RESEARCH PAPER
Stem therian mammal Amphibetulimus from the Middle Jurassicof Siberia
Alexander Averianov • Thomas Martin •
Alexey Lopatin • Sergei Krasnolutskii
Received: 17 July 2013 / Accepted: 4 December 2013
� Springer-Verlag Berlin Heidelberg 2013
Abstract Amphibetulimus krasnolutskii is known from
the Middle Jurassic (Bathonian) Itat Formation of Kras-
noyarsk Territory, West Siberia, Russia, by several eden-
tulous and three dentigerous dental fragments, preserving
p1, antepenultimate, and ultimate lower molars, and by an
upper molar. It is unique among stem therians by widely
open trigonids on the posterior lower molars, paraconids
that are higher than the metaconids and have keeled
mesiolingual vertical crests, pronounced unilateral hyp-
sodonty of the lower molars and correlated unequal alve-
olar borders of the dentary ramus, and a linear Meckelian
groove that is not connected to the mandibular foramen and
extends along the pterygoid ridge. Amphibetulimus differs
from more derived stem therians by a simple unicuspid
talonid without an incipient talonid basin and a distinct
labial cingulum on the upper molars. The lack of an ec-
totympanic facet and the long linear Meckelian groove
extending onto the pterygoid ridge suggest that Amphibe-
tulimus had a derived state of the transitional mammalian
middle ear, where the ear ossicles were connected to the
dentary not by a thick ‘‘ossified’’ Meckelian cartilage, but
by a thin Meckelian cartilage, as in prenatal and early
postnatal stages of some modern therians.
Keywords Mammalia � Stem Theria � Middle Jurassic �Asia
Kurzfassung Von Amphibetulimus krasnolutzkii liegen
aus der mitteljurassischen (Bathon) Itat-Formation in der
Region Krasnoyarsk in West-Sibirien (Russland) mehrere
Unterkiefer-Fragmente und ein oberer Molar vor. In drei
Kieferfragmenten sind Zahne uberliefert, ein p1 sowie
Molaren aus vor-vorletzter und letzter Position. Amphibe-
tulimus unterscheidet sich von anderen Stamm-Theria
durch ein weit geoffnetes Trigonid und den hinteren unt-
eren Molaren, Paraconide, die hoher als die Metaconide
sind und einen gekielten mesiolingualen vertikalen Grat
besitzen, ausgepragte einseitige Hypsodontie an den unt-
eren Molaren und damit verbundene ungleich hohe Alve-
olarrander am Dentale, sowie eine gerade Meckel0sche
Rinne, die sich entlang des Pterygoid-Schelfs erstreckt und
nicht mit dem Mandibular-Foramen in Verbindung steht.
Amphibetulimus unterscheidet sich von starker abgeleiteten
Stamm-Theria durch ein einfaches einhockeriges Talonid
ohne angedeutete Beckenbildung und ein deutlich aus-
gepragtes labiales Cingulum an den oberen Molaren. Das
Fehlen einer Facette fur das Ectotympanicum und die
lange, gerade Meckel0sche Rinne, die sich auf den Ptery-
goid-Schelf erstreckt legen nahe, dass Amphibetulimus ein
A. Averianov (&)
Zoological Institute of the Russian Academy of Sciences,
Universitetskaya nab. 1, 199034 Saint Petersburg, Russia
e-mail: [email protected]
A. Averianov
Department of Sedimentary Geology, Geological Faculty,
Saint Petersburg State University, 16 liniya VO 29,
199178 Saint Petersburg, Russia
T. Martin
Steinmann-Institut fur Geologie, Mineralogie und Palaontologie,
Universitat Bonn, Nussallee 8, 53115 Bonn, Germany
e-mail: [email protected]
A. Lopatin
Borissiak Paleontological Institute of the Russian Academy of
Sciences, Profsouznaya str. 123, 117997 Moscow, Russia
e-mail: [email protected]
S. Krasnolutskii
Sharypovo Regional Museum, 2nd Microrayon 10,
Sharypovo, 662311 Krasnoyarsk, Russia
e-mail: [email protected]
123
Palaontol Z
DOI 10.1007/s12542-013-0217-x
fortgeschrittenes Stadium des Ubergangs zum Saugetier-
Mittelohr (transitional mammalian middle ear) erreicht
hatte, in dem die Gehorknochelchen nicht durch einen
dicken, ‘‘ossifizierten’’, sondern einen dunnen Mec-
kel0schen Knorpel mit dem Dentale verbunden waren, wie
in pranatalen und manchmal postnatalen Stadien moderner
Theria.
