Three new Jurassic euharamiyidan species reinforce early divergence of mammals

Article (PDF Available)inNature 514(7524) · September 2014with 804 Reads
DOI: 10.1038/nature13718 · Source: PubMed
Abstract
The phylogeny of Allotheria, including Multituberculata and Haramiyida, remains unsolved and has generated contentious views on the origin and earliest evolution of mammals. Here we report three new species of a new clade, Euharamiyida, based on six well-preserved fossils from the Jurassic period of China. These fossils reveal many craniodental and postcranial features of euharamiyidans and clarify several ambiguous structures that are currently the topic of debate. Our phylogenetic analyses recognize Euharamiyida as the sister group of Multituberculata, and place Allotheria within the Mammalia. The phylogeny suggests that allotherian mammals evolved from a Late Triassic (approximately 208 million years ago) Haramiyavia-like ancestor and diversified into euharamiyidans and multituberculates with a cosmopolitan distribution, implying homologous acquisition of many craniodental and postcranial features in the two groups. Our findings also favour a Late Triassic origin of mammals in Laurasia and two independent detachment events of the middle ear bones during mammalian evolution.
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Skeletal features of euharamiyidans. a, Reconstruction of the skeleton of Shenshou lui, based in part on Xianshou linglong and Xianshou songae. b, The vertebral column of Shenshou lui. c, The anterior section of the rib cage in Shenshou lui. d, The right scapular of Shenshou lui. e, The distal end of the humerus in Shenshou lui. f, Reconstruction of the hand of Shenshou lui, based on LDNHMF2001 and WGMV-001. g, Reconstruction of the foot of euharamiyidans, based on Shenshou lui (JZT-D061) and Xianshou songae. The cervical ribs, present in monotremes and many Mesozoic mammals4, 17, 20, 24, are absent. Similar to therians, such as Eomaia32 and Sinodelphys27, the first ten thoracic ribs are connected to the ossified manubrium and sterna via costal cartilages and the last three ribs float freely. The capitulum of each rib articulates between two thoracic centra at a ventral position. The last thoracic rib (13th) is identified as the diaphragmatic vertebra because the articular facets of its zygapophyses with the first lumbar are more vertical than horizontal, as in many extant mammals49. The anticlinal vertebrate is located at lumbar four. The tail consists of 18–22 caudal vertebrae, with the proximal ones bearing expanded transverse processes as in extant prehensile therians50. The scapular blade is roughly rectangular and has a large and deep infraspinous fossa but lacks a supraspinous fossa. The clavicle is strap-shaped and slightly curved anteriorly. Its rough proximal end indicates a flexible contact with the depression on the clover-leaf-shaped interclavicle. The distal end of the humerus has a bulbous radial condyle, a relatively smaller spherical ulna condyle, and a prominent entepicondyle. The femur has a hemispherical head with an extensive articular surface but a short neck, the greater trochanter is triangular and does not extend above the head. The distal condyles are small with a shallow patellar groove. The ankles are comparable to those of multituberculates, such as Kryptobaatar24, in that the calcaneus has a short and mediolaterally compressed tuber calcanei and are partly superposed by the astragalus. The cuboid is positioned obliquely and has little contact with the calcaneus so that metatarsal V is separated from the calcaneus. The entocuneiform is elongated, and its joint with metatarsal I is offset anteriorly from the joint of the intermediate cuneiform and metatarsal II, similar to that of Asioryctes and Eomaia32. Metapodials and proximal phalanges possess a well-developed palmar groove for the digital flexor muscle tendon. Metatarsals I and V are short and robust compared to others. The distal ends of proximal and intermediate phalanges are well trochleated. Terminal phalanges are compressed laterally and curved strongly with a sharp tip; each has a massive digital flexor tubercle on the ventral side and a small dorsally extended ridge. as, astragalus; ce, centrale; cm, calcaneum; ct, capitate; cu, cuboid; ec, ectocuneiform; en, entocuneiform; hm, hamate; L, lumbar; ltp, lumbar transverse process; lu, lunate; me, mesocuneiform; T, thoracic; td, trapezoid; tm, trapezium; sp, scaphoid; pi, pisiform; tq, triquetrum; ts, tarsal spur. The 10 mm scale applies to panel a and the 5 mm scale bar applies to all other postcranial elements. See photographs of skeletons and postcranial structures in Extended Data Figs 1, 3, 4a, 5a and 7d–g.
… 
ARTICLE doi:10.1038/nature13718
Three new Jurassic euharamiyidan species
reinforce early divergence of mammals
Shundong Bi
1,2
, Yuanqing Wang
1
, Jian Guan
3
, Xia Sheng
4
& Jin Meng
5
The phylogenyof Allotheria, including Multituberculata and Haramiyida, remains unsolved and has generated contentious
views on the origin and earliest evolution of mammals. Here we report three new species of a new clade, Euharamiyida,
based on six well-preserved fossils from the Jurassic period of China. These fossils reveal many craniodental and post-
cranial features of euharamiyidans and clarify several ambiguous structures that are currently the topic of debate. Our
phylogenetic analyses recognize Euharamiyida as the sister group of Multituberculata, and place Allotheria within the
Mammalia. The phylogeny suggests that allotherian mammals evolved from a Late Triassic (approximately 208 million
years ago) Haramiyavia-like ancestor and diversified into euharamiyidans and multituberculates with a cosmopolitan
distribution, implying homologous acquisition of many craniodental and postcranial features in the two groups. Our
findings also favour a Late Triassic origin of mammals in Laurasia and two independent detachment events of the middle
ear bones during mammalian evolution.
Mammalia Linnaeus, 1758
Allotheria Marsh, 1880
Euharamiyida (new clade)
Shenshou lui
gen. et sp. nov. Bi, Wang, Guan, Sheng and Meng
Etymology. Shen, from pinyin of the Chinese word, meaning deity, divin-
ity or cleaver; shou, from pinyin of the Chinese word for creature, animal
or beast; specific name after Lu Jianhua, the collector of the holotype.
