a, b, c,
f and scale=5 mm for d and e
(Fig. 2a). There is no mastoid plate, a thin ledge of bone that
may overhang the subarcuate fossa (see O’Leary 2010; Orliac
2012: fig. 3). This structure, so far identified only in suoids
(Orliac 2012), is not observed in D. ilicis. The cochlear aqueduct is situated at the posterior end of the foramen acusticum
inferius, on the medial surface of the petrosal. It lies in a deep
concavity outlined by a bony ridge. The vestibular aqueduct is
a small aperture, opening in a posterior position, located
medial and posterior to the subarcuate fossa.
The mastoid region consists of two main areas: a ventrally
protruding part that bears a wide vascular groove and a flat
wedge-shaped dorsolateral part (Fig. 2a). The external acoustic meatus lies between these two regions. The ventrally
protruding part of the mastoid region is widely exposed on
the ventral part of the skull, where it is intercalated between
the base of the paracondylar process of the exoccipital and the
posttympanic process of the squamosal. Our in situ reconstruction reveals that part of the flattened, wedge-shaped
dorsal part of the mastoid region is also exposed on the
temporal part of the skull (Fig. 10a). We cannot, however,
eliminate the possibility that this unexpected exposure may be
due to deformation and breakage of the specimen.
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Fig. 6 Ventrolateral views of the petrosals of (a) Dichobune leporina (MNHN Qu 16586); and (b) Homacodon vagans (USNM 482369; reversed from
right). Grey surfaces indicate broken parts of the specimens. Scale=2 mm for a, and scale=5 mm for b
Cebochoeridae: Acotherulum saturninum (Figs. 2b, 3b, 4b,
and 5b; Fig. S2)
The virtual reconstruction of the left petrosal was derived
from the 3D reconstruction of the in situ petrosal of the skull
of Acotherulum saturninum (MNHN Qu 16366) from the
Quercy fissure fillings (S-W France, Paleogene, unknown
locality, BioChroM’97 1997). Right and left petrosals of the
specimen had been previously exposed by removal of the
tympanic bullae (completely removed on the right side, but
half remains on the left). On the ventrolateral surface (Fig. 2b),
the promontorium is an anteroposteriorly elongate ellipsoid
that reveals little evidence of the underlying coiling of the
cochleae. The promontorium gives rise to a large epitympanic
wing, which is fully contiguous with the posteromedial flange
on the promontorium. The anterior extreme of the
epitympanic wing comes to a gentle point. There is a pointed
lateral process of the epitympanic wing that defines the posterolateral edge of the piriform fenestra. The fenestra vestibuli
is an elongate oval and is larger than the fenestra cochleae. The
fenestra cochleae is narrow and opens in a posterior direction.
The promontorium is distinguished by two very distinct
grooves: a single transpromontorial sulcus that extends from
the posteromedial to the anterior aspect of the promontorium,
and a sulcus for the stapedial artery branching from it that
terminates at the medial edge of the fenestra vestibuli. The
transpromontorial sulcus creates a pronounced furrow on the
J Mammal Evol
Fig. 7 Dorsomedial views of the petrosals of (a) Dichobune leporina (MNHN Qu 16586); and (b) Homacodon vagans (USNM 482369; reversed from
right). Scale=2 mm for a, and scale=5 mm for b
medial side of the lateral process of the epitympanic wing. The
sulcus for the stapedial artery is on the promontorium anterior to
the broad crista interfenestralis. The fossa for the tensor tympani
is a broad, shallow depression with indistinct boundaries; it very
gently excavates the tegmen tympani.
On the pars canalicularis, the tegmen tympani is a narrow
shelf that is distinctly separated from the promontorium; it is
only somewhat inflated, occupying approximately one-fourth
of the width of the ventrolateral surface of the petrosal. There
is a very large tegmen tympani canal, located just posterior to
the opening of the hiatus Fallopii (Fig. 4b). The hiatus Fallopii
is a wide opening on the dorsolateral edge of the petrosal,
halfway along the fossa for the tensor tympani. The anterior
process, which terminates in a point, does not extend anterior
to the epitympanic wing. The secondary facial foramen is
directly lateral to the fenestra vestibuli. The epitympanic
recess is an indistinct depression lateral to the secondary facial
foramen, and it lacks a distinct fossa for the head of the
malleus. The fossa incudis cannot be identified. Anterior to
this is the ventrolateral tuberosity, which is a small process.
The petrosal contribution to the external acoustic meatus
forms a shallow, wide trough. The facial sulcus is a distinct
and deep channel extending to the stylomastoid notch; the
stapedial muscle fossa, is not visible, covered by the crista
parotica. The tympanohyal is a small knob located just posterior to the fenestra cochleae. The crista parotica extends from
the posterior aspect of the stylomastoid notch and runs anteriorly between the secondary facial foramen and the
J Mammal Evol
Fig. 8 Ventrolateral views of the petrosals of (a) ?Helohyus plicodon (USNM 13079; reversed from right); and (b) Gobiohyus orientalis (USNM 26277;
reversed from right). Grey surfaces indicate broken parts of the specimens. Scale=5 mm for a, and scale=2 mm for b
epitympanic recess. The caudal tympanic process is an indistinct bump posterior to the fenestra cochleae that is separated
from the posteromedial flange by a notch. The pars cochlearis
does not protrude medially relative to the mastoid region.
The dorsomedial surface of the petrosal (Fig. 3b) is smooth.
The internal acoustic meatus is shallow with the foramen
acusticum superius relatively round and the foramen
acusticum inferius more elongate and broad. These openings
are separated by a distinct, ridge-shaped crista transversa.
There is no prefacial commissure fossa and the tegmen tympani meets the dorsomedial surface of the petrosal at a right
angle. The basicapsular groove is present and visible on the
dorsomedial surface extending just anterior to the minute
opening for the cochlear aqueduct. The cochlear aqueduct is
situated ventromedial to the foramen acusticum inferius. The
small opening of the vestibular aqueduct is situated in a dorsal
depression, located medial and posterior to the subarcuate
fossa. A distinct ridge defines the ventromedial border of
the deep and oval-shaped subarcuate fossa. The subarcuate
fossa shelters a petromastoid canal (out of view in Fig. 3b).
There is no crista petrosa and no pronounced tegmen tympani fossa.
