LETTER doi:10.1038/nature12353

A new arboreal haramiyid shows the diversity of crown in the period

Xiaoting Zheng1,2, Shundong Bi3,4, Xiaoli Wang1,2 & Jin Meng3,5

A major unsolved problem in mammalian is the origin of Mammalia Linnaeus, 1758 , including and Haramiyida1–5. Multituber- Allotheria Marsh, 1880 culates are the most diverse and best known era mammals Hahn, Sigogneau-Russell and Wouters, 1989 and ecologically resemble , but haramiyids are known mainly Arboroharamiyidae gen. nov. from isolated teeth, hampering our search for their phylogenetic Arboroharamiya jenkinsi gen. et sp. nov. relationships. Here we report a new haramiyid from the Jurassic period of China, which is, to our knowledge the largest reported so Etymology. arbor (Latin): tree; Haramiya (Arabic): trickster, petty far. It has a novel , a resembling advanced multi- thief; jenkinsi: in honour of Farish A. Jenkins Jr for his contribution tuberculates and postcranial features adapted for arboreal . Our to the study of Mesozoic mammals, haramiyids included. phylogenetic analysis places Haramiyida within crown Mammalia, Holotype. A partial skeleton with both associated with teeth suggesting the origin of crown Mammalia in the Late period and isolated upper teeth (STM33-9, Tianyu Museum of , and diversification in the Jurassic, which contrasts other estimated Shandong Province, China; Fig. 1 and Supplementary Figs 1–7). divergence times of crown Mammalia6–8. The new haramiyid reveals Locality and horizon. The holotype is from the Middle– additional mammalian features of the group, helps to identify other in the town of Mutoudeng, Hebei Province, China, haramiyids represented by isolated teeth, and shows again that, dated about 160 million (Myr)9 (Supplementary Information). regardless of various phylogenetic scenarios, a complex pattern of Diagnosis. The largest known haramiyid with a body mass estimated evolution involving many convergences and/or reversals existed in at 354 g; dental formula I1?-C0-P2-M2/i1-c0-p1-m2; the enlarged lower Mesozoic mammals. fully covered with enamel; the only lower high, triangular

lm Figure 1 | The holotype specimen rm and line drawing of Arboroharamiya lc jenkinsi (STM33-9). The counterpart of the holotype is lra illustrated in Supplementary Fig. 1. lu ip ca, calcaneum; ca1–17, first to pp t tr rra seventeenth caudal vertebrae; ip, tr tp intermediate phalanges; ip2–5, l1 ru second to fifth intermediate tr phalanges; mc2–5, second to fifth lfe tp metacarpals; mt1–5, second to fifth l7 left metatarsals; mt2–5, second to lti li s1 ? s2 pp1–5 fifth right metatarsals; l1–7, first to lfi ri seventh ; lc, left ? mc2–5 ca1 rti clavicle; lfe, left femur; lfi, left fibula; lis rfe mt1–5 ip li, left ; lis, left ischium; lm, left ip2–5 rfi mandible; lra, left ; lti, left tibia; lu, left ; pp, proximal pp1–5 ip2–5 ca mt2–5 phalanges; pp1–5, first to fifth tp1–5 pp1–5 proximal phalanges; rfe, right femur; rfi, right fibula; ri, right ilium; rm, tp1–5 right mandible; rra, right radius; rti, right tibia; ru, right ulna; t, thoracic ; tp, terminal phalanges;

tp1–5, first to fifth terminal 5 cm 5 phalanges; tr, thoracic ribs; s1–2, first to second sacral vertebrae; ?, unknown element.


1Institute of Geology and , Linyi University, Shuangling Road, Linyi City, Shandong 276005, China. 2Shandong Tianyu Museum of Nature, Pingyi, Shandong 273300, China. 3Key Laboratory of Vertebrate Evolution and Origin of Chinese Academy of Sciences, Institute of and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China. 4Department of , Indiana University of Pennsylvania, Indiana, Pennsylvania 15705, USA. 5Division of Paleontology, American Museum of , Central Park West and 79th Street, New York, New York 10024, USA.