Schlusselworter Mammalia � Stamm-Theria � Mittlerer
Jura � Asien
Introduction
The Middle Jurassic (Bathonian) Itat Formation in the
Berezovsk Quarry is one of the richest Jurassic vertebrate
assemblages in Asia. The non-mammalians include hyb-
odontiform sharks, palaeonisciform and amiiform acty-
nopterygians, dipnoans, xinjiangchelid turtles, primitive
lepidosauromorphs, scincomorph lizards, choristoderes,
crocodilyforms, various ornithischian and saurischian
dinosaurs, pterosaurs, and tritylodontids (Alifanov et al.
2001; Skutschas et al. 2005; Skutschas 2006; Valeev 2008;
Averianov and Krasnolutskii 2009; Averianov et al. 2010a;
Skutschas and Krasnolutskii 2011). The mammalian
assemblage consists of haramiyidans, multituberculates,
diverse docodontants, derived triconodontans, symmetr-
odontans, and stem therians (Averianov et al. 2005, 2008,
2010b, 2011, 2013; Lopatin and Averianov 2005, 2007;
Averianov and Lopatin 2006). Thus, the mammalian
assemblage of Berezovsk Quarry includes all major
mammalian groups that lived in Laurasia during the
Jurassic (Kielan-Jaworowska et al. 2004; Luo 2007). The
most derived mammals of that time were pretribosphenic
stem therians, stem representatives of the large clade
Theria that includes modern marsupials and placentals
(McKenna 1975; Martin 2002; Kielan-Jaworowska et al.
2004; Lopatin and Averianov 2006; Averianov et al. 2013).
In the Berezovsk Quarry, stem therians were represented so
far by a single specimen found by one of us (SK) in 2006.
It is a dentary fragment with a lower molar (PIN 5087/3),
the holotype of Amphibetulimus krasnolutskii Lopatin et
Averianov, 2007 (Lopatin and Averianov 2007). Here we
describe additional specimens of this taxon that were col-
lected in 2010–2012 by the joint Russian–German expe-
dition to Berezovsk Quarry.
Materials and methods
The newly collected mammal specimens were obtained
during screen-washing of *12.5 tons of matrix of the
fossiliferous level within the Itat Formation in Berezovsk
Quarry in 2010–2012. The jaw fragments were found in the
field by picking the coarse fraction of fossiliferous con-
centrate. The teeth were recovered during sorting of the
fine fraction in the laboratory. The specimens described
here are housed in the Borissiak Paleontological Institute of
the Russian Academy of Sciences, Moscow (PIN). For
comparison we used specimens of stem therians housed in
the Natural History Museum, London (NHM).
The nomenclature of dental cusps and crests employed
here is shown in Fig. 1. The measurements, crown length
(L) and width (W), were taken under the scanning electron
microscope.
We use the term Mammalia in a broad sense, following
Kielan-Jaworowska et al. (2004), as a stem-based taxon
including a common ancestor of Sinoconodon and crown
mammals. The crown group concept of Mammalia is not
used because of the unstable position of the Monotremata.