The mastoid region tapers posteriorly and then fans into an
irregular, roughened area. A mastoid plate is absent. The
J Mammal Evol
Fig. 9 Dorsomedial views of the petrosals of (a) ?Helohyus plicodon (USNM 13079; reversed from right); and (b) Gobiohyus orientalis (USNM 26277;
reversed from right). Scale=5 mm for a, and scale=2 mm for b
mastoid region represents approximately half of the total size
of the petrosal. The mastoid region is also visible on the lateral
aspect of the skull ventrally near the base of the paracondylar
process of the exoccipital, just posterior to the opening of the
external auditory meatus. The flattened, wedged-shaped dorsal part of the mastoid region is not exposed on the temporal
part of the skull.
Dichobunidae: Dichobune leporina (Figs. 4c, 5c, 6a, and
7a; Fig. S3)
The petrosal of a representative species of Dichobunidae is
described here from the virtual reconstruction of the right in
situ petrosal of Dichobune leporina (MNHN Qu 16366) from
the Quercy fissure fillings (S-W France, Paleogene, unknown
locality). The tympanic bullae are missing on both sides.
J Mammal Evol
The promontorium (Fig. 6a) is oval in outline shape and is
relatively flat except immediately anterior to the fenestra cochleae where it is convex. The promontorium lacks
transpromontorial and stapedial sulci. At the anterior aspect of
the promontorium, between the epitympanic wing and the
lateral process of the epitympanic wing, are two depressions
of relatively equal size. Posteriorly, the fenestra vestibuli is oval
and separated by a wide crista interfenestralis from the larger
fenestra cochleae, which has a round outline. The outline of the
fenestra cochleae is weakly defined at the posteromedial margin. The fossa for the tensor tympani is a large, wide trough that
has a poorly defined anterior margin. The hiatus Fallopii is a
very small pit situated just anterior to the anterior margin of the
fossa for the tensor tympani on the anterolateral edge of the
petrosal. There is a large epitympanic wing extending anteriorly
from the fossa for the tensor tympani; this wing comes to a
sharp point anteriorly. The epitympanic wing also has a sharp
lateral process that defines the posterolateral edge of the
piriform fenestra. The posterior border of the piriform fenestra
is a distinct concavity in the petrosal. The epitympanic wing is
fully continuous with the posteromedial flange. The caudal
tympanic process is an unremarkable knob posterior to the
fenestra cochleae. A sharp crista parotica runs from the
posteromedial extreme of the bone along the medial edge of
the tegmen tympani as a distinct, unbroken ridge.
The tegmen tympani is a modest shelf of bone with a small,
knob-shaped ventrolateral tuberosity. The anterior process of
the tegmen tympani is small and blunt. The tegmen tympani
canal is a small but distinct opening. The contribution of the
petrosal to the external acoustic meatus is limited to a shallow
and wide trough; the epitympanic recess is very indistinct. The
secondary facial foramen is a slit that is anterolateral to the
fenestra cochleae (and thus relatively anterior in position). It
opens onto a wide and distinctive facial sulcus that is continuous with the posterior margin of the fenestra cochleae. The
tympanohyal cannot be identified on the mastoid region and is
either broken or absent. The stapedial muscle fossa is wide
and deep, its medial margin is not defined. The mastoid region
is wedge-shaped and roughened. The epitympanic recess is an
unremarkable depression that lacks a distinct fossa for the
head of the malleus. The fossa incudis cannot be identified.
The smooth dorsomedial surface (Fig. 7a) has a rather small
internal acoustic meatus with relatively poorly defined borders.
The foramina acusticum superius and inferius are small, oval,
and of approximately equal size. They are distinctly separated
by a crista transversa. The basicapsular groove is very conspicuous in this view and runs from the anterior extreme of the bone
to the mastoid region. The cochlear and vestibular aqueducts
are located within very small pits, and are positioned more
posteriorly than is the internal acoustic meatus. The vestibular
aqueduct is located in a relatively dorsal position, in a small
depression, superior to the posterior margin of the subarcuate
fossa. The internal acoustic meatus is well-separated from the
deep and wide subarcuate fossa, a depression that is larger and
deeper than the internal acoustic meatus. The posterolateral
edge of the subarcuate fossa is marked by a clear groove, and
a petromastoid canal is present. The tegmen tympani meets the
dorsolateral surface at a right angle (Fig. 4c) and the prefacial
commissure fossa is absent. A short crista petrosa is present
anterior to the subarcuate fossa (Fig. 7a). It delineates a small
fossa, dorsal to the hiatus Fallopii (Fig. 4c). The mastoid region
occupies almost half of the volume of the petrosal and the
cancellous bone that comprises it is partly visible (Figs. 5c
and 7a). A mastoid plate is absent. The mastoid region is visible
on the ventral surface of the skull anterior to the base of the
paracondylar process of the exoccipital. The mastoid region is
not exposed on the temporal surface of the cranium.
Homacodontidae: Homacodon vagans (Figs. 1, 4d, 5d, 6b,
7b, and 10a; Figs. S4, S11)
The petrosal of a representative member of the
Homacodontidae is described here from the virtual reconstruction of the left in situ petrosal of Homacodon vagans (USNM
482369). It was collected by Frank L. Pearce in 1941 from the
Bridger D Formation, locality “Bridger Basin, 100–150 ft above
white layer of S Twin Buttes, Wy [sic].” It has some breakage
just anterior to the fenestrae cochleae and vestibuli, visible in the
reconstructed specimen. The tympanic bullae are not preserved.
The promontorium is mostly flat and is oval in outline. We
interpret this specimen to have both transpromontorial and
stapedial sulci as these sulci are observable on the in situ left
petrosal (not reconstructed). The fenestra cochleae is much
larger than the fenestra vestibuli. The crista interfenestralis
created a substantial separation between these openings; however, due to breakage the full size of this crest cannot be
observed. The fossa for the tensor tympani is a large, wide,
and well-defined ovoid depression. There is a large
epitympanic wing that comes to a point anteriorly. The
epitympanic wing is fully connected to the posteromedial
flange forming a complete lip around the promontorium.
The specimen has a large and pointed lateral process of the
epitympanic wing that defines a distinct piriform fenestra. The
hiatus Fallopii is oval and opens dorsally, slightly posterior to
the anterior margin of the fossa for the tensor tympani.