8 AUGUST 2013 | VOL 500 | NATURE | 199 ©2013 Macmillan Publishers Limited. All rights reserved RESEARCH LETTER in lateral view and lacking serrations; the lower having a greatly inflated mesiolingual (a1) and a central basin mesiodistally elong- ab ate and deeper distally than mesially; the upper dentition having at least 2 mm a multi-cuspate incisor, probably two and two molars; the distobuccal cusp (A1) the largest in the upper molars; the deep mandible lacking the postdentary trough and Meckelian groove but having a small angular process, a small coronoid process and a mandibular condyle that 10 mm levels with the row and is dorsoventrally oriented; limbs slim with i1 I1 proportionally short metapodials but long phalanges (Supplementary Information). Arboroharamiya, as with other mammals, has body (preserved as impressions), a single-boned (dentary) mandible that implies a three-boned , and the digit formula of 2-3-3-3-3. The den- P3 tition is differentiated into and multi-rooted premolars and A7 molars, with the canine presumably lost. It differs from other mam- c B7 A5 mals but is similar to allotherians in having two mesiodistally aligned p4 rows of cusps that allow orthal (vertical) and palinal (backward), but P4 not proal (forward) or transverse, movement in mastication. A2 B1 Arboroharamiya isalso similar toother haramiyids in having basined Mesial A1 M1 molars with cusps of uneven heights, but differs from them in being Buccal larger and having a more inflated a1 and elongate central basin surrounded m1 M1 by more cusps in lower molars. Arboroharamiya further resembles A1 a1 b1 multituberculates in having one pair of enlarged lower incisors, a a1 multi-cuspate upper incisor, loss of the canine, two upper and lower molars, and the mandibular with a mesially extended masseteric m2 M2 a7 b5 and a condyle positioned low and oriented more vertically than trans- m1 versely. It differs from the Jurassic multituberculates in having a small angular process and a highly specialized dentition with one lower Figure 2 | Teeth, mandibles and tooth occlusal relationships of premolar and two upper premolars and with an occlusal pattern in Arboroharamiya jenkinsi. a, Occlusal views of right upper and lower incisors which the enlarged a1 bites into the basin of the upper molar. (I/i), premolars (P/p) and molars (M/m). Some of the teeth (Supplementary Previously, the only known haramiyid with the mandible and den- Fig. 3) have been photographically flipped in the stippling drawings. The general shape of p4 is similar to that of Kermackodon, one of the earliest known tition preserved was Haramiyavia10, which was thought to resemble multitubuerculates4, but differs from it in lacking serrations. m1 and m2 are and in having the masseteric fossa similar in having a high and inflated cusp a1 with cusps decreasing height un-extended beyond the posterior part of the last molar, the condyle distally. The distal end of the central basin is closed by cusps. Enamel ridges above the level of the teeth, and presence of the postdentary trough2,5. extend distally from cusps towards the basin, which enhance grinding as A1 of Although Arboroharamiya is similar to in having a1 as the upper molar ‘moves’ in the valley. The upper premolar differs from molars the largest cusp and the lower molar basin deeper distally than mesially in being more rounded, with the broad central basin bearing numerous small and possessing a gracile postcranial skeleton, it is morphologically cusps or crenulations. Upper molars are more mesiodistally elongate and have more advanced than Haramiyavia in lacking the canine and having cusps A1 and A5 the largest and ridges extending