Holotype. A nearly complete skeleton from an adult individual (LDN
HMF2001, Lande Museum of Natural History, Tangshan, Hebei Prov-
ince, China) (Figs 1a and 2d, and Extended Data Figs 1a and 2). Three
specimens arereferred to as the paratypes(see Supplementary Informa-
tion, section A).
Paratypes. Three specimens are referred to as the paratypes (see sec-
tion A of Supplementary Information).
Locality and horizon. The Tiaojishan Formation, Daxishan site of
Linglongta, Jianchang County, Liaoning Province, China; the locality
was dated as approximately 160 million years ago (within the Oxfordian)
(see Supplementary Information, section C, for age constraint).
Diagnosis.Medium-sized euharamiyidan with an estimatedbody mass
of 300 g (Supplementary Information, section D). Dental formula I
1
-
C
0
-P
2
-M
2
/I
1
-C
0
-P
1
-M
2
(I, incisor; C, canine; P, premolar; M, molar;
superscript, upper teeth; subscript, lower teeth). The only pair of upper
incisors (I
2
) are in contact so that a facet is present on the medial side of
each tooth;I
2
with two cusps.The mesial upper premolar (P
3
)small(not
basined) and the ultimate premolar (P
4
) not significantly larger than
upper molars. Upper molars with two main cusps in the buccal row,
separated by a low ridge; threecusps in the lingualone, of which the pen-
ultimate cusp (B2) is thelargest.P
4
sub-molariform with a main mesio-
lingualcusp (a1) and a long basined heel with two rows of cusps;M
1
with
three cusps in each cusp row, M
2
with four cusps in the lingual and three
in the labial row (Fig. 2d; see Supplementary Information, section A, for
differential comparisons). The terminology we use to designate cusps
in allotherian teeth is as follows: for upper teeth, the buccal (labial or
lateral) cusp row is A, lingual row is B, cusps are numbered from the
distal end; lower teeth, the lingual cusp row is a, the buccal row is b (lower
case), numbering starts from the mesial (anterior) end.
Eleutherodontidae Kermack et al., 1998
Xianshou
gen. nov. Wang, Meng, Bi, Guan and Sheng
Etymology. Xian, from pinyin of the Chinese word meaning celestial
being or immortal.
Locality and horizon. Same as Shenshou.
Diagnosis.Dental formula: I
2
-C
0
-P
2
-M
2
/I
1
-C
0
-P
1
-M
2
; upper and lower
molars ovoid in outline, with a shallow central basin. Differ from Sine-
leutherus in having threewell-separated cusps of I
2
, non-molariformP
4
with a hypertrophic mesiolingual cusp (a1) and a weakly basined heel.
Differ from Eleutherodonin the ovoid upper molars by absence of third
row of cusps, and lack of cuspules and transverse ridges in the central
basin. Differ from Shenshou and Arboroharamiya in having an extra-
small I
1
, ovoid upper and lower molars, more distally positioned disto-
buccal cusp (A1) on P
4
and M
1
; a hypertrophic mesiolingual cusp (a1)
on lower molars (Fig. 2e, f; see Supplementary Information, section A,
for differential comparisons, and Extended Data Figs 5 and 6 for addi-
tional figures).
Xianshou linglong
sp. nov. Wang, Meng, Bi, Guan and Sheng
Etymology. linglong, from pinyin of the Chinese word, meaning ‘exquisite’,
and also after the town name Linglongta where the specimen came from.
Holotype. A skeleton preserved on a split slab of laminated siltstone
(IVPP V16707A-B, Institute of Vertebrate Paleontology and Paleoan-
thropology, Chinese Academy of Sciences, Beijing, China; Figs 1b and
2e, and Extended Data Figs 1b and 5).
Diagnosis. Estimated body mass of 83 g. I
2
with three cusps; I
3
extre-
mely small and budlike. Upper molars with sharp cusps and stronger
and sharper ridges (flutings) than those in Shenshou and X. songae;M
1
with two maincusps at the mesial and distalend and connected by a low
and sharp ridge in each cusp row; an enlarged and more distally extended
distobuccal cusp (A1) on P
4
and M
1
;P
4
enlarged with a hypertrophic
mesiolingual cusp (a1) and a small talonid heel; cusp a1 of lower molar
procumbent, projecting mesially beyond the crown.
1
Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044,
China.
2
Department of Biology, Indiana University of Pennsylvania, Indiana, Pennsylvania 15705, USA.
3
Beijing Natural History Museum, 126 Tianqiao Street, Dongcheng District, Beijing 100050, China.
4
Paleontological Museum of Liaoning, Shenyang Normal University, Shenyang, Liaoning 110034, China.
5
Division of Paleontology, American Museum of Natural History, Central Park West at 79th Street,
New York, New York 10024, USA.
00 MONTH 2014 | VOL 000 | NATURE | 1
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©2014
Xianshou songae
sp. nov. Meng, Guan, Wang, Bi and Sheng
Etymology. The specific name is after Rufeng Song, the collector of the
holotype specimen.
Holotype. A skeleton preserved partial skull, mandible, and most of
the postcranial skeleton (BMNHC-PM003253, Beijing Natural History
Museum, China) (Figs 1c and 2f, and Extended Data Fig. 6).
Diagnosis. A small euharamiyidan with an estimated body mass of
40 g. Differ from X. linglong by having significantly smaller body size
and in having P
4
more transversely oval, cusp A1 on P
4
and M
1
pro-
portionally smaller and less distally extended. The lingual row of M
1
bears three cusps, of which the middle (B2) is the largest; lower molars
anteroposteriorly short with a vertical hypertrophic mesiolingual cusp
(a1) and low buccal cusps.
