4
Supplementary Information I
For
A Mesozoic Gliding Mammal from Northeastern China
Jin Meng, Yaoming Hu, Yuanqing Wang, Xiaolin Wang & Chuankui Li
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This file contains:
I-A. Preservation of the specimen
I-B. Age of the Daohugou Beds
I-C. Comparative description
I-D. Notes on Limb Measurements
I-E. Character list and data matrix
I-F. Phylogenetic analysis
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I-A. Preservation of the specimen
The specimen came from the Daohugou beds of the Daohugou locality, Ningcheng County, Inner Mongolia, China. It is a squashed skeleton, preserved in a tuffaceous shale slab that also contains numerous carapace valves of small conchostracans (Euestheria), the most common invertebrate fossils in the Daohugou beds (Shen et al., 2003). The slab slit through the skeleton and most part of the patagium so that the fossil remains are seen in part and counterpart (See Supplementary Figures S1-S10 in Supplementary Information II). The specimen was broken into several pieces. A main portion of the skeleton is preserved as a single piece in the part. Some parts of the counterpart are missing. Nothing has been added to the slab during the preparation and the broken pieces of the slab containing the skeleton remain separate. Some areas of the specimen have been briefly prepared to reveal critical structures. The removed matrix includes small patches of impressions that covered part of the foot. The impression continues into the area of the slab that was not split; therefore, the entire patagium is not completely exposed. Radiographic images reveal embedded bones, but not the impressions. Some bony structures such as the hip girdle and distal phalanges are missed. There is no duplicate or additional bony element was found in the disarticulated trunk region. The preserved limbs are largely in articulation. The parallel orientations of hair along some caudal vertebrae indicate originally anatomical relationships of the hair, skin and bones. These indicate that all the structures preserved in the split slab belong to an individual mammal.
Reference
Shen, Y. B., Chen, P. J., Huang, D. Y., 2003. Age of fossil conchostracans from Daohugou of Ningcheng, Inner Mongolia, Journal of Stratigraphy (in Chinese), 27(4): 311-313.
I-B. Age of the Daohugou Beds
Biostratigraphic and radiometric dating methods have generated inconsistent age estimates of the Daohugou beds. The estimates range from the Middle Jurassic (Chen et al., 2004; Liu and Liu, 2005), Late Jurassic (Zhang, 2002), or Early Cretaceous (He et al., 2004, 2005; Wang et al., 2005). In the study of the docodontan Castorocauda lutrasimilis (Ji et al., 2006), the age of the beds was cited as old as 164 million years. Although various age estimates are present, the consensus is that the Daohugou beds predate the Yixian Formation that produces remains of the Jehol Biota. The lower beds of the Yixian Formation were dated as about 125 Ma (Swisher et al., 1999; 2002). Therefore, the age of the Daohugou beds should be within the interval between 164 and 125 Ma. Because it is universally agreed that the Daohugou fauna is earlier than the Jehol Biota, we take a conservative age estimate of the Daohugou fauna and concluded that, given the earliest confirmed record of bats about 51Ma, the new discovery extends the earliest record of flight for mammals at least 70 million years earlier in the geological history.
References
Chen, W., Ji, Q., Liu, D.-Y., Zhang, Y., Song, B., Liu, X.-Y. Isotope geochronology of the fossil-bearing beds in the Daohugou area, Ningcheng, Inner Mongolia, Geological Bulletin of China (in Chinese), 23(12): 1165-1169 (2004).
He H.-Y., Wang X.-L., Zhou Z.-H., Zhu R.-X., Jin F., Wang F., Ding X., Boven A. 40Ar/39Ar dating of ignimbrite from Inner Mongolia, northeastern China, indicates a post-Middle Jurassic age for the overlying Daohugou Bed. Geophys Res Lett, 31, L20609, doi:10.1029/2004GL020792 (2004)
He H.-Y., Wang X.-L., Zhou Z.- H., Zhu R.-X., Jin F, Wang F, Ding X, Boven A. Reply to comment by Liu and Liu on ‘‘40Ar/39Ar dating of ignimbrite from Inner Mongolia, northeastern China, indicates a post-Middle Jurassic age for the overlying Daohugou Bed’’. Geophys. Res. Lett., 32, L12315, doi:10.1029/2005GL02278 (2005)
Ji, Q., Luo Z.-X., Yuan, C.-X. & Tabrum, A. R. A swimming mammaliaform from the Middle Jurassic and ecomorphological diversification of early mammals. Science 311, 1123-1127 (2006).
Liu, Y., and Liu Y. Comment on ‘‘40Ar/39Ar dating of ignimbrite from Inner Mongolia, northeastern China, indicates a post-Middle Jurassic age for the overlying Daohugou Bed’’ by H. Y. He et al., Geophys. Res. Lett., 32, L12314, doi:10.1029/2005GL022466 (2005).