The tegmen tympani is mediolaterally narrow, terminating
in a small, spike-shaped anterior process. The tegmen tympani
canal is a narrow passage with a small opening that is closer to
the ventral than to the dorsal surface of the bone (Fig. 4d). The
ventrolateral tuberosity is a small knob. The contribution of
the petrosal to the external acoustic meatus is a shallow,
narrow but deep trough. The epitympanic recess is an indistinct structure that is offset ventrally from the level of the facial
sulcus; a very subtle depression could correspond to the fossa
incudis. The secondary facial foramen is a small slit that is
anterolateral to the fenestra vestibuli, and that opens onto a
wide and shallow facial sulcus. The crista parotica is a
J Mammal Evol
distinctive, continuous ridge from the anterior process of the
tegmen to the stylomastoid notch. There is a small caudal
tympanic process. The tympanohyal is broken on the reconstructed petrosal but can easily be seen on the other side of the
skull where it consists of a small knob located just posterior to
the fenestra cochleae. It almost closes off the anterior margin
of the stylomastoid foramen as on the specimen illustrated by
Coombs and Coombs (1982:fig. 1). The mastoid region is
large and wedge-shaped comprising over half of the total size
of the bone (Figs. 4, 5, 6b, and 7); its cancellous structure is
visible in several figures.
The dorsomedial surface of the petrosal (Fig. 7b) is smooth.
The internal acoustic meatus is poorly defined; both the foramina acusticum superius and inferius are oval in outline and
separated by only a narrow crista transversa. The basicapsular
groove is very wide and distinct, running from the anterior
extreme of the bone to the mastoid region. The cochlear and
vestibular aqueducts are small oval pits, both hidden under
Fig. 10 Coronal (left column) and lateral (right column) views of the right
ear region and skull showing dorsal exposure of the mastoid region: (a)
Diacodexis ilicis (AMNH 16141), reversed from left, (b) Homacodon
vagans (USNM 482369), reversed from left; and (c) ?Helohyus plicodon
(USNM 13079), reversed from left. Double-headed arrows indicate the
location of the coronal section in the 3D reconstruction. Scale=10 mm
J Mammal Evol
flanges of bone. The cochlear aqueduct is situated posterior to
the posterior margin of the foramen acusticus inferius, and the
vestibular aqueduct is more posterior, as posterior as the
posterior margin of the subarcuate fossa. The internal acoustic
meatus is separated from the subarcuate fossa by a wide bar of
bone. The subarcuate fossa is deep and wide; it is broadly
open on the posterodorsal extreme and contains a wide
petromastoid canal (out of view in Fig. 7b). The tegmen
tympani is perpendicular to the dorsomedial surface of the
petrosal and there is no prefacial commissure fossa. A crista
petrosa is present anterior to the subarcuate fossa (Fig. 7b) and
delineates a wide fossa on the tegmen tympani, dorsal to the
hiatus Fallopii (Fig. 4d). A mastoid plate is absent.
The mastoid region is widely exposed on the external
surface of the skull (Fig. 10a), particularly on the ventral
surface, where it intercalates between the base of the
paracondylar process of the exoccipital and the posttympanic
process of the squamosal (Fig. 1d). The mastoid region is also
visible in lateral view, and its dorsal part is also widely
exposed on the temporal surface of the skull situated between
the parietal of the occipital bones (Fig. 10a).
Helohyidae: ?Helohyus plicodon (Figs. 4e, 5e, 8a, 9a, 10b;
Figs. S5, S12)
The petrosal of ?Helohyus plicodon is described here from
the virtual reconstruction of the right in situ petrosal of the
specimen AMNH 13079 from the Bridger Formation locality
B5, Sweetwater County, Wyoming. Only the ventrolateral
surface of this specimen was previously described by Coombs
and Coombs (1982). Sinclair (1914) tentatively referred this
partial skull to Helohyus. The specimen has a broken posterior
tooth row, and this taxonomic assignment is based on the size
of the specimen and on an associated P3. Coombs and
Coombs (1982) noted the specimen’s potential affinities with
Lophiohyus, another helohyid, and thus referred to this specimen to as ?Helohyus. In the absence of any new information,
we follow Coombs and Coombs (1982) here.
The promontorium is circular in outline and slightly bulging. Sulci on the promontorium are faint but can be seen in the
CT scan. The transpromontorial sulcus makes an almost right
angle bend anterior to the fenestra cochleae, where it gives rise
to a sulcus for the stapedial artery that is equally wide. The
fenestra cochleae is much larger and more oval than is the
fenestra vestibuli. The fossa for the tensor tympani is a very
shallow and low depression. The epitympanic wing and
posteromedial flange form the anterior and medial periphery
of the promontorium but their separations from it are indistinct. The tegmen tympani is mediolaterally broad (about half
the width of the promontorium); the anterior process of the
tegmen tympani is blunt and short. There is a small tegmen
tympani canal, opening lateral to the fenestra vestibuli and
visible in lateral view (Fig. 4e). A very modest lateral process
of the epitympanic wing lies anteromedial to the tegmen
tympani. The ventrolateral process of the tegmen tympani is
absent. The hiatus Fallopii is a small hole oriented dorsally
(Fig. 4). The location of the secondary facial foramen is
difficult to determine because the floor of the fossa for the
tensor tympani muscle is partly broken. The foramen appears
to be positioned relatively far anteriorly, but this may be due to
it being broken through to the dorsal side. The facial sulcus is
a deep and distinct channel. The stapedial muscle fossa is not
well preserved and has a crack running through it. The caudal
tympanic process is a small knob posterior to the fenestra
cochleae. The tympanohyal cannot be identified on the mastoid region and may either be broken or absent. The mastoid
region is large and wedge-shaped (Figs. 4 and 5) and exhibits
cancellous bone (Fig. 5). The epitympanic recess is a wide
indistinct depression that lacks a distinct fossa for the head of
the malleus. The fossa incudis cannot be identified.
