A New Basal Hadrosaurid (Dinosauria: Ornithischia) From the Latest Cretaceous Kita-ama Formation in Japan: the Rise of Hadrosaurs


 Here we describe a partial hadrosaurid skeleton from the marine Maastrichtian Kita-ama Formation of the Izumi Group in Japan as a new taxon, Yamatosaurus izanagii gen. et sp. nov. Our phylogenetic analysis demonstrates it belongs to the Hadrosauridae, composed of Hadrosaurus foulkii + (Yamatosaurus izanagii + (Saurolophinae + Lambeosaurinae). Yamatosaurus izanagii is unique in having only one functional tooth/row in the middle of the dentary dental battery and complete absence of the branched ridges on the occlusal surfaces. The coracoid lacks a biceps tubercle as in non-hadrosaurid hadrosauroids, suggesting its presence is a key feature for the clade of Saurolophinae and Lambeosaurinae. The evolutionary rate analysis further supports that shoulder and forelimb features, which are likely to be involved in locomotion, are important for the early evolution of Hadrosauridae. Our biogeographic analyses show that the basal Hadrosauridae was widely distributed in Asia and Appalachia, and the clade of Saurolophinae and Lambeosaurinae originated in Asia. The contemporaneous occurrence of basal (Yamatosaurus izanagii) and derived (Kamuysaurus japonicus) hadrosaurids during the Maastrichtian in Japan is the first record in Asia. Because of a long geographical distance between these localities, they may not co-exist but show some level of provinciality.


Introduction
Hadrosauroids are successful herbivorous ornithischian dinosaurs during the Cretaceous. Fossil records of basal hadrosauroids have been discovered mainly from the Lower Cretaceous deposits of Europe, eastern Asia, and Africa, whereas derived forms are commonly known from the Upper Cretaceous rocks of all continents except Australia and the Indian subcontinent. A large clade of derived hadrosauroids, ourished in post-Campanian, called differently in previous studies such as Euhadrosauria 1-3 , Hadrosauridae 4,5 , and Saurolophidae 6 , consists of two major clades with solid-crested (Hadrosaurinae 7 or Saurolophinae 6 ) and hollow-crested (Lambeosaurinae) skulls 2,6 . Hadrosauridae is de ned as the most recent common ancestor of Edmontosaurus regalis, Saurolophus osborni, Lambeosaurus lambei, and Hadrosaurus foulkii and all of its descendants 6 . The members of hadrosaurids were successful in both abundance 8,9 and cosmopolitan distribution including the Arctic [10][11][12] . The high diversi cation of hadrosaurids is attributed to their e cient oral processing system, established by specialized dentitions with complex grinding surface 13 together with cranial kinetics 14,15 . Social behaviors, expressed by unique supracranial crests, are also likely to have contributed to the success of the derived hadrosauroids [16][17][18] . In addition to the functional adaptations, Kobayashi, et al. 19 recently proposed that inhabitation in marine-in uenced environments by ancestral hadrosaurids also played an important role in the early evolution of hadrosaurids. However, because the members of sister clades of Hadrosauridae vary among previous studies (e.g., Telmatosaurus transsylvanicus, Plesiohadros djadokhtaensis, Eotrachodon orientalis, and Lophorhothon atopus), the rise of hadrosaurids has been obscure.

Geological setting
The new specimen was recovered from blocks of dark grey mudstones of the upper part of the Kita-ama Formation of the Izumi Group, exposed at a cement industry quarry (Loc. Aw14, Morozumi 22 ) in Yura Town, Sumoto City of the Awaji Island in Hyogo Prefecture. The upper part of the Kita-ama Formation, composed of inter-arc basin deposits including conglomerate, sandstone, and mudstone of the distal turbidite faces (Fig. 1C-E), is rich in invertebrate fossils; the ammonoid Nostoceras hetonaiense, the nautilid Eutrephoceras sp., bivalves (e.g., Apiotrigonia (Microtrigonia) amanoi, Eriphyla japonica, and Inoceramus (Endocostea) shikotanensis), and gastropods (e.g., Gigantocapulus problematicus), decapods (e.g., Archaeopus ezoensis, Hinecaris simplex, and Ahazianassa masanorii) [22][23][24] . Fragmentary materials of vertebrates also have been reported from this quarry such as shes, a turtle (Mesodermochelys undulatus), a mosasaur, and a hesperornithiform 23,25−27 (Tanaka,et al. 27 erroneously listed pterosaur and plesiosaur occurrences from the locality). Plant fossils from the quarry include angiosperms (Platanus sp. and Ulmus sp.) and cycad (Zamiophyllum sp.) 23 . The exposed beds at the quarry are within subchron 32.1r 28  Nomenclatural Acts. This published work and the nomenclatural acts it contains have been registered in ZooBank, the proposed online registration system for the International Code of Zoological Nomenclature.
