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Science Journals RESEARCH | REPORT PALEONTOLOGY the hyoid apparatus in monotremes and placen- tals, and in a modified condition in marsupials (for details, see the supplementary materials) New Jurassic mammaliaform (16–18). Based on the distinctly mammal-like morphol- sheds light on early evolution ogy of the hyoid elements of Microdocodon,we can now identify hyoid elements of several other mammaliaforms (16)(figs.S4toS9).TheJurassic of mammal-like hyoid bones haramiyidan Vilevolodon has preserved basihyal 1,2 3 4 and ceratohyal bones (fig. S6 and movie S2) (19). Chang-Fu Zhou *, Bhart-Anjan S. Bhullar *, April I. Neander , The Cretaceous eutriconodontan Yanoconodon 5† 4† Thomas Martin , Zhe-Xi Luo also has preserved hyoid elements (fig. S6) (20). Computed tomography (CT) scanning has re- We report a new Jurassic docodontan mammaliaform found in China that is preserved vealed the basihyal, thyrohyals, ceratohyals, and with the hyoid bones. Its basihyal, ceratohyal, epihyal, and thyrohyal bones have mobile epihyals of the trechnotherian Maotherium and joints and are arranged in a saddle-shaped configuration, as in the mobile linkage the multituberculate Sinobaatar of the Cretaceous of the hyoid apparatus of extant mammals. These are fundamentally different from (figs. S7 and S8 and movie S2) (16). Addition- the simple hyoid rods of nonmammaliaform cynodonts, which were likely associated ally, Sinobaatar has preserved stylohyal bones with a wide, nonmuscularized throat, as seen in extant reptiles. The hyoid apparatus (fig. S7), which is similar to the Cretaceous multi- provides a framework for the larynx and for the constricted, muscularized esophagus, tuberculate Kryptobaatar (21). We interpret this crucial for transport and powered swallowing of the masticated food and liquid in extant to mean that multituberculates have an integro- Downloaded from mammals. These derived structural components of hyoids evolved among early cornuate anterior hyoid cornu, characterized diverging mammaliaforms, before the disconnection of the middle ear from the by the complete series of ceratohyal–epihyal– mandible in crown mammals. stylohyal connected to the basicranium (movie S2) (16).Moreover,wenowcanidentifythehyoid arly diverging mammaliaforms of the Meso- community of Daohugou (7, 11, 12, 16). Its skel- elements in the early eutherian Eomaia (fig. S9) “ ” zoic are the nearest predecessors to modern eton shows a T -shaped interclavicle, curved (16), which are similar to those of the recently http://science.sciencemag.org/ Mammalia (1) and provide direct fossil evi- clavicles, and strap-shaped scapulae, which are discovered eutherian Ambolestes (22). E dence of how the mammalian structures similar to those of other mammaliaforms (16). The newly identified hyoids in the early mam- have evolved (2–4). One early mammalia- The girdle and limb bones are very slender, and maliaform Microdocodon (fig. S4 and movie S2) form group is the docodontans, with a wide dis- the radius and ulna are elongate relative to the show the rodlike basihyal, thyrohyals, ceratohyals, tribution on Laurasian continents in the Jurassic humerus. It has an exceptionally long tail: the and epihyals, which are similar to those of and Cretaceous (5–13). We report here a newly postpelvic length of the caudal vertebrae is Yanoconodon, Sinobaatar, Maotherium,and discovered, exquisitely preserved docodontan skel- ~120% of the head–body length. On the basis of Eomaia (figs. S6 to S9), in an extant mammal-like eton that offers fresh insight on the transforma- these characteristics, we interpret this to mean configuration. Therefore, the hyoids of Microdocodon tion of hyoid bones and the earliest evolution of that it was a scansorial animal (figs. S1 and S10 represent the ancestral characters of hyoid appa- hyolingual function in mammals (14–18). to S12) (for details, see the supplementary ma- ratus for the clade of Microdocodon and crown Microdocodon gracilis,gen.etsp.nov.(16)is terials) (16). mammals. Phylogenetically, Microdocodon and on September 2, 2020 from the Middle Jurassic and was found in the The middle ear and hyoids are preserved with Vilevolodon are the earliest-known mammalia- Daohugou localities; it is preserved in part and the skull (Figs. 2 and 3, figs. S2 to S5, and movie form fossils with mammal-like hyoids (Fig. 3, fig. counterpart (holotype PMOL-AM00025A and B, S2). The middle ear is preserved in the postdentary S5, and movie S2). respectively: Fig. 1, fig. S1, and movie S1). The fully trough of the mandible, as in other mammalia- Although the hyoids are mammal like, the mid- erupted teeth (I?/i4?