Craniodental features
The general skull shape of the new euharamiyidans is therian-like with
a broad basicranial region and a tapered rostrum in dorsal and ventral
views (Extended Data Figs 3 and 4) but multituberculate-like in lateral
view (Fig. 2a, b). A small septomaxilla is probably present (Extended Data
Fig. 2a). The zygomatic arch is slender but fully developed, with the ante-
rior root lateral to P
4
. As reflected by the skull shape, the cranial cavity
is more inflated than those of eutriconodontans. The glenoid fossa is
anterolateral to the bulging promontorium of the petrosal and antero-
posteriorly oriented, and lacks the postglenoid process (Extended Data
Figs 4b and 5b). The dentary is similar to that of Arboroharamiya
1
and
multituberculatesin having a distinct diastema between the incisorand
premolar, a small coronoidprocess, a masseteric fossa extending ante-
riorly to the level of P
4
and a low-positioned mandibular condyle that is
a
10 mm 10 mm
b
c
10 mm
Figure 1
|
The holotypes of three euharamiyidan species. a, Holotype
(LDNHMF2001) of Shenshou lui.b, Holotype (IVPP V16707A) of Xianshou
linglong.c, Holotype specimen (BMNHC-PM003253) of Xianshou songae.See
Extended Data Fig. 1 for interpretations of the skeletal features.
10 mm
2 mm
a
d
e
f
b
cCoronoid
Masseteric fossa
Pterygoid fossa
Mandibular foramen
Angular process
Mesial
Mesial
Mesial
Mesial
Mesial
Buccal
Buccal
Buccal
Buccal
Buccal
M1
M1
M1M2
P4
P4
P3
P3
I2
I2
I1
M2P4M1M2
P4
P4
M1
M1
M2
I2
Figure 2
|
Teeth, skull and mandibles of euharamiyidans. a, Reconstruction
of the skull and jaws of Xianshou linglong (the small I
1
is on the medial side
of the large I
2
). b, The labial view of the lower jaw of Xianshou linglong.
c, Lingual view of the lower jaw of Xianshou linglong. Part of the ascending
ramus and coronoid bone have not been preserved and are reconstructed based
on Shenshou lui.d, Right I
2
,M
1,2
, and left P
4
–M
2
of Shenshou lui in occlusal
view. e, Left I
1
,I
2
,P
4
,M
1
and P
4
–M
2
of Xianshou linglong in occlusal view.
Dashed lines represent the alveolus of P
3
.f, Right P
3
–M
2
, and P
4
and M
1
of
Xianshou songae in occlusal view. See text for description of the skull and
mandible. Dental formula are I
1?
-C
0
-P
2
-M
2
/I
1
-C
0
-P
2
-M
2
(the upper incisor is
not preserved in this species). Shenshou and Xianshou have a multicusped I
2
and a greatly enlarged I
2
that is fully covered with enamel. There is no upper
or lower canine. There are one lower and two upper premolars, and two upper
and lower molars. Small enamel ridges (flutings) vary in size and density on
cheek tooth cusps and basins. Upper premolars are broadly basined with main
cusps located peripherally. Lower premolar has an enlarged a1, which is
hypertrophic in Xianshouand Arboroharamiya
1
, but there is no serration. Cusp
A1 (distobuccal) of the upper premolar and molars is the largest and extends
distally. Cusp a1 (mesiolingual) of the lower molars is the largest cusp,
extending mesially.The lingual cusps of lower molars bear wear on theirlingual
sides, indicating that they bit into the central valley of the upper molars in
mastication. Molars have a fusiform (spindle-shaped) basin that is closed
mesially by a ridge in the upper molars and distally in the lower molars. The
ridge can be erased owing to wear so that the central valley becomes confluent
in Shenshou. Scale bars: ac,10mm;df, 2 mm. Cusp terminology follows
ref. 12. See photographs of teeth in Extended Data Figs 2, 4b, c, 5, 6 and 7a–c.
RESEARCH ARTICLE
2 | NATURE | VOL 000 | 00 MONTH 2014
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©2014
orientated ventrodorsally. A vestigial coronoid is present on the medial
side of the jaw (Extended Data Fig. 2b), posteroventral to M
2
, similar to
that of Arboroharamiya and the Jurassic multituberculate Kuehneodon
2
.
A reduced coronoid, usually indicated by a scar on the dentary, is also
present in some more advancedmammals, such as Amphitherium
3
and
Zhangheotherium
4
. This is in contrast to sizable coronoids that cover the
anterior portion of the postdentary unit in primitive mammaliaforms,
such as Morganucodon
5
and Haldanodon
6
. Unlike multituberculates
but similar to Arboroharamiya, thedentary has a small angular process
that inflects medially.
Dentitions are preserved in situ in the six specimens (Figs 1 and 2,
and Extended Data Figs 1–7), confirming the tooth identification and
orientation of Arboroharamiya
1
as well as reinterpretation
1
of some pre-
viously known euharamiyidans
7–10
. The cusp arrangement and mor-
phology from Haramiyavia,Thomasia,Arboroharamiya and the new
speciesreported here showconsistentlylarger row A cusps (buccal) than
row B cusps in upper molars, and larger rowa cusps (lingual) than row
b cusps in lower molars. In the lower cheek teeth,the mesiolingual cusp
(a1) is the largest, whereas the distobuccal one (A1) is the largest in the
upper teeth. The lingual lower cusp row bites into the central valley of the
upper molars as indicated by wear facets in the upper and lower teeth
(Extended Data Fig. 7a–c). These dental features and occlusal patterns
should also be applicable to those known only from isolated teeth, such
as Eleutherodon and Sineleutherus. It is also noteworthy that similar
tooth cusp morphology and occlusal patterns are present in the upper
and lower second molarsof some Jurassic multituberculates
11
, in which
the mesiolingual cusps are the tallest among cusps in the lower molar.
The molars with two rows of multiple cusps and their wear patterns,
coupled with the morphologies of the lower jaw and the glenoidfossa,
convincingly indicate palinal jaw movement during mastication
12
.
