Yuanqing Wang Yaoming Hit Chucmkui Li

Mammalia is biologically the most differentiated group of vertebrates, consisting of all the living mammals, their common ancestor, and their extinct allies. Mammals have predominated the modern terrestrial ecosystems throughout the Cenozoic lira since some 65 million years (Myr) ago, which is thus often referred to as the "Age of Mammals". However, the first two-thirds of mammalian history occurred in the preceding Mesozoic Era that extended from roughly 250 to about 65 Myr before present. After their first appearance in the Late Triassic (about 220 Myr ago) and throughout the remainder of the Mesozoic, mammals shared the earth with some great reptiles such as dinosaurs. During all that time, mammals were small and scarce, and lived in the shadow of dinosaurs. Mammals, however, outsmarted dinosaurs by surviving through the mass extinction at the end of the Cretaceous and became dominant on the earth's landmasses afterwards.

Mammals lived in the Mesozoic Era tor about 1 55 Myr, but their fossil record is rather poor and fragmentary. Unlike the uniform teeth of reptiles, mammalian teeth differentiated into four kinds: incisor, canine, premolar, and molar, with each kind performing a different function. Based mainly on the dental morphology, Mesozoic mammals are grouped as Triconodonta, Docodonta, Multituberculaca, Symmetrodonta, Eupantotheria, Monotremata, Marsupialia, and Eutheria. Among them, only the last three groups are still living on earth today. Before the recovery of mammals from thejehol Biota, ten localities had been reported to yield Mesozoic mammal fossils in China. Of them, only the Early Jurassic Lufeng of Yunnan Province in southwestern China produced some well-preserved specimens, including a number of skulls of triconodonts, such as Simconodon and Morgant/codott. Fossils from the other sites were generally represented by fragmentary jaws. From the Middle Jurassic coal-bed of northeastern China was reported the first Chinese Mesozoic mammal, Manchurodon. Later, two other mammals, Endothelium and Liaotherium, were discovered in that area.

In 1992, the first mammal of thejehol Biota was unearthed near a small village, Jianshangou of western Liaoning Province. It was named

Zhangheothenum quinqueatspidem in 1997. Since then, six other mammalian species have been reported from thejehol Biota. Compared to many other kinds of animals in the fauna, especially to the feathered dinosaur-bird lineage and a variety of invertebrates, mammals were not at all that rich. Despite this, fossil mammals of the Jehol Biota are an important and integrative part of the Mesozoic mammalian history. The exceptionally well-preserved materials provide critical evidence for understanding the transition of mammalian characteristics and reconstructing the phylogeny of early mammals. These fossils have shown a fairly high diversity of Mammalia in eastern Asia during the Early Cretaceous and represent four major mammalian groups: triconodonts, multituberculates, symmetrodonts, and eutherians. In the following paragraphs, they will be briefly introduced in systematical sequence.

Triconodonts Triconodonts consist of the most primitive known mammals and some of their derived relatives. As their name implies, their basic dental structure comprises three major cusps anreroposteriorly aligned, whereas some advanced forms have an enlarged fourth cusp on the distal margin. The triconodont lineage spans the entire Mesozoic mammalian history from the Late Triassic to Late Cretaceous. Although abundantly represented by teeth and some cranial and postcranial materials, fully articulated skeleton of triconodonts was yet unknown until the discovery of triconodonts in thejehol Biota.

The first triconodont reported from thejehol Biota isJebolodens jenkimi (Figs. 195, 196). It was represented by a nearly complete skeleton consisting of a partial skull and the whole postcranial skeleton preserved as two counterparts and was described by Q. Ji and others in 1999.Jebolodens is distinctive from the other primitive mammals in having diagnostic features: dental formula (i.e., number of incisors, canine, premolars, molars on each side of the upper/lower jaw) 4-1-2-3/4- i -2-4; buccolingually compressed molars with three main cusps in a straight alignment, and possessing spoon-shaped incisors that is uniquely derived among triconodonts.