For the phylogenetic analysis, we used the data matrix
published previously by Averianov et al. (2013, 2013; this
morphological data set is available at Morphobank: http://
www.morphobank.org: Project 876) in addition to the new
information available on A. krasnolutskii. All the charac-
ters in the matrix are phylogenetically informative and
treated as non-additive. A. krasnolutskii can be coded by 74
of 137 characters from that matrix (54.0 %). These codings
are the following: 2(0), 3(0), 7(1), 18(0), 30(1), 31(1),
32(0), 33(0), 34(0), 35(1), 36(1), 38(1), 39(0), 40(0), 41(1),
42(0), 43(1), 44(0), 45(0), 46(0), 47(0), 48(1), 49(1), 50(1),
Fig. 1 Dental nomenclature for the stem therian molar design
employed in the article. The labial side is up, and the anterior side is
to the left
A. Averianov et al.
123
56(1), 57(0), 58(1), 59(0), 60(0), 61(0), 62(0), 63(1), 64(0),
65(1), 66(2), 67(1), 68(1), 69(0), 70(2), 71(0), 72(0), 73(2),
74(1), 75(1), 76(1), 77(1), 78(1), 79(0), 80(0), 81(0), 82(0),
83(1), 84(1), 85(0), 86(0), 87(1), 88(0), 89(1), 90(1), 91(0),
92(2), 94(0), 95(0), 96(1), 97(0), 98(0), 99(0), 101(1),
102(0), 103(0), 106(0), 109(1), and 110(1).
The matrix was analyzed using the New Technology
Search algorithm of TNT version 1.1 (Goloboff et al.
2003), and the trees were analyzed using Winclada version
1.00.08 (Nixon 1999). The analysis produced five most
parsimonious trees with a length of 423 steps, a consistency
index of 0.37, and a retention index of 0.74.
Systematic paleontology
Mammalia Linnaeus 1758
Stem lineage of Theria Parker et Haswell 1897
Amphibetulimus Lopatin et Averianov 2007
Type species A. krasnolutskii Lopatin et Averianov, 2007.
Revised diagnosis As for the type and only known species.
Included species Type species.
A. krasnolutskii Lopatin et Averianov, 2007
Figures 2, 3, 4, and 5.
Holotype PIN 5087/3, right dentary fragment with the
antepenultimate molar and roots or alveoli for four other
cheek teeth.
Type locality and horizon Berezovsk Quarry, Sharypovo
District, Krasnoyarsk Territory, Russia; Itat Formation,
Middle Jurassic (Bathonian).
Referred specimens PIN 5087/34, right upper molar. PIN
5087/39, left dentary fragment with p1 (the tooth has been
lost when taking SEM images), alveoli or roots for i1–4,
Fig. 2 Amphibetulimus krasnolutskii, PIN 5087/34, right upper molar in occlusal (a, stereopair), distal (b), labial (c), and mesial (d) views.
Berezovsk Quarry, Krasnoyarsk Territory, Russia. Itat Formation, Middle Jurassic (Bathonian). Scale bar is 1 mm
Stem therian mammal Amphibetulimus
123
double rooted canine, and p2. PIN 5087/44, right dentary
fragment with alveoli for two middle molars. PIN 5087/43,
right dentary fragment with alveoli for ultimate and pen-
ultimate molars. PIN 5087/40, right dentary fragment with
ultimate molar and roots of the penultimate molar. PIN
5087/45, right dentary fragment with alveolus for ultimate
molar.
Revised diagnosis A. krasnolutskii is referred to the stem
lineage of Theria based on the complete distal metacristid,
oblique cristid, deep hypoflexid, and talonid width larger
than 40 % of trigonid width. It differs from Amphitherium
prevostii by the larger trigonid angle, Meckelian groove
parallel to the ventral border, and lacking coronoid and
splenial facets on the dentary. It differs from more derived
stem therians (Zatheria) by the metacone labial to the
paracone, crest-like metacone, distinctly smaller than the
paracone, and absent talonid basin. According to the cur-
rent phylogenetic hypothesis, A. krasnolutskii has eight
autapomorphies: a continuous lingual cingulid on the lower
premolars (known only for p1), upper molars wider than
long (L/W between 0.75 and 0.99), unilateral hypsodonty of
the lower molars, lowest point of the paracristid higher
than that on the protocristid, vertical paraconid, the para-
conid higher than the metaconid, talonid single-cusped and
heel-like, and similar height of the mandibular ramus
between the canine and last molar.