Swisher, C. C. III et al. Cretaceous age for the feathered dinosaurs of Liaoning, China. Nature 400, 58-61 (1999).
Swisher C. C. III, Wang X.-L., Zhou Z.-H., Wang Y.-Q., Jin F., Zhang J.-Y., Xu X., Zhang F.-C., Wang Y. Further support for a Cretaceous age for the feathered-dinosaur beds of Liaoning, China: new 40Ar/39Ar dating of the Yixian and Tuchengzi formations. Chinese Science Bulletin 47: 135–138 (2002).
Wang, X.-L., Zhou, Z.-H., He, H.-Y., Jin, F., Wang, Y.-Q., Zhang, J.-Y., Wang, Y. Xu, X., and Zhang, F.-C. Stratigraphy and age of the Daohugou bed in Ningcheng, Inner Mongolia. Chinese Science Bulletin 50: 2369-2376 (2005).
Zhang, J.-F. Discovery of Daohugou Biota (Pre-Jehol Biota) with a discussion on its geological age. Journal of Stratigraphy 26: 173-177 (2002). (Chinese with English summary)
I-C. Comparative Description
The skull of Volaticotherium antiquus is partially preserved. The hard palate is fully formed and the incisor foramen, as a single opening, is immediately posterior to the incisors. On the lateral surface of the rostrum, the external naris is large, broader anteriorly than posteriorly. The premaxilla has a slim internasal process that extends posterodorsally and partly bounds the naris medially so that the right and left external nares are partly confluent. This condition is similar to that of Morganucodon (Kermack et al., 1981). The naris is also proportionally larger than those of Sinoconodon, Morganucodon, and nonmammalian cynodonts, which may be related to gliding life style. The infraorbital foramen is small and at the level of cusp B of M1. The anterior edge of the orbit is preserved and indicates a large eye. The left dentary, seen in its medial side, is largely preserved, with its coronoid process being partly broken. The mandibular symphysis is deepened to accommodate the strong and long root of the canine, as in many insectivorous bats (Novak, 1999). The dentary has a mandibular condyle that is lower than the tooth row, a small angular process anteroventral to the condyle, and a square-shaped coronoid process. The smooth medial surface of the dentary indicates that the postdentary elements were detached, a feature that characteristic of mammals. A slender groove may lead to an anteriorly positioned mandibular foramen.
The dentition of Volaticotherium antiquus is highly differentiated. There are three unicuspate upper incisors (I1-3) and two lower ones (i1-2), with i2 being reduced. Both upper (C) and lower (c) canines are long, sharp and slightly curved. There are four pairs of upper (P1-4) and lower (p1-4) premolariforms. P1-p1 are single-rooted and unicuspid; others are double-rooted with increasing height and complexity posteriorly. There is no cingulum (-id) on premolariforms. Upper molariforms are transversely narrow and have tall cusps that are posteriorly procumbent and deeply separated from each other. M1 bears three main cusps (denoted as cusps B, A and C, anteroposteriorly) of nearly equal height that are aligned in line, comparable to the tooth pattern of triconodonts (Crompton, 1971). The cusp tips are somewhat rounded compared to those of M2, suggesting wear of M1. M2 is longer than M1 and differs from the former in having a distinct cusp D immediately posterior to cusp C. M3 has three cusps, with cusp C reduced. The upper molariforms of V. antiquus are most comparable in size and shape with those of Ichthyoconodon, a purported eutriconodontan represented by two molariform teeth (which were identified as lower cheek teeth) from the Early Cretaceous littoral sediments, Morocco (Sigogneau-Russell, 1995). The molariforms of V. antiquus differ from those of Ichthyoconodon in having taller cusps that are more posteriorly recurved and in being less trenchant. The first lower molariform (m1) has four cusps (denoted as b, a, c and d, anteroposteriorly) that are deeply separated and posteriorly recurved at a greater degree than its upper counterpart. Although the tooth is anteroposteriorly long, it is not transversely compressed. The three anterior cusps of m1 are subequal in size and cusp d is the smallest and overlaps the anterolabial side of cusp b of m2. The m2 is smaller than m1 and has three main cusps and a reduced cusp d. A weak cingulid is along the labial base of m1 and m2.
Tooth germs under I1, I2, C, P3 and M1, revealed by breakage, indicate replacement of these teeth during ontogeny and that a replacement tooth is at the same position of its precursor. However, the specimen is probably not from a juvenile individual because the last molariform was erupted - no sign of an additional tooth in the dentary and maxilla as confirmed by breakage and X-radiographic and because skeletal elements are well ossified.