The articulated type specimen of Jebolodens jettkinsi shows a mosaic of derived, therian-like characters for most parts of the shoulder girdle and the


«■196 Reconstruction of Jeholodens jenkinsi. (Art: Mark A. Klingler/ CMNH)

«■■195 I lolotype ofJeholodensjenkinsi, a triconodont)skull length about 2 cm), from Sihetun locality (lower part of Vivian Formation) in Beipiao, Liaoning. (I'hoto; CM NII)

«■196 Reconstruction of Jeholodens jenkinsi. (Art: Mark A. Klingler/ CMNH)

humeri, but very primitive characters for the vertebral column, pelvic girdle, hind limbs and pedes. Q. Ji and others interpreted the mosaic of derived and primitive features in Jeholodens as either the derived shoulder girdle and forelimbs representing convergence with those of multituberculates-therian clade, or the primitive shoulder girdle and forelimbs in monotremes being atavistic reversals to the ancestral conditions in the more distantly related non-mammalian cynodonts.

One year after the report of Jeholodens, J.-l. Li and her colleagues described another triconodont, Repenomamus robust us, based on a fairly well-preserved skull and some associated postcranial bones (Figs. 197, 198). Several additional specimens were collected from the same locality after the first report of this animal. It is the largest mammal known from the Mesozoic Era in the world. The skull is 108 mm long in the holotype and 114 mm in another specimen. The dental formula of Repenomamus robustus is 3-l'2 *4/3-1-2-5 (Figs. 198). On its upper molars, the middle one of three main cusps is large and the other two are weak, without distinct ectocingulum (a girdlelike structure on labial margin of the tooth). Besides the large size and the dental features, Repenomamus further differs from other Mesozoic mammals in the following character combination: short dorsal process of premaxilla not contacting the nasals; retainment of a large septomaxilla; short and low sagittal crest; well-developed lambdoid crest; and the sloping occipital surface exposed in dorsal view of the skull.

The most striking feature of these Repenomamus specimens is the presence of a separate bone attached to the medial side of dentary. The dentary is the single lower-jaw bone of all the living and most extinct mammals. In the mammallike reptiles and most primitive mammals, however, the dentary, together with postdentary bones (usually include articular, prearticular, angular, and surangular), constituted the lower jaw. During the early evolutionary stage of mammals, the postdentary bones greatly reduced and either shifted into the ear region (becoming the ear ossicles and part of bulla) or fused to the dentary. The peculiar bone on the lower jaw of Repenomamus is rodlike, with a pointed anterior tip and a flared posterior end (Fig. 197). Its anterior portion is lodged in a depression that appears to be an expanded posterior portion of the meckelian groove. Because there is no other scar on the dentary, it can be inferred that all postdentary bones in Repenomamus have been detached from the dentary. Structures of the ear region and their small dimensions indicate that in relation to the sizes of the skull and mandible, the ear ossicles in Repenomamus must have been reduced in size.

Auditory Ossicles With Scar Tissue

mbi 198 Skull of Repenomamus robostus in anterior (Upper) and lateral views lLower), showing the tooth morphology. (Photo: Jin Meng/AMNH)

1197 Skull (108 mm longl of the holotype of Repenoniamus robustus, the largest Mesozoic mammal to date, in dorsal (Left) and ventral (Right) views, from Lujiatun locality (lowest Yixian Formation) in Beipiao, Liaoning, red arrow denoting the ossified Meckel s cartilage on the lower jaw. (Photo: Jin Meng/AMNH)

Therefore, it is reasonable to conclude chat the rodlike bone attached to the denrary is not any of the postdentary bones. Embryological studies of living mammals have demonstrated the whole process from the posterior part of the Meckel's cartilage to the ear ossicles, and anatomical research reveals the Meckel's cartilage lying in an internal groove ol the dentary in prenatal and some postnatal extant marsupials, monotremes, and eutherians. The shape of the separate bone and its relation to the skull in Rtpenomamus are closely comparable to those of the Meckel's cartilage in the aforementioned living mammals. We identified this peculiar bone as the ossified middle portion of the Meckel's cartilage in 2001. This finding, for the first time, documented the Meckel's cartilage ossified in fossil record and provided direct evidence for its persistence in adults of the common ancestor of living mammals.