Etymology. "Yamato" refers to the ancient name for a region of the Japanese archipelago, including the western half of the main island (Honshu Island), Shikoku Island, and the northern half of Kyushu Island, ruled by the Yamato Kingdom from the third to the seventh century. "Sauros" means reptiles. The speci c name, "izanagi", refers to a deity in Japanese mythology, which created eight countries of Yamato with another deity, Izanami, based on the oldest history book in Japan, called "Kojiki (Records of Ancient Matters)", published in 712 CE (Common Era). The rst country created was the Awaji Island, followed by the Shikoku, Oki, Kyushu, Iki, Tsushima, Sado, and Honshu islands.
Diagnosis. The hadrosaurid with unique characters in having the presence of only one functional tooth/row in the middle of the dentary dental battery and the complete absence of the "branched ridges" on the dentary tooth occlusal surfaces. It is also unique in the combination of the following characters: the small angle between the medial surface of dentary symphysis and lateral surface of the dentary and ventrally facing ventral surface of the surangular.
Description. The right dentary is nearly complete, missing its posterior end and the coronoid process. The lateral surface of the main body of the dentary bears multiple neurovascular foramina. A large foramen is positioned at the level of the seventh dentary tooth, and several smaller foramina are present posteriorly.
In lateral view, the anterior portion of the dentary is downturned, and an angle between the ventral edge of the anterior portion and a horizontal plane, or tooth row, is 20 degrees (Fig. 2A). In medial view (Fig. 2B), the long axis of the tooth row is parallel to the ventral margin of the middle region of the dentary main body as in hadrosaurids except for Brachylophosaurini 36 . A thin alveolar parapet, covering the medial surface of the dental battery, is dorsoventrally taller posteriorly than anteriorly. The nutrient foramina are organized in a shallow arch ventral to the dental battery. The Meckelian groove extends along the ventral margin of the posterior two-thirds of the dentary. The ventral edge of the dentary main body below the coronoid process is weakly bowed. In dorsal view, the occlusal surface of the dental battery is straight and parallel to the lateral surface of the dentary main body (Fig. 2C).
The dentary diastema is approximately 99 mm. The length is 30% of the length between the anterior end of the dental battery and the posterior margin of the coronoid process (330 mm). Although the coronoid process is not preserved, the latter length was estimated from the base of the coronoid process. The dorsal margin of the dentary, where the lateral ramus of the predentary contacts, is strongly concave in lateral view and is angled by 110 degrees from a horizontal plane (Fig. 2B).
The symphysial process of the dentary curves medially at nearly a right angle (Fig. 2E) as in nonhadrosaurid hadrosauroids (e.g., Plesiohadros djadokhtaensis; MPC-D 100/745) and some members of Lambeosaurini, including Olorotitan arharensis 37 and Parasaurolophus tubicen (NMMNH P-25100). The maximum mediolateral width of the dentary symphysial region in dorsal view is 81 mm, which is approximately twice as wide as the minimum breadth of the dentary posterior to the dentary symphysial region (Fig. 2C). The medial margin of the symphysial process is largely divergent from the lateral surface of the main body of the dentary by an angle of 20 degrees as in Eotrachodon orientalis 38 but unlike a nearly parallel alignment in hadrosaurids such as Edmontosaurus regalis 39 and Parasaurolophus tubicen (NMMNH P-25100). The medial surface of the symphysial process bears a shallow groove for contact with its counterpart (Fig. 2B). The ventral surface of the symphysial process has a large neurovascular foramen (Fig. 2D).
The base of the coronoid process is laterally expanded as in hadrosaurids and some non-hadrosaurid hadrosauroids such as Plesiohadros djadokhtaensis, Nanningosaurus dashiensis, and Adynomosaurus arcanus [40][41][42] and is separated from the dental battery (Fig. 2E). The posteromedial surface of the coronoid process is largely excavated, forming the mandibular adductor fossa.
The dorsolateral portion of the right surangular is preserved (Fig. 3). The preserved region of the anterodorsal process is thin and bears a well-de ned ridge for the attachment of m. adductor mandibulae externus super cialis 43 . The ridge is posteriorly continuous with the dorsolateral ange, which is gently arcuate in dorsal view. The lateroventral surface of the surangular bears no foramen as in derived hadrosauroids including Bactrosaurus johnsoni 44,45 . The dorsal surface of the anterior half of the surangular is concave to form the mandibular adductor fossa, whereas the posterior half forms a glenoid fossa that receives the mandibular condyles of the quadrate. The ventromedial portion of the surangular is lost before collection thus the morphology of the caudal process and the retroarticular process is unavailable.