Postcranial skeleton
Although the vertebral column varies considerably in extant mam-
mals, particularly those from the southern continents
13
, the general or
primitive cervical and thoracolumbar counts for therian mammals are
conservative
14
. The axial skeleton of the new euharamiyidans is therian-
like in possessing 7 cervical and 19 thoracolumbar vertebrae (13 thoracic
and 6 lumbar; Fig. 3). In contrast to the docodontan Castorocauda
15
,the
eutriconodont Liaoconodon and Yanoconodon
16,17
, and the symmetro-
dont Akidolestes
18
, which all have lumbar ribs, euharamiyidans (includ-
ing Arboroharamiya) have true lumbar vertebraethat lack ribs but have
obliquely oriented facets of the prezygapophysis, elaboration of the trans-
verse process, and the laminapophysis (a mammalian neomorph that
split into the anterior metapophysis and posterior anapophysis)
19
(Fig. 3b).
These features define a distinct thoracolumbar boundary (Fig. 3a) and,
along with fixation of cervical vertebrae
20
and well-developed ribcage,
are indicative of development of the diaphragm, a unique feature that
allows mammals to progressively increase ventilation in adapting to
fast movement
19,20
.
5 mm
a
10 mm
bc
d e
f g
ltp Anapophysis
Metapophysis
L6 Anticlinal L4 L1 Diaphragmatic T13
Postparathrum
Clavicle Interclavicle
Manubrium
tm
sp
ce
ts
cu
cm
as en
ec
me
td
lu
Sternebrae 1-4
Costal
cartilage
Spine Acromion
Coracoid
Glenoid
Infraspinous
fossa
Entepicondylar
foramen
Entepicondyle Ulnar
condyle
Radial
condyle
Ectepicondyle
Xiphoid process
Preparathrum
hm
tq
ct
pi
Figure 3
|
Skeletal features of euharamiyidans. a, Reconstruction of the
skeleton of Shenshou lui, based in part on Xianshou linglong and Xianshou
songae.b, The vertebral column of Shenshou lui.c, The anterior section of
the rib cage in Shenshou lui.d, The right scapular of Shenshou lui.e,The
distal end of the humerus in Shenshou lui.f, Reconstruction of the hand of
Shenshou lui, based on LDNHMF2001 and WGMV-001. g, Reconstruction of
the foot of euharamiyidans, based on Shenshou lui (JZT-D061) and Xianshou
songae. The cervical ribs, present in monotremes and many Mesozoic
mammals
4,17,20,24
, are absent. Similar to therians, such as Eomaia
32
and
Sinodelphys
27
, the first ten thoracic ribs are connected to the ossified
manubrium and sterna via costal cartilages and the last three ribs float freely.
The capitulum of each rib articulates between two thoracic centra at a
ventral position. The last thoracic rib (13th) is identified as the diaphragmatic
vertebra because the articular facets of its zygapophyses with the first
lumbar are more vertical than horizontal, as in many extant mammals
49
.
The anticlinal vertebrate is located at lumbar four. The tail consists of 18–22
caudal vertebrae, with the proximal ones bearing expanded transverse
processes as in extant prehensile therians
50
. The scapular blade is roughly
rectangular and has a large and deep infraspinous fossa but lacks a
supraspinous fossa. The clavicle is strap-shaped and slightly curved anteriorly.
Its rough proximal end indicates a flexible contact with the depression on
the clover-leaf-shaped interclavicle. The distal end of the humerus has a
bulbous radial condyle, a relatively smaller spherical ulna condyle, and a
prominent entepicondyle. The femur has a hemispherical head with an
extensive articular surface but a short neck, the greater trochanter is triangular
and does not extend above the head. The distal condyles are small with a
shallow patellar groove. The ankles are comparable to those of
multituberculates, such as Kryptobaatar
24
, in that the calcaneus has a short
and mediolaterally compressed tuber calcanei and are partly superposed by
the astragalus. The cuboid is positioned obliquely and has little contact with
the calcaneus so that metatarsal V is separated from the calcaneus. The
entocuneiform is elongated, and its joint with metatarsal I is offset anteriorly
from the joint of the intermediate cuneiform and metatarsal II, similar to that
of Asioryctes and Eomaia
32
. Metapodials and proximal phalanges possess a
well-developed palmar groove for the digital flexor muscle tendon. Metatarsals
I and V are short and robust compared to others. The distal ends of proximal
and intermediate phalanges are well trochleated. Terminal phalanges are
compressed laterally and curved strongly with a sharp tip; each has a massive
digital flexor tubercle on the ventral side and a small dorsally extended ridge.
as, astragalus; ce, centrale; cm, calcaneum; ct, capitate; cu, cuboid; ec,
ectocuneiform; en, entocuneiform; hm, hamate; L, lumbar; ltp, lumbar
transverse process; lu, lunate; me, mesocuneiform; T, thoracic; td, trapezoid;
tm, trapezium; sp, scaphoid; pi, pisiform; tq, triquetrum; ts, tarsal spur. The
10 mm scale applies to panel aand the 5mm scale bar applies to all other
postcranial elements. See photographs of skeletons and postcranial structures
in Extended Data Figs 1, 3, 4a, 5a and 7d–g.
ARTICLE RESEARCH
00 MONTH 2014 | VOL 000 | NATURE | 3
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The scapula (Fig.3d and Extended Data Fig. 7g) is primitively similar
to that of Megazostrodon,Haldanodon and monotremes
21,22
in that it
lacks the supraspinous fossa, but differs from those taxa in that it has a
reduced coracoid that is fused to the scapula and forms a small part of
the glenoid fossa that faces ventrally. The clavicle (Fig. 3c) is similar to
that of multituberculates
23
. As in multituberculates the humerus has a
slight shaft torsion (approximately 15u)
23
, in contrast to a strong prox-
imodistal torsion in cynodonts and other early mammals
4,24
. The distal
end of the humerusis highly comparable to thatof multituberculates
23,24
(Fig. 3e and Extended Data Fig. 7e). In the wrist, the hamate is hyper-
trophied and the scaphoid and triquetrum are enlarged, as in some extant
arboreal marsupials
25,26
and the scansorial Sinodelphys
27
. Metacarpal V
is offset from the hamate and the pisiform is sizable, similar to those of
Zhangheotherium
4
(Fig. 3g and Extended Data Fig. 8a).