Description The upper molar (PIN 5087/34; Fig. 2) has a
relatively narrow (mesiodistally; L/W = 0.81) triangular
crown dominated by the large lingually positioned para-
cone. The trigon angle is *33�. The stylocone is also well
developed, and possibly was only slightly lower than the
paracone (the tip of the latter is broken off). The next
largest cusp is the parastyle, which is connected to the
stylocone by a short longitudinal ridge. The preparacrista is
mesially convex in occlusal view, deflecting distally
towards the stylocone tip. It is considerably worn between
the bases of the paracone and stylocone. There is also an
extensive wear facet (facet 1) on the mesial side of the
crown, between the preparacrista, the ridge connecting the
stylocone and parastyle, and the parastyle. The lingual side
of the parastyle is broken, and the presence of a prepara-
style is not certain. There is a peculiar small cusp labial to
the parastyle. It is connected to the base of the stylocone by
a short ridge. A similar cusp, but placed opposite to the
stylocone instead of parastyle, is rarely present in the
known specimens of Palaeoxonodon ooliticus (Sigogneau-
Russell 2003: fig. 16B). The postmetacrista is nearly
straight in its lingual half and somewhat convex in labial
direction. The metacone and the postmetacrista cusp are
crest-like. The metacone is slightly smaller than the post-
metacrista cusp. There is some wear (facet 2) along the
postmetacrista on the distal side of the crown. The meta-
style is a small cusp connected to the labial cingulum by its
short distal arm which deflects lingually. The labial cin-
gulum is prominent and remarkably straight; it extends
between the metastyle and the stylocone. There is a distinct
ectoflexus on the distal third of the labial side of the crown
opposite to the labial cingulum. The trigon basin is a
shallow valley between the paracone and cristae cusps
closed labially by the labial cingulum. The tooth has three
roots. The largest root is lingual and supports the paracone.
The lower incisors (i1–4) are known only from their
alveoli in PIN 5087/39 (Fig. 3). These were relatively large
teeth, with the relative size i1 \ i2 \ i3 [ i4. The alveolus
for the anteriormost incisor (i1) is almost horizontal, and
the tooth was likely procumbent. The second and third
Fig. 3 Amphibetulimus krasnolutskii, PIN 5087/39, left dentary
fragment with p1, alveoli or roots for i1–4, double rooted canine, and
p2, in antero-occlusal (a), occlusal (b), labial (c), and lingual
(d) views. Berezovsk Quarry, Krasnoyarsk Territory, Russia. Itat
Formation, Middle Jurassic (Bathonian). Scale bar is 1 mm. c, roots
of double-rooted canine; i1–i4, alveoli for incisors; mf, mental
foramen; p1 first lower premolar; p2 mesial root and distal alveolus
for second lower premolar; sf symphyseal foramen
A. Averianov et al.
123
incisors, i2 and i3, were inclined at *56�–57� angles and
i4 at *72� to the horizontal.
The lower canine, known from the roots in PIN 5087/39
(Fig. 3), was a robust double-rooted tooth continuing the
incisor arc. The mesial root is mesiodistally shorter than
the distal root. The tooth was set at an angle of *60� to the
horizontal.
The first lower premolar (p1) is a relatively large dou-
ble-rooted tooth separated by a distinct diastema from the
canine (Fig. 3). The crown is dominated by the main cusp
(its tip is broken off) and has a small accessory distal cusp.
The mesial side of the main cusp is slightly convex in
lateral view; the distal side is straight. A faint lingual
cingulid runs around the crown. The roots are coalesced
above the alveolus and separated inside; they bear ring-like
thickenings just above the alveolus (Fig. 3c, d). Both roots
are of similar size.
The second lower premolar (p2) is known from the
mesial root and distal alveolus in PIN 5087/39 (Fig. 3).
The mesial root is oval in cross section and slightly com-
pressed mesiodistally. The alveolus for the distal root is
about twice as large as the mesial root alveolus.