mesially. Cusp B3 is the fewer incisors, premolars and molars. Most importantly, the dentary of largest in cusp B-row. b, Buccal (top) and lingual (bottom) views of the mandible show the anterior extension of the masseteric fossa to the level below Arboroharamiya is highly specialized and considerably different from p4 and lack of the postdentary trough (Supplementary Fig. 2). The empty that of Haramiyavia, but similar to those of derived multituberculates arrows point to the angular process. c, Line drawings illustrate the cusp such as taeniolabidids, in being short and deep and in lacking the numbering of M1 and m1 (right column) following ref. 2 and their relationship postdentary trough, which is one of the characteristics previously used in (upper left). Grey arrows show the relative movements of a1 of m1 to differentiate haramiyids from multituberculates2,5,10. and A1 of M1 (bottom left). Tooth identification, measurements and Assignment of tooth locus and thus identification of for most photographs in Supplementary Information. haramiyids are ambiguous because only isolated teeth are preserved1–5. The discovery of Haramiyavia10 helped to solve part of the puzzle. for the buccal row of the lower molar to bite into the valley of the upper However, because the upper premolars of Haramiyavia are not pre- molars. This is because the tall and inflated a1 at the longitudinal axis of served, the difference of the upper premolar and molar of haramiyids m1 and the distally closed central basin in lower molars prevent such remains unclear. In light of the new findings from Arboroharamiya an occlusion. The cusp shape and arrangement, wear pattern and occlusal (Fig. 2 and Supplementary Fig. 3), some haramiyid teeth identified as match of M1 and m1 show that, during mastication, a1 of the lower upper molars4,11 are most likely premolars. Similarly, the largest cusp molar must have bit orthally in the basin of the upper molar in the identified as b2 (mesiobuccal) in the lower molar of eleutherodontid puncture-crushing and then moved palinally within the basin in haramiyids2,11–13 is probably a1, and, if so, it would result in a different a grinding cycle (Fig. 2 and Supplementary Figs 3–6). In a reversed interpretation of the occlusal pattern in those haramiyids. symmetry, A1 of the upper molar bit into the central basin of the lower The occlusal pattern is a critical feature that was used not only to molar and ‘moves’ mesially in the valley of the lower molar. This identify tooth locus and species within haramiyids2,4,5, but more impor- ‘double engaged’ occlusion prevents both proal and transverse tantly to distinguish Allotheria from other Jurassic mammals that have motion; it creates wear in the tooth basin at the distal V-notch and on transverse jaw movement during mastication14. In Allotheria, the upper the buccal side of A1–3, but not the lingual side of M1. It also creates and lower molariform teeth have essentially two longitudinal rows of wear on the lingual and buccal sides of a1 in lower molars. This occlusal cusps, and the buccal row of the lower molar was considered to bite into pattern is unique among mammals and differs from what has been the valley between the two rows of the upper molar, involving orthal interpreted for both haramiyids and multituberculates2,4,10. The tooth and/or palinal jaw movement2–4. The tooth and wear morphology and occlusal pattern suggest that Arboroharamiya is pattern of Arboroharamiya confirm the orthal and palinal jaw move- probably either granivorous, as proposed for some haramiyids4,or ments in haramiyids, but nonetheless demonstrate that it is impossible omnivorous, as in multituberculates3.