The epipubic bone, a plesiomorphic feature common in several groups
of Mesozoic mammals, including eutherians
28
, is absent. The pelvis is
similar to that of therians in being shallow and differs from the deep
pelvis of multituberculates and monotremes in having a reduced pubis
and an ischium with a straight dorsal margin and an ischial tuberosity
that is slender and less extended dorsoposteriorly
24
. The ilium is shorter
than that of multituberculates. The femur has a short neck, similar to
eutriconodonts
16,29,30
, symmetrodonts
4,18,31
and more primitive forms
21,22
,
but different from multituberculates, in which the femoral head has
a long neck and the greater trochanter projects beyond the head
24
.
There is no parafibula, differing from Eomaia and Jeholodens
30,32
. The
proximal end of the tibia is roughly symmetrical, contrasting to that of
multituberculates
33
. The bony extratarsal spur is distinctive and displays
different relative sizes in different species reported here. The spur or its
os calcaris exists in monotremes
34
and is common in Mesozoic mam-
mals and their close relatives
15,35
.AsinArboroharamiya and some extant
arboreal didelphids and cheirogaleid primates
1
, the manus and pes are
characterized by relatively short metapodials and long phalanges (Fig. 3f, g
and Extended Data Fig. 8). The limb features are collectively indicative
of scansorial and/or arboreal adaptation
1,26,32
.
Phylogenetic relationship
A major unsolved problem in mammalian taxonomy and phylogeny
concernsAllotheria(Multituberculata and Haramiyida)
9,12,33,36–39
,which
affects how we view the early ev olution of mammal s. Most recent studies
present contrasting hypotheses that either place allotherians in mammals
1
,
indicating an explosive model for the origin of mammals in the Late
Triassic (approximately 208 million years ago) and a long-fuse model
for the origin of therians, or separate them from multituberculates and
place them outside mammals
40
, suggesting an explosive model for the
origin of the Mammalia in the Middle Jurassic epoch. In light of the
new data reported here,we are able to revise characters used in previous
studies
1,11,40
, discuss existing problems relating to Megaconus (Supplemen-
tary Information, section E), the postdentary trough in ‘haramiyidans’
(now demonstrated to be a paraphyletic group) (Supplementary Infor-
mation, section F) and Hadrocodium(SupplementaryInformation, sec-
tion G) and conduct phylogenetic analyses including the new species
(Supplementary Information, sections H–J). The result shown in Fig. 4
(see also Extended Data Fig. 9) is consistent with most recent phyloge-
netic analyses
1,11,41,42
, which suggest that the ‘haramiyidans’ are related
to multituberculates to form Allotheria within the Mammalia. This sup-
ports a Late Triassic origin of mammals
1
. This hypothesis gains support
from some Late Triassic ‘symmetrodontans’, such as Kuehneotherium
and Woutersia, thatare considered taxonomically to be members of the
trechnotherian mammals
33,43,44
. Our analyses also recognize a new clade,
here named Euharamiyida, that pairs with Multituberculata; this is consis-
tent with the view that previously discovered ‘haramiyidans’ seem to form
a paraphyletic group, from which multituberculates were derived
12,36,39
.
Primitive species traditionally placed in ‘haramiyidans’, such as Hara-
miyavia and Thomasia, form the stem members of allotherians. This
resultant topology remains the same whether Megaconus was included
(Extended Data Fig. 10a) or both Megaconus and Hadrocodium were
excluded (Extended Data Fig. 10b) (see discussions in Supplementary
Information, sections E and G).
Character evolution of early mammals
With the discoveries of the new euharamiyidans, it becomes increas-
ingly evident that the cranial and postcranial features of euharamiyidans
and multituberculates are similar to each other and to other mammals.
However, the fundamental obstacle in interpreting their mammalian
affinity remains the fact that the toothpattern consists of two main rows
of multiplecusps that are capable of longitudinal (palinal)chewing func-
tion in allotherians
12,39,45
. If allotherians were placed outside mammals, it
is equally difficult to derive the allotherian tooth patter n from other mam-
maliaformes, such as tritylodontids. Our phylogenetic analyses (Fig. 4)
suggest that the primitive allotherian tooth pattern, as represented by
Haramiyavia, was probably derived by developing an extra cusp row,
Mammaliaformes Crown Mammalia
Allotheria
Euharamiyida
Cladotherians
(including metatherians and eutherians)
Multituberculata
220 200 180 160 140 120 100 80 60
Triassic Jurassic Cretaceous
Lower LowerMiddleUpper UpperMiddle Upper
Cenozoic
1
2
4
3
5
6
Thrinoxodon
Massetognathus
Probainognathus
Tritylodontids
Adelobasileus
Sinoconodon
Pachygenelus
Morganucodon
Megazostrodon
Haldanodon
Castorocauda
Hadrocodium
Monotremata and kin
Eutriconodontans
Haramiyavia
Thomasia
Cimolodontans
Plagiaulacids
Sinobaatar
Kuehneodon
Rugosodon
Shenshou
Arboroharamiya
Eleutherodon
Sineleutherus
Xianshou linglong
Xianshou songae
Tinodon
‘Symmetrodontans’
Figure 4
|
Phylogeny of mammals with focus on Allotheria. This simplified
cladogram is based on the consensus tree (Extended Data Fig. 9) computed
from a data matrix with 113 taxa and 495 characters (see Supplementary
Information). The dashed line of ‘symmetrodontans’ indicates occurrences
of taxa that existed in the Late Triassic, such as Kuehneotherium and
Woutersia
33,43
, but are not included in our phylogenetic analyses because of
their fragmentary preservation. Tree nodes represent the following clades:
(1) Mammaliaformes; (2) Mammalia; (3) unnamed clade consisting of
Eutriconodonta, Allotheria and Trechnotheria
33
; (4) Allotheria; (5)
Trechnotheria; and (6) Cladotheria. Mammaliaformes, Crown Mammalia,
Allotheria, Multituberculata and Euharamiyida are also marked as nested
colour blocks from the most to the least inclusive group.