The tooth morphology of V. antiquus is most similar to, and probably derivable from, those of triconodonts, but its dentition is more specialized than those of triconodonts. In addition to the high, posteriorly procumbent cusps, the cheek teeth of V. antiquus differ from typical triconodont teeth in having a strong cusp b and cusp d of m1 labially overlapping cusp b of m2 but lacking an anterior accessory cuspate on lower premolariforms and the interlock relationship of molariform teeth. Moreover, the presence of a posteriorly positioned angular process on the dentary and the internasal process of the premaxilla further distinguishes V. antiquus from eutriconodontans, which have no angular process at all
The molariforms of V. antiquus is most comparable in size and shape with those of Ichthyoconodon (Sigogneau-Russell, 1995), a mammal represented by two molariform teeth from Early Cretaceous littoral sediments, Morocco. The teeth referred to as the lower molars of Ichthyoconodon may actually be upper cheek teeth because their similarities with the upper molariforms of V. antiquus. The molariforms of V. antiquus differ from those of Ichthyoconodon in having even taller cusps that are more posteriorly recurved and in being less trenchant. Several taxonomic allocations, Pterosauria included, have been entertained for Ichthyoconodon (Sigogneau-Russell, 1995); the current view is that Ichthyoconodon has the mammalian teeth of triconodont design but its teeth differ from other triconodontids in several aspects, making its affinities problematic (Cifelli et al., 1998: 239; Kielan-Jaworowska et al., 2004).
Some thoracic and/or lumbar vertebrate are preserved. These vertebrae are disarticulated and are typical of mammals with a platycoelous centrum. The neural process is low in all preserved vertebrae and the vertebral canal is large. At least 18 caudal vertebrae are recognized, indicating a long and robust tail. A distinct feature is that the caudal vertebrae are elongated, broad and dorsoventrally flat with a low dorsal, longitudinal ridge. The haemal arch that bridges two adjacent caudal vertebrae is also long and flat. These morphologies and the preserved relationship of the caudal vertebrae with the patagium indicate that the tail probably participated in supporting the patagium; thus, an uropatagium was present between the tail and the hindlimbs. The morphologies also suggest a stiff tail that had limited sideway movement and acted as a stabilizer when the animal was gliding, which is consistent with the prediction that longitudinal control and stability of a glider are archived more easily with a long, dorsoventrally flattened tail (Norberg, 1985a, b; Lindenmayer, 2002).
Hindlimbs are preserved nearly in articulation. The femoral head is small, oval-shaped and the femoral neck is absent. All preserved limb elements are elongated compared to those of other Mesozoic mammals (see Suppplementary Information III for measurements). The right pes was twisted or flipped in relation to the tibia and fibula. The calcaneus in the ankle is large and flat, with a broad, rounded peroneal process, similar to that of morganucodontids (Jenkins and Parrington, 1976; Szalay, 1994). The pes has five digits and have the following features: the hallucal metatarsus articulates with a large entocuneiform, with their articulation being more distal to that between the second metatarsal and mesocuneiform; the hallux diverges medially at an 35º angle from Mt II; the peroneal process of the hallucal metatarsus is enlarged; both metatarsals and proximal phalanges are dorsally arched with paired sesamoid bones them; the proximal phalange is relatively long compared to the metatarsal; the flexor sheath ridges are pronounced and flare outward so that the ventral surface of the proximal phalange is actually a longitudinal groove and its mid-shaft diameter is relatively broad; a large sesamoid is at the distal phalange joint of the hallux; the proximal end of the intermediate phalange is dorsoventrally deep, corresponding to a robust and well-trochleated distal end of the proximal phalange; the terminal hallucal phalanx is large and mediolaterally compressed, indicating a large, deep claw. The manus was poorly preserved, with only four digits being partially preserved. Nonetheless, as in the pes the metacarpals and proximal phalanges are dorsally arched, with the latter being proportionally long in comparison with the former; the proximal phalanges have strong flexor sheath ridges and similar proximal and distal articulation of the pedal elements. These features are significantly different from those that have a more general locomotion adaptation, such as morganucodontids (Jenkins and Parington, 1976), but are similar to arboreal and gliding mammals such as Carpolestes, paromomyids, Cynocephalus, and gliding squirrel Anomalurus, as results of adaptation for vertical postures and climbing in similar arboreal environments (Block et al., 2002; Hamrick et al., 1999; Beard, 1990, 1993). The climbing ability would be essential for V. antiquus to obtain altitude to a launch point of glide and to exploit terminal branch habitats.
Although we recognized the specimen as from a mammal by its dentition and skeletal features, we first compared it with pterosaurs for several reasons. First, Jeholopterus, a small anurognathid pterosaur with short rostrum and wing membrane covered with “hairs” (Wang et al., 2002) and Pterorhychus, a long-tailed rhamphorhynchid (Czerkas and Ji, 2002), have been known from the same locality. Second, some early pterosaurs, such as Eudimorphodon, have specialized dentition comprising uni-, tri-, and even pentacuspid teeth (Wellnhfer, 2003). Finally, pterosaurs are the only known Mesozoic animals from the area that have furry flying membranes.