At least 34 tooth positions are present, and each tooth position bears a maximum of four teeth in the right dentary, and at least twelve isolated dentary teeth from the left side are preserved. Tooth crowns are diamond-shaped and bear a prominent straight primary ridge in the middle teeth, while the primary ridge is sinuous in mesial and distal teeth (Figs. 2B, 4A, 4H). The secondary ridges are faint, wrinkled, and in some cases branched as in Eotrachodon orientalis 38 and Hypacrosaurus altispinus 46 but unlike the straight secondary ridges of Corythosaurus casuarius (ROM 868) and Lambeosaurus lambei (CMN 361, CMN 2869). The largest tooth crown, located in the middle portion of the dental battery, is approximately 41.94 mm high and 14.66 mm wide. The tooth crowns become shorter and narrower mesially and distally (Fig. 2B). The height/width ratios of the dentary tooth crowns are slightly less than three on average although vary largely by position. The marginal denticles along the mesial/distal edges of the coronal half of the tooth crown are proportionately smaller than those of Eotrachodon orientalis 38 and Lambeosaurus lambei (CMN 351) and resemble those of Hypacrosaurus altispinus in size 46 . The marginal denticles of Yamatosaurus izanagii are formed of multiple small papillae ( Fig. 4B-C), which are unorganized unlike in Eotrachodon orientalis 38 and Corythosaurus casuarius (AMNH FARB 8527), but resembling Gryposaurus notabilis (AMNH FARB 8526). The angle between the crown and root of the dentary teeth is 132 degrees (Fig. 4B).
An occlusal surface of an isolated tooth changes from a at pentagonal surface ( Fig. 4D-E) to a concaved oval-shaped surface (Fig. 4F-G) as it wears. At most two teeth are functional per tooth position throughout the dental battery unlike hadrosaurids (e.g., Edmontosaurus regalis, CMN 2289; Parasaurolophus tubicen, NMMNH P-25100), which have more than two functional teeth in the middle of the dental battery. Only one functional tooth in 9th, 11th, 14th, 16th, 19th, 21st, and 23rd tooth positions ( Fig. 4I-J), which is unique to Yamatosaurus izanagii. The occlusal surface of the dental buttery is steeply inclined as in Prosaurolophus maximus (CMN 2277, CMN 2280), the distal area of the dental battery of Brachylophosaurus canadensis (CMN 8893), and the mesial area of the dental battery of Gryposaurus (Gryposaurus notabilis, ROM 873; Gryposaurus latidens, AMNH FARB 5465). The occlusal surface of Yamatosaurus izanagii bears low ridges that are associated with cementum and longitudinal giant tubules that ll the pulp cavity 13,47 . The occlusal topography is much lower than in Corythosaurus 13 but resembles that of Brachylophosaurus canadensis (CMN 8893). The strong inclination and the low topography of the occlusal surfaces may suggest the pulp cavity of teeth of Yamatosaurus izanagii is lled mainly with transverse giant tubules, which are less wear-resistant than longitudinal giant tubules 13 .
At least four cervical vertebrae are preserved, and three of them are fairly complete (Fig. 5A-O). Although the exact position of these vertebrae is ambiguous, two are identi ed as anterior (fourth or fth and fth or sixth) and one as a middle (seventh to ninth) cervical vertebra based on comparisons with Gobihadros mongoliensis (MPC-D 100/746). The anterior cervical vertebrae are nearly complete other than postzygapophyses, whereas the middle cervical vertebra is missing the ventral half of its centrum. The anterior centra are strongly opisthocoelous. The anterior convexity and the posterior concavity are the most pronounced in the anteriormost cervical vertebra. The lateroventral surface of the centrum is deeply excavated and bears several foramina. The ventral surfaces of the centra are slightly convex and do not form a distinct keel. The neural canal is slightly wider than its height in the anteriormost cervical vertebra and becomes wider posteriorly. The transverse process is the shortest in the anteriormost cervical vertebra and becomes longer posteriorly. The dorsal surfaces of the prezygapophyses are slightly inclined mediodorsally. The diapophyses become longer posteriorly relative to the articular facets of the prezygapophyses. The neural spine is faint and lacks signi cant dorsal projection in the anteriormost cervical vertebrae and becomes larger posteriorly. Both sides of the base of the neural spine are shallowly depressed in the anteriormost cervical vertebra. The depressions are shallower and smaller in posterior cervicals. The postzygapophyses are less than three times as long as the anteroposterior length of the neural arch unlike hadrosaurids, including Maiasaura peeblesorum (ROM 44770) and Hypacrosaurus stebingeri (MOR 549) but resemble non-hadrosaurid hadrosauroids such as Gilmoreosaurus mongoliensis (AMNH FARB 6551). The postzygapophyseal articular surface is anteroposteriorly longer than mediolaterally wide in the anterior cervical vertebrae, whereas the articulation surface is subcircular in the middle cervical vertebra.