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or rows, from a triconodont-like tooth pattern or even from a tooth pattern
with an initially reversed triangular cusp arrangement.It was noted that
in lateral view the teeth of Haramiyavia are more similar to those of
Sinoconodon and Morganucodon than to those of multituberculates
46
.
We note, however, that the tooth pattern of Haramiyavia is also similar
to that of Woutersia, which co-existed with Theroteinus, another Late
Triassicharamiyidan
36,43
. The tooth morphology and occlusionof euha-
ramiyidans indicate that, if the allotherian tooth pattern was derived
from a triconodont tooth pattern, the secondary cusp row has to be added
on the buccal side in the lower teeth. In the conventional view, how-
ever, development of extra cusps on the lingual cingula is common, but
buccal cingula are rare on lower molars
45
, although exceptions exist, such
as Hallautherium
47
. Nonetheless, the orientation of an isolated tooth
in early mammals is not always certain, as demonstrated in the case of
eleutherodontids
1
(this study). There is no convincing evidence to rule
out the possibility that additional cusps could be added on the buccal
side of the tooth in early mammals. Better material with teeth in situ
from each taxon of interest, such as Woutersia, is needed to test this
hypothesis.
Interpretations of character evolution in early mammals depends
on their phylogeny. If ‘haramiyidans’ were separated from multituber-
culatesand placed outside mammals, while multituberculatesfell within
mammals
40
, then numerous similar craniodental and postcranial fea-
tures, particularly the molar pattern with two cusp rows and bilateral
occlusion, must have evolvedindependently in ‘haramiyidans’ andmul-
tituberculates during different periods of time. In addition, detachment
of the postdentary bones from the dentary would have evolved at least
four times independently in ‘haramiyidans’, multitubuculates, mono-
tremes andtherians. However, our phylogeny (Fig. 4 and Extended Data
Figs 9 and 10) indicates that Euharamiyida and Multituberculata were
probably derived from a Haramiyavia-like commonancestor at a min-
imum oldest age (according to current fossil records; future finds may
reveal an earlier ancestor)in the Late Triassic and diversified thereafter
during the Jurassic epoch, with known euharamiyidans adapting to a
scansorial and/or arboreal lifestyle which may explain their rare fossil
record. In contrast to interpreting numerous parallelisms in ‘harami-
yidans’ and multituberculates
40
, our hypothesis favours homologous
acquisition of many similar craniodental and postcranial features in
euharamiyidans and multituberculates, such as reduction of teeth, enlarge-
mentof the lower incisors,possessing only twomolars in each side of the
upper and lower jaws, and a palinal chewing motion. Moreover, euhar-
amiyidans are similar to multituberculates in lacking the postdentary
trough and Meckelian groove, indicating the presence of the definitive
mammalian middle ear
3
. If the reinterpretation is correct—that the den-
tary of Haramiyavia has only the Meckelian groove (see Supplemen-
tary Information, section F)—then the clade containing Eutricondonta,
Allotheria and Trechnotheria
33
(Fig. 4 and Extended Data Fig.9) would
have evolved from a common ancestor that had a transitional mamma-
lian middle ear
16
. This clade and the geological and geographic occur-
rences of its earliest known members are consistent with accumulating
evidence fromGondwana landmassesthat shows a cosmopolitandistri-
bution ofmembers in the clade
48
and suggest a Laurasianorigin of mam-
mals. Finally, by reinterpretating Hadrocodium as having postdentary
bones (see Supplementary Information, section G), our phylogeny sug-
gests that detachment of the postdentary bones evolved twice indepen-
dently during the early evolution of mammals, once in the clade leading
to monotremes and once towards the clade containing Eutricondonta,
Allotheria and Trechnotheria.
Online Content Methods, along with any additional Extended Data display items
and SourceData, are available in theonline version of the paper;references unique
to these sections appear only in the online paper.
Received 11 April; accepted 25 July 2014.
Published online 10 September 2014.
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Supplementary Information is available in the online version of the paper.
Acknowledgements We thank H.-J.Li and Z.-J. Gao for using the specimens housedat
the JizantangPaleontological Museum;Z.-Y. Sun and D.-Y. Sun for using the specimen
housed at the Museum of Wuyishan Mountain; J.-C. Lu
¨for assistance in specimen
collecting;S.-H. Xie for specimen preparation; M. A. Klingler and F.-X. Wu for specimen
drawing and photography; W.-D. Zhang for SEM imaging;Z.-H. Zhou, X. Xu, F.-C. Zhang
and X.-L.Wang for discussion on stratigraphy and faunalcompositions; and A. Weiland
G. W. Rougierfor instructive comments.The study was supportedby the National Basic
Research Program of China (973 program, 2012CB821906), the Strategic Priority
Research Program of Chinese Academy of Sciences (XDB03020501), the National
Science Foundation of China (41128002) and the Hundred Talents Programs of the
Chinese Academy of Sciences.
Author Contributions S.B., J.M. and Y.W. designed the study, performed the
comparative andanalyticalwork and wrote the paper. J.G. and X.S. collected data and
contributed to the writing and discussion.
Author Information The LifeScience Identifiers (LSIDs) for this publication have been
deposited at http://zoobank.org/ and include: urn:lsid:zoobank.org:pub:766EBC08-
EF77-41E5-AC59-9F69E9F59BAA (for this publication), urn:lsid:zoobank.org:act:
32B0742D-2DD3-47F9-A35B-E1FB284E9EA5 (Shenshou), urn:lsid:zoobank.org:act:
BA8BF69D-0F21-4DE7-9EA5-BA6082973940 (Shenshou lui), urn:lsid:zoobank.org:
act:4C10F9F1-A920-450B-8E5F-C88F3BD0920C (Xianshou), urn:lsid:zoobank.org:
act:3DB1D738-70E9-4966-93FE-3FE5269F9C91 (Xianshou linglong), urn:lsid:
zoobank.org:act:1F7EEE49-5E88-4941-AE8B-B2C7C31F9788 (Xianshou songae).