This has been strengthened yet by another partial skull with both lower jaws from the same locality that also preserves the ossified Meckel's cartilage. The specimen represents a new species of Gobiconodon, also a triconodont (Fig. 199). This genus is phylogenetically closely related to Rcpenomamm and has been previously known from the Early Cretaceous of both North America and Asia. Its dental formula is 2 I-4-4/1 • I -4-5. In 2003, C.-k. Li and his colleagues named it Gobiconoclon zofiae.

Discovery of the ossified Meckel's cartilage helps interpret the function of the internal groove on dentaries of many early mammals. The groove has been variably considered as holding dental nerves and/or arteries, or the Meckel's cartilage, or even as facets tor the postdentary bones. Because of the presence of such a groove in a number of phylogenetically derived mammalian forms, the interpretation for the persistence of the postdentary bones in these taxa argues for multiple origins of (he definitive triossicular mammalian middle ear. The discovery of the ossified Meckel's cartilage from the internal groove of the dentary in Repenomamus and Cobiconodon clearly shows the function of the groove as holding the cartilage. This in turn suggests that in early mammals a Meckel's cartilage, whether ossified or not, should be considered as a potential, or even primary, occupant for the internal groove. Thus, this extrapolation no lunger calls for multiple origins of the triossicular mammalian middle ear.

Multituberculates Multituberculates first appeared in the latest Triassic and became extinct in the late Eocene of the Cenozoic lira. They are frequently called "rodents of the Mesozoic". due to their superficially rodentlike features, such as the pair of enlarged and procumbent lower incisors. In later forms, the first pair of lower incisors is chisellike and only the ventral side is covered by enamel, which is especially similar to those of rodents. But, unlike rodents, multituberculates usually have more than one pair of incisors. In the mid-portion of the lower dentitions of most multituberculates, premolars are modified into bladelike structure. Their molars have varying number (from several to more than a dozen) of

)9 Holotype of Cobiconodun zofiae (skull length 45 mm), showing cranium in lateral (Upper) and ventral (Middle) views and lower jaw in labial and lingual views (Lower), from Lujiatun locality (lowest Yixian Formation) in Beipiao, Liaoning, red arrow denoting the ossified Meckel's cartilage. (Photo: IVPP)

200 Holoiype of Sinnboatar Hngyuanensis (Slab A, skull length 2G.f> mm), a multituberculate from Dawangzhangzi locality (middle part of Yixian Formation) in Lingyuan. Liaoning. (Photo: 1VPP)

200 Holoiype of Sinnboatar Hngyuanensis (Slab A, skull length 2G.f> mm), a multituberculate from Dawangzhangzi locality (middle part of Yixian Formation) in Lingyuan. Liaoning. (Photo: 1VPP)

1201 A bladelike premolar on the lower jaw o fSinobaatar lingyuanensis (cast), (Photo: Jin Mc-ng/ AMNH)

a^Êl.' I lylijtype oF%hangiw0liiciuwi quwqueais'pidens, .1 symmetrodonr (skull 353 mm),Tram r* Í s h an^ (3 u jocálity/foWr part of Yixjan

Formation in Ikipw'tiaomns, fEhótor ¡VPP)

mm 203 The upper and tower tooth rows and the lower jaw of Zhangheotherium quinquecuspidens,

Tibialis Anterior Tendon

mm 204 Reconstruction of the ear region of Zhangheotherium quinquecuspidens, showing the finger-shaped Promontorium (denoted by a red arrow! thai houses the cochlea, implying its auditory system not very sensitive to high frequency sound.


tuberclelike low cusps, from which they derived their name. Distinct changes in their dental morphology through time are characterized by the decrease in the number of premolars, the increase in the number of serrations and ridges on the bladelike last lower premolar and in the number of molar cusps.