In dorsomedial view (Fig. 9a) the surface of the bone is
completely smooth; the internal acoustic meatus is roughly
oval in outline shape. The foramen acusticum superius is oval
and narrow and the foramen acusticum inferius is larger and
round. The crista transversa forms a wide separation between
these two openings. The basicapsular groove is continuous
from anteromedial to posteromedial and does not extend
posterior to the internal acoustic meatus. The subarcuate fossa
is set off from the internal acoustic meatus by a wide bar of
bone; the fossa itself is extremely shallow and wide, and it is
relatively expanded anteriorly. A petromastoid canal occurs at
the deepest part of the fossa. The tegmen tympani is perpendicular to the dorsomedial surface and a prefacial commissure
fossa is absent. A very short crista petrosa is present anterior to
the subarcuate fossa and joins the anteromedial tuberosity of
the petrosal anteriorly (Fig. 9a). There is no indication of a
tegmen tympani fossa. The cochlear aqueduct is a minute
opening within a rounded pit that is situated directly posterior
to the foramen acusticum inferius. The vestibular aqueduct
lies more posteriorly and dorsally, nearer the posterior margin
of the subarcuate fossa. A mastoid plate is absent.
The mastoid region is widely exposed on the external surface
of the skull (Fig. 10a). This exposure consists of two parts: a
ventral protrusion that bears a wide sulcus, and a flat, wedgeshaped dorsolateral part. The ventrally protruding part of the
mastoid region is the widest area of external exposure and it
intercalates between the paracondylar process of the exoccipital
and the posttympanic process of the squamosal. The more dorsal
part of the mastoid region that is exposed on the temporal part of
the skull intercalates between the parietal and occipital bones.
Helohyidae?: Gobiohyus orientalis (Figs. 4f, 5f, 8b, and
9b; Figs. S6, S13)
The petrosal of Gobiohyus orientalis is described here from
the virtual reconstruction of the right in situ petrosal of the
specimen AMNH 26277 from Inner Mongolia (Ulan Shireh
Formation, Chimney Butte North Mesa, Shara Murun region).
J Mammal Evol
The specimen consists of a skull (the only one that has ever been
reported) and dentition. The ventrolateral surface of the right
petrosal is exposed and the dorsomedial surface has been prepared and is partially exposed (the right petrosal is only partially
preserved). This view of the petrosal has been described previously in Coombs and Coombs (1982), and we include here new
details visible from the CT scans. The tympanic bullae are not
preserved. There are a few breaks in the promontorium anterior
to the fenestra cochleae but the bone is generally intact.
The promontorium is almost circular to square in outline
shape. It is surrounded by an epitympanic wing and a
posteromedial flange that are fully contiguous. The lateral process of the epitympanic wing is a short prong that marks the
lateral edge of the piriform fenestra. The transpromontorial
sulcus is very shallow and stapedial sulus is not conspicuous.
The fenestra vestibuli is round and only slightly smaller than the
oval fenestra cochleae. The two are separated by a crista
interfenestralis that was as wide as the fenestra cochleae. The
fossa for the tensor tympani muscle shows some breakage but is
preserved adequately to show that it was a distinct, large, and
oval depression lateral to the secondary facial foramen. This
fossa extensively excavates the tegmen tympani. The hiatus
Fallopii is very wide and is located anterior to the anterior
margin of the fossa for the tensor tympani. This margin is
broken, creating an artificial union between the hiatus Fallopii
and the facial sulcus. The secondary facial foramen appears to
have been located in a relatively anterior position in comparison
to the promontorium. The facial sulcus is a long trough that
passes lateral to the fenestra vestibuli and medial and posterior to
the stapedial muscle fossa. The tegmen tympani is a narrow bar
of bone that terminates in a blunt anterior process. The external
acoustic meatus is deep and very wide and the epitympanic
recess is indistinct. The fossa incudis cannot be identified with
certainty, but a very subtle depression could correspond to this
fossa. The ventrolateral tuberosity is an indistinct knob anterior
to the external acoustic meatus. A very small tegmen tympani
canal appears approximately halfway between the ventral and
dorsal surfaces of the petrosal; it perforates the tegmen tympani
lateral to the fenestra vestibuli and opens on its lateral surface
through a small foramen (Fig. 4e). Coombs and Coombs
(1982:225) described a slight development of a tympanohyal
on the mastoid region of Gobiohyus. We could not identify this
structure; it may have been broken subsequent to their paper or
is absent. The crista parotica is a sharp ridge that extends fully
medial to the external acoustic meatus and terminates posterior
to the estimated location of the stylomastoid notch. The mastoid
region is large and wedge-shaped. The caudal tympanic process
is fully continuous with the posteromedial flange and forms a
low shelf posterior to the fenestra cochleae.
The dorsomedial surface of the petrosal is completely smooth
with a deep internal acoustic meatus that has an irregular margin.
The prefacial commissure fossa is absent. The crista transversa is
broken making the distinction between the foramen acusticum
superius and inferius unclear. The basicapsular groove is most
clearly defined at its anterior extreme. It is identifiable, but not
well defined, posteriorly. The cochlear aqueduct is a small opening in a slit posteromedial to the internal acoustic meatus. The
vestibular aqueduct is situated more dorsally and is posterior to
both the internal acoustic meatus and the subarcuate fossa.
Separating the internal acoustic meatus from the subarcuate fossa
is a wide ridge of bone. The subarcuate fossa is deep; however, it
is poorly defined on its dorsolateral margin where it becomes
shallower. It is separated from a thin flange of bone by a groove.
The subarcuate fossa shelters a clear petromastoid canal (out of
view in Fig. 9b). There is no crista petrosa and no contact with
the cerebrum on the tegmen tympani.
A mastoid plate is absent. The mastoid region consists of two
main areas: a ventrally protruding part that bears a wide sulcus
and a dorsolateral part that is a flat wedge. These are separated
by the external acoustic meatus. The ventrally protruding part of
the mastoid region is widely exposed on the ventral part of the
skull, where it is intercalated between the base of the
paracondylar process of the exoccipital (structure not preserved
on specimen) and the posttympanic process of the squamosal.
Anatomical Comparison and Character States
Below we compare the anatomy of the petrosal bone among
dichobunoids and other mammals and make brief remarks
about the hypothesized soft tissue contents of certain bony
features. We also review relevant character states previously
published for basal Artiodactyla based on data available from
the literature. Remarkable characters and their hypothesized
polarities are here discussed in the current context of an
unstable phylogeny for dichobunoids (e.g., Spaulding et al.
2009; Geisler and Theodor 2009). The distribution of the
discrete characters discussed bellow among dichobunoid taxa
is summarized in Table 1.