-C1/c1-P6/p6-M4/m4) indi- forms (Figs. 2 and 3 and figs. S1 to S4) (5–7, 11, 16). dle ear in docodontans is fully attached in the cate that it was an adult. Among docodontans, The basihyal, thyrohyal, ceratohyal, and epihyal postdentary trough of the mandible (Fig. 3B), Microdocodon is phylogenetically nested in the bones (distal part incomplete and possibly carti- which is also present in haramiyidans, albeit in Tegotheriidae (16), but differs from other tego- laginous) are preserved near the base of the skull a modified condition (Fig. 3C) (19). The hyoids theriids by several dental characteristics (fig. S2) (figs. S3 and S4). The basihyal is a rod-like bone are also mammal like in eutriconodontans and (9–12). Geologically, it is the oldest of the tego- with two slightly enlarged ends that bear articu- spalacotherioids, whereas the middle ears in these theriid taxa (16). lating facets for the paired thyrohyals and cera- animals are still connected by an ossified Meckel’s This animal has a diminutive size with a body tohyals. These facets are similar to the articular element to the mandible (Fig.3,fig.S6,andmovie mass ranging from 5 g (as estimated from limb facets of the basihyal–thyrohyal and basihyal– S2). The mammal-like, jointed anterior hyoid cornu bone lengths) to 9 g (as estimated from skull ceratohyal joints in the monotreme Tachyglossus and the saddle-like basal hyoid structure (Fig. 3) length) (tables S1 and S2) (16). It is much smaller (Fig. 3 and figs. S4 and S5). As in monotremes, the evolved before the separation of the middle ear than other docodontans from the paleoecological thyrohyals in Microdocodon have proximal ends fromthemandiblebyresorptionofMeckel’scar- wider than the shaft, whereas the distal ends are tilage, which occurred convergently in separate incomplete or unossified in the fossil. The right clades of crown Mammalia. The development thyrohyal (best seen on the main part) overlaps of a mobile linkage of the mammal-like hyoids is 1Paleontological Museum of Liaoning, Shenyang Normal University, Shenyang Liaoning, 110034, China. 2College of the well-preserved manubrium of the right mal- decoupled from transformation of the ear bones Earth Science and Engineering, Shandong University of leus (best seen on the counterpart). The ceratohyals in articulation with the mandible into the sepa- Science and Technology, Qingdao, Shandong 266590, China. are slender rods. The ceratohyal–epihyal joint was rated middle ear during mammaliaform evolu- 3 Department of Geology and Geophysics and Peabody mobile and forms a sharp angle. We interpret this tion (Fig. 3). Museum of Natural History, Yale University, New Haven, CT 06511, USA. 4Department of Organismal Biology and to mean that the basihyal, thyrohyals, and cera- Mammaliaform hyoids show neomorphic char- Anatomy, The University of Chicago, Chicago, IL 60637, USA. tohyals formed a “i—h” configuration, in which the acters not developed in nonmammaliaform the- 5Section Paleontology, Institute of Geosciences, Rheinische basihyal was the transverse strut (Figs. 2 and 3 and rapsids (Fig. 2). (i) The basihyal is ossified and Friedrich-Wilhelms-Universität Bonn, 53115 Bonn, Germany. movie S2). This configuration, herein called the forms a transverse strut in a saddle configuration *These authors contributed equally to this work. †Corresponding author. Email: [email protected] (T.M.); saddle-shaped configuration, is typical of the with the ceratohyals, and with the thyrohyals [email protected] (Z.-X.L.) basal parts (basihyal, ceratohyals, thyrohyals) of that connect the hyoids to the thyroid cartilage Zhou et al., Science 365, 276–279 (2019) 19 July 2019 1of4 RESEARCH | REPORT Downloaded from http://science.sciencemag.org/ on September 2, 2020 Fig. 1. Mammaliaform Microdocodon gracilis. (A) Skeletal reconstruction, (B) photo, and (C) illustration of holotype main part PMOL- AM00025A. PMOL-AM00025B is shown in fig. S1 and movie S1, mandible and dentition in fig. S2, and middle ear and hyoids in the details in figs. S3 and S4 and movie S2. (14, 16). By contrast, the basihyal and thyrohyals and unsegmented rods that lack the flexibility of in which to swallow the masticated food, as seen are not ossified (unknown as fossils) in non- the anterior hyoid cornu of mammals (24–26). in modern mammals (3, 14, 27). By contrast, in mammaliaform therapsids (2, 24–26)(fordetails, (iii) The jointed anterior hyoid cornu swings into nonmammaliaform therapsids, the long hyoid see the supplementary materials (16). (ii) The a posterior posture in mammaliaforms, enabled rods are situated anteriorly in an “A-shaped” con- basihyal, ceratohyal, and epihyal in the anterior by the angled joints of the basihyal–ceratohyal figuration,asseeninearlysynapsids(28)andin hyoid cornu (which hypothetically also includes and the ceratohyal–epihyal (Figs. 2 and 3 and extant nonmammalian amniotes (15, 27). the stylohyal) form a jointed linkage to the crista fig. S5). This posterior posture is necessary for In extant mammals, under the control of the parotica of the petrosal of mammaliaforms (Fig. the basihyal–thyrohyal to cradle the thyroid car- suprahyoid and infrahyoid musculature, the mo- 3andfig.S5)(16, 23). However, in nonmamma- tilage and the larynx for a narrow and muscu- bile linkage of the jointed anterior hyoid cornu liaform therapsids, the hyoids are a pair of long larizedpharynx,creatinganoropharyngealspace plays a crucial role in cyclic movement of the Zhou et al., Science 365, 276–279 (2019) 19 July 2019 2of4 RESEARCH | REPORT Downloaded from http://science.sciencemag.org/ on September 2, 2020 Fig.
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