The lower molars are known from two specimens, both
preserved in dentary fragments. The antepenultimate
molar, preserved in the holotype (Fig. 4), was the largest
molar in the series. The size of the cheek teeth decreases
mesially and distally from this tooth. The crown of the
antepenultimate molar is high, with a large trigonid and
small talonid. The crown is unilaterally hypsodont, with the
labial side deeper than the lingual side. The trigonid angle
is 84�. The protoconid is the highest cusp, with its base
occupying most of the trigonid. The labial slope of the
protoconid is convex, while the lingual slope is flat, almost
vertical. The paraconid is vertical, much higher and larger
than the metaconid. The bases of the paraconid and met-
aconid are widely spaced. There is no trigonid basin
between the trigonid cusps. There is no cingulid at the base
of the crown. The anterior cingulid cuspules e and f are
high vertical crests on the sides of a deep groove on the
mesial wall of the crown, which accommodates the talonid
cusp of the preceding tooth. The mesiolingual cuspule e is
much better developed and forms the mesial keel of the
paraconid. The talonid is broken off distally. It was likely
unicuspid. Any traces of a talonid basin cannot be detected.
Fig. 4 Amphibetulimus krasnolutskii, PIN 5087/3, holotype, right
dentary fragment with the antepenultimate molar and roots or alveoli
for four other cheek teeth, in lingual (a), occlusal (b, stereopair), and
labial (c) views. Berezovsk Quarry, Krasnoyarsk Territory, Russia.
Itat Formation, Middle Jurassic (Bathonian). Scale bar is 1 mm. mc
mandibular canal, mf masseteric fossa, Mg Meckelian groove, ptf
pterygoid fossa
Stem therian mammal Amphibetulimus
123
The lingual wall of the talonid is vertical. The labial slope
of the talonid is almost entirely occupied by an extensive
wear facet (facet 1 ? 3), which is produced by the para-
cone. Most of the posterior wall of the metaconid is also
worn; therefore, the wall is almost vertical. Because of
wear, it is not possible to establish the presence of a distal
metacristid. Another relatively small wear facet (facet 2) is
seen on the labial slope of the protoconid near its apex. The
tooth has two roots. The mesial root is slightly larger than
the distal root.
In the holotype, in spite of the extensive wear of the
antepenultimate molar, the ultimate molar was only
recently erupted, as is evident from its undivided alveolus
(Fig. 4b). The ultimate molar preserved in PIN 5087/40
documents an earlier ontogenetic stage: it is not fully
erupted above the alveolar level, and its alveolus excavates
the lingual side of the dentary (Fig. 5b). The ultimate molar
is 30 % shorter than the antepenultimate molar and much
lower. The trigonid is widely open as in the antepenulti-
mate molar, with a trigonid angle of *83�. The protoconid
is still the highest trigonid cusp but possibly was not much
higher than the paraconid. The paraconid is broken off. It
has a strong mesial keel, as in the antepenultimate molar.
The paracristid is longer than the oblique protocristid. The
metaconid is distinctly smaller than the paraconid. There is
a distinct distal metacristid extending distolabially from the
metaconid. The talonid is short, unicuspid, and not basined.
The distal root is longer mesiodistally than the mesial root.
The dentary is known from several posterior and one
anterior fragments (PIN 5087/39; Fig. 3). The anterior end
of mandibular ramus is shallow, tapering anteriorly. The
ventral margin of the ramus is nearly straight, whereas the
dorsal margin is convex, except the area between canine
and p2, where it is excavated. Possibly this excavation is
connected with a recent eruption of teeth in this region in
PIN 5087/39. On the labial side, there are four anterior
mental foramina, which increase in size posteriorly: below
i3, i4, the distal root of the canine, and distal root of p1
(Fig. 3c). The mental foramen below p1 is the largest, but
not hypertrophied as in Nanolestes drescherae (Martin
2002: fig. 7). The mandibular symphysis is long, occupy-
ing the ventral half of the lingual side of PIN 5087/39 and
tapering anteriorly. The symphysis was likely terminating
at p2, and it seems that PIN 5087/39 was broken along the
weak part of the dentary posteriorly to the symphysis. At
the anterior end, there is a distinct short ridge dorsal to the
symphysis. At the posterior edge of this ridge and along the
ventral margin of the ramus, there is a relatively large
symphyseal foramen (Fig. 3d). The labial and lingual
dentary borders are equal in height in PIN 5087/39.