Promontorium Shape and Vascular Grooves
Each of the dichobunoids studied here has an elongate
promontorium that is round-oval in outline, like that of many
terrestrial artiodactyls (O’Leary 2010). The promontoria of the
dichobunids are relatively flat whereas those of cetaceans are
relatively bulbous (Luo and Gingerich 1999; O’Leary 2010).
Several of the promontoria described here exhibit both
transpromontorial and stapedial sulci arranged at a right angle.
The petrosal of Dichobune is devoid of such sulci (Fig. 6). The
grooves are particularly pronounced in the cebochoerid
Acotherulum (Fig. 2b) where they deeply excavate the
promontorium. Within crown Artiodactyla, a transpromontorial
groove has been reported in each of its major extant subclades
(suines, hippopotamids, ruminants, and camelids), either within
the subclades themselves, or on their stems, or both (O’Leary
J Mammal Evol
Table 1 Comparative morphological features of the dichobunoid species in this study
Diacodexis
Dichobune
Acotherulum
Homacodon
Gobiohyus
?Helohyus
tps
lpew
ftt
tts
aptt
cp
amt
ttc
ttf
hfs
demr
sf
+
+
?
+
+
+
+
+
+
+
small
+
+
+
+
+
+
+
+
+
+
+
+
+
-
+
+
+
+
+
+
+
+
+
+
+
-
+
-
+
+
?
+
+
+
+
+
+
-
Abbreviations: amt anteromedial tuberosity; apt anterior process of tegmen tympani; cp crista petrosa; demr dorsal exposure of mastoid region; ftt fossa
for tensor tympani excavating the tegmen tympani; hfs hiatus Fallopii size; lpew lateral process of the epitympanic wing; sf subarcuate fossa; tps
transpromontorial sulcus; ttc tegmen tympani canal; ttf tegmen tympani fossa; tts tegmen tympani size
2010). Unambiguous transpromontorial grooves in Diacodexis
and Acotherulum shown here indicate that this bony feature also
characterized the oldest fossils to have been referred to
Artiodactyla. Future comprehensive phylogenetic work testing
the positions of these taxa will be crucial for determining
whether these ancient taxa are also the most basal, and whether,
as hypothesized by Wible (1986), the presence of these grooves
is the primitive condition for both Artiodactyla and
Artiodactylamorpha.
Whether the presence of promontorial grooves necessarily
implies the presence of a transpromontorial internal carotid
artery and/or nerve, or the stapedial artery requires further
description of soft tissue data from dissections and the incorporation of these data directly into the phylogenetic analysis
for optimization of both types of characters (Bryant and Russell 1992; Witmer 1995; O’Leary et al. 2013). This work will
be particularly important given that Artiodactyla is a clade for
which loss or reduction of the internal carotid artery has been
reported (reviewed in Geisler and Luo 1998; O’Leary 2010),
making the clade an interesting test case for how osteological
and soft anatomy co-evolve.
Flanges Extending from the Promontorium
All of the species examined here have flanges extending from
the promontorium as reported in many other terrestrial artiodactyls (O’Leary 2010). These include both the epitympanic
wing and the posteromedial flange. These structures are continuous in all of these species but vary in width from relatively
narrow in Diacodexis (Fig. 2a) and Dichobune (Fig. 6a) to
wider in Gobiohyus (Fig. 8b). The epitympanic wing typically
forms a sharp point anteriorly in Dichobune, Homacodon,
Acotherulum, and particularly in Diacodexis. Lateral to the
point is the lateral process of the epitympanic wing. These
taxa also lack a separate carotid foramen. This process, which
is present in all of the taxa examined here, and is particularly
sharp in Dichobune, Homacodon, and Acotherulum, has not
previously been identified in extant or fossil artiodactyls (e.g.,
Geisler and Luo 1998; Theodor 2010; O’Leary 2010), except
in the basal suoids Perchoerus and Palaeochoerus (= lateral
anterior process, Orliac 2012). As noted above, the lateral
process of the epitympanic wing delineates the posterior and
lateral edges of the piriform fenestra (this fenestra is clearly
separated from the foramen ovale in dichobunoids;
Dechaseaux 1969; Coombs and Coombs 1982; Russell et al.
1983). In ?Helohyus, the posterior margin of the piriform
fenestra indents only slightly into the pars cochlearis, and, as
such, the lateral process of the epitympanic wing is limited to a
small blunt spike. Overall the morphology of this region
differs most substantially in ?Helohyus, in which the anterior
edge of the epitympanic wing is rounded, without a pointed
process. The lateral process of the epitympanic wing has not
been reported in “condylarthran” ungulates, and is absent in
Protungulatum (MacIntyre 1972; O’Leary 2010),
Meniscotherium (Gazin 1965), Hyopsodus (Cifelli 1982),
Pleuraspidotherium and Orthaspidotherium (Ladevèze et al.
2010). Among euungulates (Asher et al. 2009), a lateral
process of the epitympanic wing has so far only been observed
in Artiodactyla. In the fetal stage of living eutherians, an
alicochlear commissure separates the carotid foramen from
the piriform fenestra (MacPhee 1981: 21 and fig. 1). This
commissure can be replaced in the adult by an expansion of
the petrosal, which ensures the complete separation between
the carotid foramen and the piriform fenestra (e.g., in
Carnivora, Wang and Tedford 1994). In the species described in this paper there is no separate carotid foramen,
a condition that has been described in other extinct artiodactyls and relatives (see Geisler and Luo 1998), and the
transpromontorial branch of the internal carotid artery
may have entered the cranial cavity via the piriform
fenestra (Geisler and Luo 1998).
Fossa for the Tensor Tympani
All the dichobunoids described here present a clearly delimited
fossa for the tensor tympani on the ventromedial surface of the
petrosal, anterior to the fenestra vestibuli. Diacodexis shows a
wide and shallow fossa for the tensor tympani muscle;
J Mammal Evol
however, this fossa does not form an excavation into the tegmen
tympani as reported in some artiodatyls (O’Leary 2010). The
fossa is particularly wide in ?Helohyus and Gobiohyus (Fig. 9)
and deeply excavates the tegmen tympani.
sensu Billet and Muizon (2013) and most probably received
part of the temporal lobe of the cerebrum and the trigeminal
ganglion of the trigeminal nerve (V).