To date, only one species of multituberculates has been recovered from the Jehol Biota. Y.-m. Hu and Y.-q. Wang, in 2002, named it Sinobaatar lingyuanensis (Fig. 200). The type specimen represents a subadult. Its body length, from the tip of rostrum to the hip, is about 10.3 cm. Its dental formula is 3-?"5-2/l-0-3'2. Differing from later multituberculates, the first lower incisor of Sinobaatar is conical and completely covered by enamel. The bladelike middle portion of the lower dentition involves three premolars (Fig. 201). Sinobaatar has the same dental formula as and similar dental morphology, especially of the cheek teeth, to that of some Early Cretaceous multituberculates from Mongolia.

The holotype of Sinobaatar lingyuanensis is the most complete pre-Late Cretaceous multituberculate specimen. It also provides new morphological information of postcranial skeleton previously unknown for early multituberculates. In contrast to the significant changes of their dental features, the available information shows little change in the postcranial morphology of multituberculates during their history. This may suggest that the locomotory patterns in different multituberculates did not change much during evolution. Their morphologically generalized postcranial skeletons indicate that they lived on a variety of substrata.

The specimen of Sinobaatar by far reveals most morphological information on multituberculate hand. The wrist structure of Sinobaatar is very similar to that of Kryptobaatar, a Late Cretaceous multituberculate of Mongolia, and that of Zhangheotherium, a symmetrodont from the Jehol Biota. Sinobaatar has well-preserved feet and resembles Ptilodus, a Paleocene multituberculate of North America, in having a large tibial condyle, and asymmetrical but widely movable astragalotibial joint, etc. Based on the foot and ankle structure, plus the long and prehensile tails, F. A. Jenkins, Jr. and D. W. Krause reconstructed Ptilodus as an arboreal animal, a lifestyle that may also be shared by Sinobaatar.

Symmetrodonts Symmetrodonts were shrew-sized mammals, characterized by the triangular, imperfectly symmetrical cusp arrangement of both upper and lower molars. The orientation of the triangles on the upper and lower molars is reversed — the central cusp is at the lingual side on the uppers, while at the buccal side on the lowers. The earliest symmetrodonts were found in the latest Triassic to earliest Jurassic of Wales, while their latest record was from the Late Cretaceous of North America.

Y.-m. Hu and his colleagues reported a symmetrodont mammal, Zhangheotherium quinquecuspidens, from the Jehol Biota in 1997 (Figs. 202—205). It is the first mammal known from the Biota and is represented by a well-preserved skeleton consisting of a partial skull and most of the postcranial skeleton, including all cervical and thoracic vertebrae, forelimbs and pectoral girdle, as well as excellent impressions of the hind limbs, pelvic girdle, and ribs. The dental formula of Zhangheotherium is 3T-2-5/3T-2-6 (Fig. 203). This animal is diagnosed by having blunt trigonid cusps, weak cristids, large cingulid cuspules, and no labial and lingual cingulids. Before the discovery of Zhangheotherium, symmetrodonts were only known from the fragments of upper and lower jaws. The nearly complete skeleton of Zhangheotherium reveals some valuable morphological information for this group.

One of the most interesting cranial features is related to auditory apparatus. Although fractured and distorted in preservation, the petrosal bone of Zhangheotherium is complete. Its promontorium, in which the cochlea is housed, has a cylindrical and fingerlike shape (Fig. 204), similar to those of triconodonts and multituberculates. This kind of promontorium is closely correlated with either a straight or slightly curved (but uncoiled) cochlea, a spiral-shaped cavity of the inner ear. An uncoiled cochlea was, therefore, inferred for Zhangheotherium. This means that the hearing function of Zhangheotherium was not as well-developed as in most of more derived mammals.