In the middle and posterior parts, the mandibular ramus
has convex ventral and dorsal borders, which are deepest at
the ultimate and penultimate molars (Fig. 4). Posteriorly,
the labial and lingual borders of the mandibular ramus are
not equal; the lingual border is distinctly higher. The
mandibular canal is revealed by breakage of the bone on
the labial side at the anterior end of the holotype specimen
(Fig. 4c). The posterior end of this opening likely repre-
sents the posterior edge of the posterior mental foramen
(Lopatin and Averianov 2007). There is a small posterior
mandibular foramen in a middle dentary fragment PIN
5087/44, but its relative position cannot be established
because of the incompleteness of this specimen. In stem
therians, the size and position of the posterior mental
foramen is highly variable: it can be present at the level of
p4, p5, or m1 (Martin 2002; Li et al. 2005; Lopatin and
Averianov 2006).
Fig. 5 Amphibetulimus krasnolutskii, PIN 5087/40, right dentary
fragment with ultimate molar and roots of the penultimate molar in
occlusal (a), lingual (b), and labial (c) views. Berezovsk Quarry,
Krasnoyarsk Territory, Russia. Itat Formation, Middle Jurassic
(Bathonian). Scale bar is 1 mm. Mg Meckelian groove
A. Averianov et al.
123
The Meckelian groove is very thin and linear, and it runs
close and parallel to the ventral border (Figs. 4a, 5b).
Posteriorly, it extends onto the pterygoid crest. The pter-
ygoid fossa is very small and oval shaped. It extends
posteriorly to the mandibular foramen dorsal to the ptery-
goid crest. The masseteric fossa is very shallow (Fig. 4c).
Its ventral border is a low and broad crest approximately
equal in height to the half of the mandibular ramus height.
Measurements PIN 5087/34, upper molar: L = 1.11;
W = 1.37; PIN 5087/3, antepenultimate lower molar:
L = 1.75; W = 0.87. PIN 5087/40, ultimate lower molar:
L = 1.23; W = 0.63.
Discussion
According to the phylogenetic analysis performed in this
article, A. krasnolutskii forms a clade with P. ooliticus and
N. drescherae (Fig. 6). This clade is part of a polytomy
with Mozomus shikamai and Zatheria. A. krasnolutskii
differs from Zatheria by an unicuspid talonid lacking a
basin. Notably, the contemporaneous P. ooliticus from the
Middle Jurassic of England shows great variation in the
development of additional talonid cuspules and in the
characteristics of the talonid basin (Sigogneau-Russell
2003). The taxon-based definition of Zatheria was founded
upon the Early Cretaceous Peramus tenuirostris (McKenna
1975; Prothero 1981; Martin 2002; Kielan-Jaworowska
et al. 2004). The unambiguous and non-homoplastic syn-
apomorphy of this group is the position of the metacone
approximately at the same level as the paracone [Character
40(1) in Fig. 6]. In more basal cladotherians, the metacone
is labial to the paracone. A. krasnolutskii and P. ooliticus
share this primitive condition, and these taxa are clearly
outside of Zatheria.
As was reviewed by Lopatin and Averianov (2006),
some stem therians have a characteristic ‘‘partially molar-
iform’’ m1 with a widely open trigonid basin, whereas the
more posterior molars have a lower trigonid angle. Am-
phibetulimus is unique among stem therians in having
antepenultimate and ultimate molars with a widely open
trigonid basin and large trigonid angle. Another distinctive
feature of Amphibetulimus is the distinct unilateral hyp-
sodonty of the lower molars echoed in the unequal alveolar
borders of the mandibular ramus. Unilateral hypsodonty is
developed to some extent in other stem therian taxa, but in
Amphibetulimus it is developed to the extreme, paralleling
the condition of dryolestids. There are two other characters
of Amphibetulimus not found in other stem therians, but
surprisingly characteristic of metatherian mammals. The
first character is a paraconid that is higher than the meta-
conid. This character is related to the predominance of
postvallum/prevallid shear in contrast to the prevallum/
postvalid shear of dryolestidans and eutherians (Fox 1975;
Schultz and Martin 2010). The other character is the keeled
mesiolingual vertical crest of the paraconid. According to
the current phylogenetic hypothesis, these characters were
independently acquired by Amphibetulimus and
Metatheria.