Tegmen Tympani Canal
Tegmen Tympani
The tegmen tympani is a distinct, continuous shelf on the
lateral aspect of the pars canalicularis of the petrosal and is
continuous with the mastoid region in euungulates (Luo and
Gingerich 1999; O’Leary 2010). In the taxa studied here the
tegmen tympani is typically narrow relative to the width of the
promontorium, an important exception being ?Helohyus,
which has the widest tegmen tympani (Fig. 8a). In Diacodexis,
the tegmen tympani is relatively small consisting only of a thin
strut of bone.
Anterior Process of the Tegmen Tympani
All extant and fossil artiodactyls described in the literature so
far exhibit an anterior process of the tegmen tympani (when
this area is preserved). The anterior process of the tegmen
tympani of dichobunoid taxa is relatively modest in size and
blunt in shape. O’Leary (2010) reported the presence of this
feature as a synapomorphy of a clade of Artiodactyla+
mesonychians based on the phylogenetic analysis of O’Leary
and Gatesy (2008). Those authors did not record a score for
this feature for either species of Diacodexis that they studied
because the feature could not be assessed from the available
data. We find that an anterior process of the tegmen tympani
is, however, absent in North American Diacodexis, indicating
that the character does show some variability, at least among
extinct taxa that have been assigned to Artiodactyla. Should
future phylogenetic studies corroborate the highly nested position of Diacodexis found in Spaulding et al. (2009), the
absence of this feature would optimize as a reversal. This
process is also absent in “condylarthran” ungulates such as
Protungulatum sp. (O’Leary 2010:fig. 3), Meniscotherium
(Cifelli 1982), and Hyopsodus (Gazin 1965), but is present
in Orthaspidotherium (Ladevèze et al. 2010).
Tegmen Tympani Fossa
In Diacodexis, the tegmen tympani is excavated by a wide
fossa, located dorsal to the hiatus Fallopii and separated from
the subarcuate fossa by a sharp crista petrosa (Fig. 4a). This
fossa is also present in Dichobune (Fig. 4c) and Homacodon
(Figs. 1b and 4d), but is smaller and shallower than in
Diacodexis. Acotherulum (Fig. 4b), Gobiohyus (Fig. 4e), and
?Helohyus (Fig. 4f) do not present this fossa. The tegmen
tympani fossa is located lateral and anterior to the crista
petrosa and is directed towards the cerebral cavity. This area
likely corresponds in part to the fossa for trigeminal ganglion
In all species described here, the tegmen tympani is perforated
by a canal, the tegmen tympani canal (new term, this study).
This passageway pierces the tegmen tympani from the ventrolateral surface of the petrosal adjacent to the secondary
facial foramen, and opens onto its anterolateral surface
(Fig. 4). The canal connects anteriorly to the orbitotemporal
canal (Fig. S14). We have separately observed, but do not
figure, that the tegmen tympani canal exists in Bunomeryx
(AMNH 2070, Homacodontidae), and in the European Eocene artiodactyls Mouillacitherium (UM2 ACQ 6625,
Hyperdichobuninae), and Cainotherium (UM2 PDS 3352).
Dechaseaux (1974) and Coombs and Coombs (1982) also
did not report the presence of this canal in the dichobunoid
taxa they studied, and, with the exception of the five genera
examined here, no other artiodactyls for which the petrosal is
known has been described as having such a canal (e.g., Geisler
and Luo 1998; Luo and Gingerich 1999; O’Leary 2010). The
most similar structure is what Geisler and Luo (1998: fig. 2)
identified in some extinct artiodactyls as the stapedial foramen, but that structure lies between the petrosal and the
squamosal. Those authors also identified a stapedial foramen
in the archaeocetes Pakicetus, Basilosaurus, and Dorudon. A
tegmen tympani canal for the ramus superior of the stapedial
artery has also been identified in the ‘condylarths’
pleuraspidotheriids (Ladevèze et al. 2010) and in notungulates
(Billet and Muizon 2013).
The orbitotemporal canal has been reported to transmit the
anterior division of the ramus superior of the stapedial artery into
the orbit (Wible and Gaudin 2004:162). It is possible that the
tegmen tympani canal, connected to the orbitotemporal canal,
gave passage to the ramus superior of the stapedial artery in life.
This soft tissue – osteology correlation would also be consistent
with the presence of a stapedial sulcus observed in these taxa.
A tegmen tympani canal is absent in some of the most
ancient taxa that may be members of or on the stem to crown
clades within Artiodactyla: Suoidea (Perchoerus, Orliac
2012), Ruminantiamorpha (Leptomeryx AMNH 53596),
Hippotamidamorpha (Heptacodon AMNH 12462). A canal
for the ramus superior of the stapedial artery passing through
the petrosal or petrosal/squamosal suture on dorsolateral edge
of epitympanic recess is considered to be plesiomorphic for
Artiodactyla and Perissodactyla (Ladevèze et al. 2010: character 11) and is, for example, present in the “condylarths”
Pleuraspidotherium and Orthaspidotherium (Ladevèze et al.
2010). Loss of the tegmen tympani canal would therefore be
derived among Artiodactyla and might have occurred several
times in artiodactyl evolution.
J Mammal Evol
Hiatus Fallopii
Although out of view in the illustrations except from the
ventromedial view in Fig. 5, the hiatus Fallopii is typically a
very small opening at the anterior edge of the tegmen tympani
in all the species we examined (e.g., Fig. 1b). Only one of the
taxa studied, Acotherulum, has an enlarged (relative to the
total size of the petrosal) hiatus such as is found in
hippopotamids and cetaceans (O’Leary 2010).
Epitympanic Recess
The epitympanic recess in the taxa described here is similar to that
described in many terrestrial artiodactyls (O’Leary 2010), in that it
is ventrally offset relative to the facial sulcus. The recess is also an
indistinct and shallow basin. None of the early artiodactyls studied
here exhibits a distinct fossa for head of malleus as seen in
cetaceans. The fossa incudis can not be identified with certainty
on any of the 3D reconstructions, but a very subtle depression
could correspond to this fossa in Homacodon and Gobiohyus.
