Stem therian mammal Amphibetulimus from the Middle Jurassic of Siberia

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: dzharakuduk@mail.ru

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: tmartin@uni-bonn.de

A. Lopatin

Borissiak Paleontological Institute of the Russian Academy of

Sciences, Profsouznaya str. 123, 117997 Moscow, Russia

e-mail: alopat@paleo.ru

S. Krasnolutskii

Sharypovo Regional Museum, 2nd Microrayon 10,

Sharypovo, 662311 Krasnoyarsk, Russia

e-mail: krasnolucki.ser@mail.ru

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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