The internal groove on the dentary of Mesozoic mam-
mals has been variously interpreted (see review in Simpson
1928b; Meng et al. 2003). The current consensus is that the
linear anterior part of the groove represents the slit of the
dentary bone that wrapped around the Meckelian cartilage
during ontogeny. The posterior, wider part of the internal
groove, when present, held the ‘‘ossified’’ Meckelian
Fig. 6 Fragment of the strict
consensus tree of five most
parsimonious trees produced by
TNT using the data set
presented in Averianov et al.
(2013, 2013) with the addition
of new information on
Amphibetulimus krasnolutskii,
demonstrating interrelationships
within stem Theria. Only
unambiguous characters are
shown (black circles are
nonhomoplasies and white
circles are homoplasies). The
numbers at the circles are
characters (above) and states
(below)
Stem therian mammal Amphibetulimus
123
cartilage, whose terminal endochondral ossification (artic-
ular) together with the intramembranous ossification (pre-
articular) was transformed into the auditory bone malleus.
The malleus was connected via other ear ossicles (incus
and stapes) to the fenestra vestibuli of the petrosal prom-
ontorium. The middle part of Meckel’s cartilage was pos-
sibly connected by a ligament to the lateral flange of the
petrosal (Wang et al. 2001; Meng et al. 2003, 2011). This
condition, when the middle ear bones are still connected to
the dentary via Meckel’s cartilage in adults, is termed the
transitional mammalian middle ear (TMME). In more
derived mammals, the Meckelian cartilage is resorbed
during embryogenesis, and the middle ear bones are
entirely incorporated into the basicranium, forming the
definitive mammalian middle ear (DMME) (Luo 2011;
Meng et al. 2011). The Meckelian cartilage in taxa with
TMME is often described as ‘‘ossified’’, although it was
most likely not affected by endochondral ossification
(except the distal part forming the malleus). The endo-
chondral ossification is a peramorphic process that is
hardly to be expected in paedomorphic animals retaining
the Meckelian cartilage during the adult stage.
In some Mesozoic mammals, the internal groove bifur-
cates posteriorly, as noted by Simpson (1928b) for the
derived triconodontan Phascolotherium bucklandi from the
Middle Jurassic of England. The groove bifurcation is
evident in the holotype, although it cannot be completely
traced posteriorly because of bone damage (Fig. 7b), and
was figured for an additional juvenile specimen, NHM
M7595 (Simpson 1928a: fig. 23). However, our study of
the latter specimen could not confirm the internal groove
bifurcation. A similar groove bifurcation is known also for
Fig. 7 Posterior part of the mandible in lingual view of selected
Mesozoic mammals showing the variation of the Meckelian groove
and associated elements: a basal triconodontan mammal Morganuc-
odon watsoni, based on Kermack et al. (1973: fig. 7B); b derived
triconodontan Phascolotherium bucklandi, based on the holotype
NHM M112; c derived triconodontan Repenomamus robustus, based
on Luo et al. (2007: fig. 3d); d stem therian Nanolestes drescherae,
based on Martin (2002: fig. 6A); e stem therian Peramus tenuirostris,
based on NHM M47799; f stem placental Prokennalestes trofimovi,
based on Kielan-Jaworowska and Dashzeveg (1989: figs. 20, 21);
g stem therian Amphibetulimus krasnolutskii, based on the holotype
PIN 5087/3. Not to scale. The dentary bone is depicted in light gray.
an angular, ap angular process, ar articular, ec ectotympanic or its
facet, co coronoid, cp coronoid process, dc, dentary condyle, mf
mandibular foramen, Mg Meckelian groove, oMc ‘‘ossified’’ Meck-
elian cartilage, pa prearticular, pap pseudoangular process, su
surangular
A. Averianov et al.
123
the stem therian mammal A. prevostii from the same
Middle Jurassic fauna of England (Allin and Hopson 1992:
fig. 28.11). The main part of the internal groove, which
certainly held the Meckelian cartilage, is directed toward
the mandibular foramen, whereas the diverging part con-
tinues onto the pterygoid crest. This diverging part was
interpreted as a groove for the angular (=ectotympanic)
(Allin 1975; Allin and Hopson 1992), and this interpreta-
tion seems to be correct.