Mastoid Region, Including Exposure
The mastoid region is relatively large in all dichobunoids
represented in this study. The proportion of the mastoid region
compared to the total size of the petrosal is about the same in
Diacodexis, Dichobune, and Acotherulum. Homacodon and
?Helohyus present a relatively greater development of the
dorsal part of the mastoid region such that it accounts for
more than half of the total size of the bone. In all
dichobunoids, the mastoid region is broadly exposed on the
ventral part of the skull at the base of the paracondylar process
of the exoccipital. This region is also visible in lateral view,
anterior to the paracondylar process, as described by Russell
et al. (1983) in D. pakistanensis. More surprisingly, however,
is that the mastoid region is also widely exposed on the
temporal part of the skull and the dorsal portion of the bone
is intercalated between the parietal and the occipital bones in
Homacodon (Fig. 10b) and ?Helohyus (Fig. 10c). In
Diacodexis (Fig. 10a), the mastoid region is also exposed on
the temporal side; however, given the postmortem deformation of this specimen, it is uncertain whether this exposure is
artifactual or real. The morphology of this area is also not clear
in Dichobune, but if this region were exposed at all, it is likely the
exposure would have been very small. We did not observe this
exposure in the cebochoerids Acotherulum (MNHN Qu 16366)
and Cebochoerus (MNHN Qu 17151), and, to our knowledge,
this exposure has not been reported in other euungulates.
Basicapsular Groove
The basicapsular groove is present in all dichobunoids described
here, extending from the medial edge of the bone to the base of
the lateral process of the epitympanic wing. The groove is wholly
situated on the dorsomedial surface of the bone as is found in the
majority of terrestrial artiodactyls described so far (O’Leary
2010). This is in contrast to a more ventral position reported in
Moschus, extant hippopotamids, Babyroussa, and Bothriogenys
(O’Leary 2010). Various positions of this groove (hypothesized
to house the inferior petrosal sinus, Presley 1979) relative to the
basioccipital bone have been described within Artiodactyla (for
review see Theodor 2010:fig. 4, “petrobasiliar canal”). For the
dichobunoid species described here, with the exception of
Gobiohyus, the location is similar to that described for
Cainotherium (Theodor 2010:fig. 3c). The hypothesized primitive condition for artiodactyls - a dorsally positioned groove
(O’Leary 2010) - is confirmed here, and a ventral location of
the basicapsular groove appears to be a derived condition that
may appear several times.
Crista Petrosa
A sharp and long crista petrosa occurs in Diacodexis, where it
delineates the tegmen tympani fossa medially (Fig. 1c). The
crista petrosa is also present in Homacodon (Figs. 1b and 4d)
and Dichobune (Fig. 4c), but shorter and not as sharp as in
Diacodexis. A shorter crista petrosa occurs in Gobiohyus
(Fig. 4e), one that extends anteriorly to the anteromedial
tuberosity of the petrosal. The crista petrosa is absent in
Acotherulum (Fig. 4b) and ?Helohyus (Fig. 4f). In the studied
sample, the presence of the crista petrosa co-occurs with the
presence of a tegmen tympani fossa.
O’Leary (2010) did not identify the crista petrosa as a
particularly significant anatomical feature in the sample of
Artiodactyla she described, and similarly Mead and Fordyce
(2009) noted that this feature was typically absent in cetaceans. In extant artiodactyls the crista petrosa and the fossa on
the tegmen tympani are variously present and have been
hypothesized to coincide with a weak development of the
tentorial crest (Mead and Fordyce 2009; e.g., Ruminantia,
Antilocapra, illustrated by O’Leary 2010: fig. 2a). A sharp
crista petrosa has been separately observed in some
“condylarthrans” that may be closely related to Artiodactyla:
Protungulatum (as visible on fig. 5 of O’Leary 2010: not
labeled); Orthaspidotherium (Ladevèze et al. 2010: fig. 5).
Subarcuate Fossa
As noted above in other features, Acotherulum and Dichobune
present a morphology very close to that of Diacodexis, in
having a relatively deep and sharply defined subarcuate fossa.
By contrast, Homacodon has a relatively small subarcuate
fossa. The subarcuate fossa is completely open and shallow
in ?Helohyus. With the exception of Diacodexis, the
petromastoid canal (originally described by Gannon et al.
1988) is observed in all dichobunoid taxa of this study, even
J Mammal Evol
in species that have a very shallow subarcuate fossa
(?Helohyus, Gobiohyus; Fig. 9). The presence of a
petromastoid canal has been proposed to have appeared
convergently several times within Artiodactyla (O’Leary
2010). Its occurrence in all dichobunoid taxa of this study
except Diacodexis opens the possibility that more taxonomically comprehensive phylogenetic studies may show that this
feature is primitive for Artiodactyla.
Conclusions
Dichobunoids are a paraphyletic assemblage of fossil taxa
(Geisler et al. 2007; Spaulding et al. 2009; Gatesy et al. 2012)
distributed in Eocene rocks over North America, Europe, and
Asia that are either members of crown Artiodactyla or are on
the stem to this clade. Our study shows that the petrosal
morphology of these Eocene artiodactyls differs in several
important ways from what has been observed in modern species. For the characters described here in five dichobunoid
species, Diacodexis has more in common with Homacodon
than with any other taxon, and ?Helohyus represents the most
morphologically divergent taxon in these features. The
dichobunoid species of our study share features that, to our
knowledge, have not been observed in extant representatives of
Artiodactyla: a lateral process of the epitympanic wing bordering the posterolateral border of the piriform fenestra, and a
tegmen tympani canal. These characters are, however, observed
in fossil representatives of other artiodactyl families and may be
shown to be plesiomophic for Artiodactyla. Some of the species
of this study (Diacodexis, Homacodon, and ?Helohyus) exhibit
a dorsolateral exposure of the mastoid region of the petrosal on
the temporal part of the cranium. This rare morphology has, to
our knowledge, not been reported in another ungulate group.
Given the current lack of resolution at the base of the artiodactyl
tree, the distribution of this character must be determined in
future comprehensive phylogenetic studies. Documenting
morphotypes of the earliest artiodactyl species such as described here is crucial to improving the quality of hypotheses
of homology between structures of morphologically distant
taxa, and helps explain the morphology of extant taxa. Some
or all of these species have been hypothesized to be basal to
crown Artiodactyla, and, as such, integrating their anatomy into
taxonomically broad phylogenetic studies will be essential for
characterizing the basal morphotype of Artiodactyla.