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Postcranial features of Arboroharamiya show for an from haramiyids, with the latter being paraphyletic2,5,21. Because of arboreal life. The femur head is not spherical but cylindrical, a derived their unique dentition and early occurrences, allotherians were also feature present in omomyines and tarsiers15. Arboroharamiya has rela- considered to originate early from other mammals, even before mam- tively short metapodials but long phalanges (Fig. 1 and Supplemen- maliaformes in the Triassic2,4,5,22. Our phylogenetic analysis supports tary Fig. 7), unique among early Mesozoic mammals but characteristic the view that allotherians form a subgroup of the crown Mammalia3,23,24 of with prehensile and feet for arboreal life, such as and that multituberculates are derived from haramiyids2,5,21 (Fig. 4). arboreal didelphids and cheirogaleid primates16 (Fig. 3). Even among Because Haramiyavia10 and several other haramiyids5,10 are from the arboreal mammals Arboroharamiya is distinctive in that both manual Upper Triassic (the –Rhaetic), the age for the origin of crown and pedal phalangeal indices, estimates for degree of prehensility of the mammals would be in the time range of 228–201.3 Myr25, younger -foot17, are clearly higher than those of extant species16,18 and than that estimated in ref. 7 but older than those in other studies6,8. extinct scansorial/arboreal species, such as and With the ecological diversification recognized in early mammals26, our (Supplementary Figs 9 and 10). Moreover, the proximal caudal region phylogeny further implies that all major and feeding is relatively long and expanded transverse processes. The trans- of mammals had diversified during the Jurassic, coincident with inferred itional and longest caudal vertebrae are more distally positioned than diversifications of major lineages of insects27,28 and angiosperms29,30. those in nonprehensile taxa. These features are functionally related to Owing to the fragmentary nature of most haramiyids, a thorough the hypertrophy of the musculature necessary for increased gripping phylogenetic analysis of Allotheria remains impractical. However, strength indicative of prehensile ability, as in some extant arboreal 19,20 Arboroharamiya demonstrates convincingly that haramiyids had become species . The postcranial morphologies of Arboroharamiya suggest highly specialized in the Jurassic. It displays several mammalian features a gracile body for arboreal habitat preference. and fills some morphological gaps between Haramiyavia and multi- The phylogenetic relationship of Allotheria remains controversial. It tuberculates. Although morphological characteristics support allotherians was presumed that haramiyids and multituberculates were not closely 10 as a , Arboroharamiya shows again that homoplasy is a common related , or they formed a clade in which multituberculates are derived phenomenon within Mesozoic mammals1.SomefeaturesofArboroharamiya, such as the reduced dentition—shared with advanced multituberculates— 10 80 and elongated digits—shared with more advanced arboreal mammals— 20 must be convergences. On the other hand, the dentition with multiple 70 Proximal phalanx length (%) 30 60 220 200 180 160 140 120 100 80 60 Present 40 50 Triassic Jurassic Mid Late Early Mid Late Early Late 50 40 Ar 60 Sd Eo 30 Tritylodontids Intermediate phalanx length (%) Je 70 Sb Ma 20 Morganucodon 80 10 10 20 30 40 50 60 70 80 Metacarpal length (%) Ambondro 10 80 Steropodon 20 Proximal phalanx length (%) 70 Teinolophos 30 60 Fruitafossor Eutriconodonts 40 50 Haramiyavia 50 Arboroharamiya 40 Ar Plagiaulacidans 60 Sd Eo 30 Cimolodontans Intermediate phalanx length (%) Je 70 Ma Symmetrodonts Sb 20 80 10 10 20 30 40 50 60 70 80 Crown mammals Metatarsal length (%) Vincelestes Rodentia (terrestrial) Marsupialia (terrestrial) Dermoptera Nanolestes Rodentia (arboreal) Marsupialia (arboreal) Eutherians (placentals) Figure 3 | Ternary diagrams showing intrinsic manual and pedal ray III proportions. Ternary plots showing relative metapodial, proximal and Metatherians () intermediate phalangeal lengths for the third digit ray of the hand and foot. The lengths of the third metapodial, proximal phalanx and intermediate phalanx Figure 4 | Relationship of Arboroharamiya and geological distributions of are shown on their respective axes as a percentage of the combined length of the major groups of Mesozoic mammals and their relatives. Thin lines represent three segments. Compared to both and extant taxa, Arboroharamiya the phylogenetic relationships and thick lines indicate geological distributions jenkinsi has the intrinsic manual and pedal ray proportions typical of arboreal of the taxa. This is a simplified consensus tree (Supplementary Fig. 11) of species in which the proximal and intermediate phalanges are long in respect to 12 equally most parsimonious trees of PAUP (Phylogenetic Analysis Using the metapodials (Fig. 1 and Supplementary Fig. 7). Abbreviations: Ar, Parsimony and Other Methods, version 4.0b), an analysis of 436 characters and A. jenkinsi; Eo, Eomaia scansoria; Je, jenkinsi; Ma, 56 taxa with a focus on Mesozoic non-therian groups (modified from ref. 23; sinensis;Sb,Sinobaatar lingyuanensis;Sd,Sinodelphys szalayi. Measurements parts G–I in Supplementary Information). Test analyses for alternative and methods in part F of Supplementary Information. hypotheses are in part J of Supplementary Information.

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