Reprints and permissions information is available at www.nature.com/reprints. The
authors declare no competing financialinterests. Readers arewelcome to comment on
the online version of the paper. Correspondence and requests for materials should be
addressed to J.M. (jmeng@amnh.org) or Y.W. (wangyuanqing@ivpp.ac.cn).
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Extended Data Figure 1
|
The holotypes of three euharamiyidan species.
a, Holotype specimen (LDNHMF2001) and line drawing of Shenshou lui.
b, Holotype specimen (IVPP V16707A) and line drawing of Xianshou linglong.
c, Holotype specimen (BMNHC-PM003253) and line drawing of Xianshou
songae. as, astragalus; c, cervical vertebrate; ca, caudal vertebrate; cc, costal
cartilage; cm, calcaneum; ct, capitate; cu, cuboid; en, entocuneiform; fr, frontal;
hm, hamate; ic, interclavicle; ip, intermediate phalanges; l, lumbar vertebrae; lc,
left clavicle; lfe, left femur; lfi, left fibula; lh, left humerus; li, left ilium; lis, left
ischium; lm, left mandible; lra,left radius; lsc, left scapular; lpb, left pubis; lti, left
tibia; lu, lunate; lul, left ulna; m, maxilla; mb, manubrium; mc, metacarpal; mt,
metatarsal; n, nasal; pa, parietal; pi, pisiform; pm, premaxilla; pp, proximal
phalanges; r, rib; rc, right clavicle; rfe, right femur; rfi, right fibula; rh, right
humerus; ri, right ilium; ris, right ischium; rm, right mandible; rra, right radius;
rsc, right scapular; rti, right tibia; ru, right ulna; s, sacral vertebrae; sm,
septomaxilla; sp, scaphoid; sq, squamosal; stb, sternebra; t, thoracic vertebrae;
td, trapezoid; tm, trapezium; tp, terminal phalanges; tq,triquetrum; tr, thoracic
ribs; ts, tarsal spur.
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Extended Data Figure 2
|
Close-up views of craniodental structure of
Shenshou lui
(LDNHMF2001). a, The skull and mandibles of Shenshou lui
(LDNHMF2001). ap, angular process; m, maxilla; maf, masseteric fossa; n,
nasal; pal, palatine; pm, premaxilla; ptf, pterygoid fossa; sm, septomaxilla;
sq, squamosal. b, The lingual surface of the mandible of Shenshou lui
(LDNHMF2001). The close-up view shows the vestige of the coronoid bone at
the ventrodistal side of the ultimate lower molar and the wear facets on the
lingual sides of the lingual cusps of M
1,2
.c, The rostrum of the skull of Shenshou
lui (LDNHMF2001). The figure is a close-up view of the rostrum region in a.It
shows the relationship of the alveoli for P
3,4
with the molars and the wear facets
on the medial side of left I
2
.d, Photographs and stippling drawings of the
dentition of Shenshou lui (LDNHMF2001). The dentitions were coated with
ammonium chloride to enhance contrast. The holotype of Shenshou is an old
individual, judging from the deeper wear on its teeth. The mesial end of the
upper molar basin and the distal end of the lower molar basin appear to be
open, not closed by ridge or cusps, but this may be partly due to the tooth wear.
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Extended Data Figure 3
|
Paratypes 1 and 2 of
Shenshou lui
.a, Dorsal view of the skeleton of Shenshou lui (paratype 1, WGMV-001). b, The split skeleton of
Shenshou lui (paratype 2, JZT-CK005A, B).
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Extended Data Figure 4
|
Paratype 3 and skulls of paratypes 1 and 2 of
Shenshou lui
.a, Dorsal view of the skeleton of Shenshou lui (paratype 3, JZT-
D061). b, Ventral view of the skull of Shenshou lui (paratype 1, WGMV-001).
Note the bulging promontorium of the petrosal, the inflected angular process
and small right P
3
.c, Lateral view of the skull and mandible of Shenshou lui
(paratype 2, JZT-CK005).
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Extended Data Figure 5
|
Holotype and close-up views of craniodental
features of
Xianshou linglong
(IVPP V16707B). a, Counterpart of the
holotype specimen of Xianshou linglong (IVPP V16707B). ca, caudal
vertebrate; ip, intermediate phalanges; lfi, left fibular; lh, left humerus; lra, left
radius; lti, left tibia; lu, left ulna; mt, metatarsal; pp, proximal phalanges; r, rib;
rfe, right femur; rfi, right fibular; tp, terminal phalanges. b,c, Skull (two sides)
and mandibles of Xianshou linglong (IVPP V16707A). b, the skull (ventral
view) and left mandible (medial view) and right mandible (labial view). c,the
skull (dorsal view) andleft mandible (later view); ap, angular process;fr, frontal;
glf, glenoid fossa; hy, hyoid; ima, internal acoustic meatus; m, maxilla; mac,
mandibular condyle; maf, mandibular foramen; mtf, masseteric fossa; n, nasal;
pa, parietal; pm, premaxilla; sm,symphysis of mandible (left); vpt, ventral ridge
of pterygoid fossa; za, zygomaticarch. d, Photographs and stippling drawings of
the dentition of Xianshou linglong (IVPP V16707). P
3
is broken; its crown was
left in the matrix so that its outline can be reconstructed in the drawing. The
lingual side of P
4
and labial side of M
1
which are exposed or broken are line-
hatched. The dentitions were coated with ammonium chloride to enhance
contrast. e, Incisors of Xianshou linglong (IVPP V16707A).
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Extended Data Figure 6
|
Close-up views of craniodental features of
Xianshou songae
(BMNHC-PM003253). a, Photographs and stippling
drawing of the dentition of Xianshou songae (BMNHC-PM003253). The
distolingual corner of M
2
is not exposed, indicated by hatched lines. P
4
and M
1
are also shown flipped horizontally and the lingual sides of P
4
and M
1
are not
exposed, indicated by hatchedlines. The dentition was coated with ammonium
chloride to enhance contrast. b, The skull and mandibles of Xianshou songae
(BMNHC-PM003253). Note that the right upper and lower dentition are
preserved in occlusion, showing that lingual cusp A
1
of M
1
bites into the valley
of upper M
2
. amf, anterior border of the masseteric fossa; mac, mandibular
condyle; maf, mandibular foramen; ptf, pterygoid fossa. c, Teeth in situ of
Xianshou songae (BMNHC-PM003253).