Acknowledgement We thank R. O’Leary (AMNH), Meng Jin
(AMNH), C. Argot (MNHN), and B. Marandat (UM2) for access to the
collections, J. Thostenson, R. Rudolph, and M. Hill for acquisition of raw
CT data at the AMNH, and A-L Charruault and R. Lebrun for acquisition
of raw CT scan data at the UM2. We are grateful to J Wible, J Geisler, and
one anonymous reviewer for their enriching comments on earlier versions
of the manuscript. We also thank the American Museum of Natural
History for use of the high resolution CT-scanner (NSF MR1–R2
0959384 to N. Landman, D. Ebel, and D. Frost), and the Montpellier
Rio Imaging platform (Montpellier, France) for use of their Skyscan
machine. This is ISE-M publication 201X-XX. This research was supported by the ANR funding project Palasiafrica, headed by L. Marivaux.
Appendix 1
Table 2 Museum accession numbers and scanning parameters of the specimens included in this study
Family
Taxon
Specimen number CT scan institution Specimen side Voxel size (μm) Number of slices File size
Dichobunidae
Homacodontidae
Helohyidae
?Helohyidae
Diacodexeidae
Cebochoeridae
Dichobune leporina
Homacodon vagans
?Helohyus plicodon
Gobiohyus orientalis
Diacodexis ilicis
Acotherulum saturninum
MNHN Qu 16586
USNM 482369
USNM 13079
USNM 26277
AMNH VP 16141
MNHN Qu 16366
UM2
AMNH
AMNH
AMNH
AMNH
UM2
left
right
right
right
left
left
75.2
48.16
61.66
62.57
34.39
25.28
1104
994
981
988
1751
984
621×540
765×563
711×702
764×702
849×678
984×984
Appendix 2
Table 3 Alphabetical list of anatomical terms used and illustration of these terms in the different figures
Term
Sources other than Giannini
et al. 2006
Anterior process of tegmen Luo and Gingerich (1999)
tympani
Anteromedial tuberosity of New term (= “knob” of O’Leary 2010)
the petrosal
Basicapsular groove
Presley (1979)
Ventrolateral Dorsomedial Anterior Ventromedial Fig.1 Fig.10 Fig. S14
Figs. 2, 6, 8 Figs. 3, 7, 9 Fig.4
Fig. 5
x
x
x
x
J Mammal Evol
Table 3 (continued)
Term
Sources other than Giannini
et al. 2006
Ventrolateral Dorsomedial Anterior Ventromedial Fig.1 Fig.10 Fig. S14
Figs. 2, 6, 8 Figs. 3, 7, 9 Fig.4
Fig. 5
Basioccipital
Caudal tympanic process of
petrosal
Cochlear aqueduct
Crista interfenestralis
Crista parotica
Crista petrosa
Crista transversa
Epitympanic recess
Epitympanic wing
External acoustic meatus
Facial nerve
Facial sulcus
Fenestra cochleae
Fenestra vestibuli
Foramen acusticum inferius
Foramen acusticum
superius
Fossa for the head of the
malleus
Fossa for stapedius muscle
Fossa for the tensor tympani
muscle
Greater petrosal nerve
Hiatus Fallopii
Inferior (= ventral) petrosal
sinus
Internal acoustic meatus
Internal carotid artery
Lateral process of the
epitympanic wing
Mastoid plate
Mastoid region
Orbitotemporal canal
Petromastoid canal
Petrosal
Pars canalicularis
Pars cochlearis
Posteromedial flange
Prefacial commissure
Prefacial commissure fossa
Giannini et al. (2006)
Giannini et al. (2006)
x
Processus muscularis
Promontorium
Ramus superior of the
stapedial artery
Secondary facial foramen
Semicircular canals
Stapedial artery
Stapedial foramen
Stylomastoid notch
Stylomastoid foramen
Sisson (1911)
Wible et al. 1995
Giannini et al. (2006)
Wible et al. (1995)
Giannini et al. (2006)
Giannini et al. (2006)
MacPhee (1981)
Giannini et al. (2006)
Giannini et al. (2006)
Giannini et al. (2006)
Giannini et al. (2006)
Giannini et al. (2006)
Giannini et al. (2006)
Giannini et al. (2006)
x
x
x
x
x
x
x
x
Giannini et al. (2006)
Giannini et al. (2006)
Giannini et al. (2006)
x
Giannini et al. (2006)
NAV
Giannini et al. (2006)
Rose and Emry (1993)
Giannini et al. (2006)
NAV, foramen stylomastoideum
x
x
x
x
x
Giannini et al. (2006)
Giannini et al. (2006)
NAV
Giannini et al. (2006)
Giannini et al. (2006)
x
x
x
x
x
O’Leary (2010)
McDowell (1958); MacPhee (1981)
Wible and Gaudin (2004)
Gannon et al. (1988)
Giannini et al. (2006)
Giannini et al. (2006)
Giannini et al. (2006)
O’Leary (2010)
Giannini et al. (2006)
O’Leary (2010)
x
x
x
Luo and Gingerich (1999)
Giannini et al. (2006)
Giannini et al. (2006)
New term
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
J Mammal Evol
Table 3 (continued)
Term
Sources other than Giannini
et al. 2006
Subarcuate fossa
Sulcus for stapedial artery
Tegmen tympani
Tegmen tympani canal
Tegmen tympani fossa
Tensor tympani muscle
Transpromontorial sulcus
Tympanic bulla
Giannini et al. (2006)
Novacek (1986)
Giannini et al. (2006)
New term
New term
Giannini et al. (2006)
Wible (1986)
NAV, bulla tympanica
Tympanic nerve
NAV, nervus tympanicus; Jacobsen’s
nerve (Wilkie 1936)
NAV, plexus tympanicus
Wible (2003)
Luo and Gingerich (1999)
Luo and Gingerich (1999)
Giannini et al. (2006)
Tympanic plexus
Tympanohyal
Vascular groove
Ventrolateral tuberosity
Vestibular aqueduct
Ventrolateral Dorsomedial Anterior Ventromedial Fig.1 Fig.10 Fig. S14
Figs. 2, 6, 8 Figs. 3, 7, 9 Fig.4
Fig. 5
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
Terminology generally follows the Nomina Anatomica Veterinaria as applied by Giannini et al. (2006) and Wible (2003), with additions from O’Leary
(2010) and Luo and Gingerich (1999) who listed standardized cranial anatomical terms in English for many Latin Nomina Anatomica Veterinaria (NAV)
terms and synonymized many terms. Online figures can be found on MorphoBank, Project 946
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