The shoulder girdle and forelimbs of Zhangheotherium are the best-preserved and most informative parts in its postcranial skeleton. The clavicle of Zhangheotherium is rodlike and in similar shape to that of marsupials and placentals. But, unlike marsupials and placentals, a separate interclavicle is present anterior to the sternum (breastbone) and between two clavicles. In marsupials and placentals, interclavicle does not exist as a separate bone, whereas it is very large in monotremes (e.g. platypus and echidnas) and acts as primary supporting structure. Unlike monotremes where the davick-interclavicle joint is fixed, Zhangheotherium has a mobile clavicle-interckvicle joint, which allows the clavicle to move in a wider range and further results in free movement of forelimbs.

■«206 Holotype of Eomala scansoria (Slab A. skull length about 3 cm|, an eutherian. from Dawangzhangzi locality (middle part of Yixian Formation) in Lingyuan, Liaoning. I Photo: CMINH)

In extant land mammals, marsupials and placentals move in a parasagittal posture, i.e., the fore and hind limbs straight under the body during movement, while monotremes in a sprawling posture with legs extending laterally in certain extent. Comparative anatomical study shows that different postures are related to morphology of limb bones. The forelimbs of Zhangheotherium have some features similar to those of therian mammals with parasagittal posture. However, they also retained some primitive characters that are common in the known non-therian mammals having a sprawling posture. The combination of both primitive and derived features of forelimbs probably suggests that Zhangheotherium has a forelimb posture intermediate between that of the sprawling monotremes and that of the parasagittal therians.

Early in 2003, G. W. Rougier and others reported another symmetrodont, Maotherium sinensis, from the Jehol Biota. It is represented by a fully articulated skeleton and closely related to Zhangheotherium. Although differing in some details, they share many morphological features of cranium, dentition, and postcranial skeleton, and thus are grouped into the same family.


Eutherians Eutherians are a group of mammals consisting of extant placentals and their extmci close relatives. They share the most recent common ancestor with marsupials. The number of molars distinguishes eutherians (three molars on each side for both upper and lower dentitions) from marsupials (four upper and four lower molars). The earliest record was previously documented in the late Early Cretaccous (Ca, 110 Myr ago). In 2002, Q. Ji and his collaborators reported an eutherian mammal, Eomaia scaast/ria, from thejehol Biota (Figs. 206, 207). It is the earliest representative of eutherians so far known in the world. The animal has specialized limb and foot features that are only known from scansorial (climbing) and arboreal (tree-dwelling) extant mammals, quite different from the terrestrial or cursorial (running) features of other Cretaceous eutherians. This suggests that the earliest eutherian lineages developed different locomotor)- adaptations, facilitating their spread to diverse ecological niches in the Cretaceous.

The phylogenetic relationships of early mammals are of great interest to paleumammalogists. Mammalian fossils from thejehol Biota are either the best-preserved or the earliest occurred specimens within their respective group. Therefore, they provide a new insight into the relationships of the major lineages of mammals and the evolution of the mammalian skeleton. Different phylogenetic analysis shows some uncertainties, but the results arc-not strongly conflicted with each other and show the evolutionär)- trends of some major mammalian characters. Given the framework of these results (Fig. 208), it Seems safe to make che following conclusions: (I) The absence of a coiled cochlea in Zbangbtothtrium is best considered primitive, i.e., a coiled cochlea yet to be evolved. (2> The parasagittal forelimb posture of living therians was not present in monorremes, mulriruberculates, and many Mesozoic mammals such as Zbangbeotberium, Henkelotberium and VinaUstes. It probably arose in later stage of mammalian evolution. (3) The presence of definitive triossicular mammalian middle ear in Rtptnvmi/m/fs and GobiconoJon provides evidence for its wide distribution in the mammals.

- Tritylodontidae






L -Priacadon



- Monotremata

- Multituberculate (e.g.. Sitniliautor)


- Maotherium



- Metatheria

«■208 Cladogram showing mammalian phylogenetic relationships, combining results of different analyses related to the Jehol mammals (in red).

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