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Extended Data Figure 7
|
Wear facets and skeletal features of
euharamiyidans. a, Left lower dentition of Shenshou lui (LDNHMF2001) in
lingual view. The image shows the wear facets on lingual sides of the lingual
cusps. b, Left P
4
–M
2
of Shenshou lui (LDNHMF2001), coated with ammonium
chloride to enhance contrast, in roughly occlusal view. c, Wear facets in the
basins of the P
3,4
and on the buccal sides of P
3
–M
1
. These wear facets indicate
that A
1
of P
4
must have occluded into the P
3,4
basins or moved from P
3
to P
4
basins. The wear facets also indicate that the lingual cusp rows of the lower
molars bite into the central valley of the upper molars so that the lingual and
buccal sides of the lingual lower cusps and the lingual side of the lower buccal
cusps bear wear facets. Similarly, the buccal sides of the buccal cusps of upper
molars have wear facets. d, Vertebral column in Shenshou lui. L, lumbard; ltp,
lumbar transverse process; T, thoracic. e, The distal end of the humerus in
Shenshou lui.f, The anterior section of the rib cage in Shenshou lui.g, the right
scapula of Shenshou lui.
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©2014
Extended Data Figure 8
|
Euharamiyidan manus and pes, and their ternary
plots. a, The manus of Shenshou lui (LDNHMF2001). b, The pes of Shenshou
lui (JZT-D061). as, astragalus; cm, calcaneum; ct, capitate; cu, cuboid; en,
entocuneiform; ip, intermediate phalanges; mc, metacarpal; mt, metatarsal; pi,
pisiform; pp, proximal phalanges; sp, scaphoid; td, trapezoid; tm, trapezium;
tp, terminal phalanges; tq, triquetrum; ts, tarsal spur. c, Ternary diagrams
showing intrinsic manual and pedal ray III proportions. Ternary plots showing
relative metapodial, proximal and intermediate phalangeal lengths for the third
digit ray of the hand and foot. The lengths of the third metapodial, proximal
phalanx and intermediate phalanx are shown on their respective axes as a
percentage of the combined length of the three segments. Compared to both
fossil and extant taxa, euharamiyidans have the intrinsic manual and pedal ray
proportions typical of arboreal species in which the proximal and intermediate
phalanges are long relative to the metapodials. Ar, Arboroharamiya jenkinsi;
Eo, Eomaia scansoria; Je, Jeholodens jenkinsi; Ma, Maotherium sinensis;Sb,
Sinobaatar lingyuanensis; Sd, Sinodelphys szalayi; Sh, Shenshou; Xl, Xianshou
linglong; Xs, Xianshou songae.
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Extended Data Figure 9
|
The strict consensus tree of 198 equally most
parsimonious trees. Tree length 52,509; consistency index (CI) 50.3304;
homoplasy index (HI) 50.6696; retention index (RI) 50.7901. The simplified
version of this consensus tree is presented in Fig. 4. Note that Tinodon was
placed as the sister taxon of Allotheria in this cladogram, which is inconsistent
with the taxonomic position of the genus
33
. This tree topology and that in
Extended Data Fig. 10b show the phylogenetic instability of Tinodon,asin
other studies
11,16,17,40
, that may be attributed to a significant amount of missing
data. However, the current phylogenetic position of Tinodon may reflect the
possibility that the allotherian tooth pattern, as represented by Haramiyavia,
was derived by developing an extra cusp row from a triconodont-like tooth
pattern or even from a tooth pattern with an initially reversed triangular cusp
arrangement, as discussed in the main text. Better material is needed to
secure the phylogenetic position of Tinodon and to test our hypothesis. See
Supplementary Information, section H, for methods as well as tree 1 and
related data.
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Extended Data Figure 10
|
Strict consensus trees with
Megaconus
and
without both
Megaconus
and
Hadrocodium
.a, The strict consensus tree
of 133 equally most parsimonious trees (including Megaconus). Tree
length 52,528; CI 50.3283; HI 50.6717; RI 50.7910. Note that Megaconus is
separated from allotherians and placed outside the crown mammals. This
suggests that the placement of Megaconus in allotherians
40
needs to be tested
when new material becomes available. See Supplementary Information, section
E, for discussion. b, The strict consensus tree of 101 equally most parsimonious
trees without Megaconus and Hadrocodium. Tree length 52,448; CI 50.3386;
HI 50.6614; RI 50.7952. See Supplementary Information, section G, for
discussion. Note that Tinodon is clustered with other ‘symmetrodonts’ plus the
clade leading to therians, and that eutriconodonts are split into two groups. See
Supplementary Information, sections E and G, for discussion.
RESEARCH ARTICLE
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©2014
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    Comparison of the early allotherian genera, Haramiyavia, Thomasia, Theroteinus, and Eleutherodon shows that their molariform teeth are variants of a common pattern, justifying the inclusion of these genera in a single order Haramiyida. Haramiyavia is made the type of a new family Haramiyaviidae. The order Haramiyida is divided into two suborders: (1) Theroteinida (only family Theroteinidae), and (2) Haramiyoidea (families Haramiyaviidae, Haramiyidae, Eleutherodontidae). Dental resemblances support the hypothesis that the Multituberculata originated within the Haramiyida, in which case the Haramiyida would be paraphyletic. Derivation of multituberculates from within the Mammaliaformes would involve a highly improbable transformation of the dentition. It is therefore postulated that allotherian (Haramiyida + Multituberculata) and non-allotherian mammaliaform clades separated before the Mammaliaformes developed a shearing dentition with unilateral occlusion and transverse jaw movements. This hypothesis implies that the two clades evolved to a large extent in parallel, to account for the apparent synapomorphies of multituberculates and therians.
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