In the Early Cretaceous gobiconodontid triconodontans
(Wang et al. 2001; Meng et al. 2003, 2011; Luo et al.
2007), the ectotympanic was considerably short, and a
wide Meckelian groove, containing the ‘‘ossified’’ Meck-
elian cartilage, extended well posteriorly along the ptery-
goid ridge (Fig. 7c). The Meckelian groove of A.
krasnolutskii matches this condition most closely: it
extends posteriorly onto the pterygoid crest beyond the
level of the mandibular foramen (Fig. 7g). However, it is
remarkably thin and linear, without a widened portion that
would hold the ‘‘ossified’’ Meckelian cartilage. Probably,
the ‘‘ossified’’ part of the Meckelian cartilage was missing
in Amphibetulimus, but the malleus was still connected to
the dentary by a thin cartilage, as in prenatal and early
postnatal stages of some mammals (Meng et al. 2003).
Other stem therians show remarkable variation in the
structure of the internal groove. In the Late Jurassic N.
drescherae from Portugal, a relatively wide Meckelian
groove extends and slightly expands toward the anteriorly
positioned mandibular foramen (Martin 2002; Fig. 7d).
There is no trace of the ectotympanic on the dentary. A
similar Meckelian groove was present in the Early Creta-
ceous stem therian Kielantherium gobiense from Mongolia
(Dashzeveg and Kielan-Jaworowska 1984: fig. 1B, D). But
in the phylogenetically more basal stem therian Arguimus
khosbajari from the same Early Cretaceous fauna of
Mongolia, the internal groove is totally lost (Lopatin and
Averianov 2006).
In the Early Cretaceous stem therian P. tenuirostris from
England (Fig. 7e) and in the Early Cretaceous stem plac-
entals Prokennalestes trofimovi from Mongolia (Fig. 7f)
and Eomaia scansoria from China (Ji et al. 2002: fig. 2d),
there is a Meckelian groove of variable width that extends
toward the mandibular foramen, and there is no scar for the
ectotympanic. However, in these taxa the mandibular
foramen is shifted far posteriorly, and the Meckelian
groove extends along the pterygoid ridge following this
shift.
The above-described variation in the structure of the
internal groove in the stem lineage representatives that led
to the modern therians suggests that the transformation of
the TMME into the DMME condition was complex and
occurred in a mosaic pattern. The DMME may have been
independently acquired in different lineages. The oldest
member of the therian stem group, for which the dentary is
known, the Middle Jurassic A. krasnolutskii, shows a
unique shape of the internal groove: it is linear, discon-
nected from the mandibular foramen, and extends onto the
pterygoid crest. The phylogenetic and functional signifi-
cance of this configuration is currently poorly understood.
Acknowledgments This study was supported by the Deutsche
Forschungsgemeinschaft (DFG) grant MA 1643/14-1, the Board of
the President of the Russian Federation (MD-802.2009.4), the Russian
Foundation for Basic Research (projects 07-04-00393, 10-04-01350,
13-04-01401, and 11-04-91331-NNIO), and the Program of the Pre-
sidium of the Russian Academy of Sciences ‘‘Origin of the Life and
Establishment of Biosphere’’. G. Oleschinski (Bonn) assisted at the
SEM. AA is grateful to A. Bochkov (Saint Petersburg) for discussion
of character-weighting methods. For assistance in the field and/or
picking the concentrate, we thank I. Danilov, D. Grigoriev, R. Hiel-
scher, K. Jager, J. Konen, S. Krasnolutskii, D. Rohkamp, R. Schell-
horn, J. Schultz, A. Schwermann, L. Schwermann, P. Skutschas, E.
Syromyatnikova, and A. Valeev. We are grateful to reviewer L.
Gaetano and editor G. Rougier for providing helpful comments on the
manuscript.
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