A distal caudal vertebra is nearly complete, missing a right prezygapophysis and a distal portion of the neural spine (Fig. 5V-Z). The centrum is amphiplatyan and is hexagonal in anterior and posterior aspects. The lateral surfaces of the centrum bear a ridge in the middle, whereas the ventral surface is gently convex. The transverse process is absent as in the 38th and more posterior caudal vertebrae of a lambeosaurine indet. (CMN 8330). The neural canal is a mediolaterally wide ellipsoid. The rod-shaped prezygapophysis lacks a distinct articular facet. The postzygapophysis is reduced and indistinguishable from the neural spine.
One right and two left cervical ribs are preserved (Fig. 5P-U). The capitulum is longer and more massive than the tuberculum in all preserved cervical ribs. The lateral crest is dorsoventrally at and welldeveloped in the anterior-most preserved cervical rib and gradually diminishes posteriorly.
The right coracoid is complete (Fig. 6). The articular facet for the scapula is shorter than the glenoid and angled 114 degrees from the glenoid in the external view. The coracoid foramen is ellipsoid and does not intersect the scapulocoracoid contact. The anterior margin of the coracoid is straight. The biceps tubercle is absent. The ventral process is only half as long as its base as in non-hadrosaurid hadrosauroids (e.g., Gilmoreosaurus mongoliensis, AMNH FARB 30722), yet the ventral process is recurved caudoventrally as in hadrosaurids (e.g., Brachylophosaurus canadensis, MOR 1071 8-10-99-541; Hypacrosaurus altispinus, AMNH FARB 5272).

Discussion
The ontogenetic stage of Yamatosaurus izanagii cannot be examined histologically due to the absence of any weight-bearing limb bones. However, the size of the preserved dentary (Supplementary Table S1) is comparable with those of large, presumably adult hadrosaurids including Kamuysaurus japonicus (526 mm) 19 and Hypacrosaurus stebingeri (500 mm) 48 . In addition, the neurocentral sutures of preserved cervical vertebrae are closed (Fig. 5), suggesting the type specimen of Yamatosaurus izanagii was at least close to maturity at the time of its death 49,50 .
Our phylogenetic analysis produced 12 most parsimonious trees (MPTs) of 1181 steps, each with a consistency index of 0.430 and a retention index of 0.834. Hadrosaurus foulkii, which has been regarded as a nomen dubium 7,51 , is recovered as a sister taxon to the clade of Yamatosaurus izanagii, Saurolophinae, and Lambeosaurinae. Since the phylogenetic position of Hadrosaurus foulkii is comparable to those proposed by Prieto-Márquez 6 , this study follows Prieto-Márquez 6 in the de nitions of Hadrosauridae, Lambeosaurinae, and Saurolophinae.
The analysis shows that Yamatosaurus izanagii belongs to Hadrosauridae, sharing two of ve synapomorphies of the family (small denticles of dentary teeth and long ventral process of the coracoid), and is a sister taxon to the clade of Saurolophinae and Lambeosaurinae (Fig. 7). The clade of Yamatosaurus izanagii, Saurolophinae, and Lambeosaurinae is weakly supported, sharing a single synapomorphy (dentary tooth crown height-width ratio in between 2.70 and 3.30). Yamatosaurus izanagii is a sister taxon to the clade of Saurolophinae and Lambeosaurinae, which is well supported by ve unambiguous characters: functional teeth up to two; symphysial region of dentary strongly curved lingually; short postzygapophysis of cervical vertebrae; straight craniodorsal margin of coracoid; and absence of biceps tubercle of the coracoid.
Three phylogenetic autapomorphies of Yamatosaurus izanagii are the crown and the root of the dentary teeth angled in between 110º and 130º, a small angle between the medial surface of dentary symphysis and lateral surface of the dentary, and ventrally facing ventral surface of the surangular. The moderately angled dentary teeth crown and root is shared with derived lambeosaurines (Parasaurolophini + Lambeosaurini) and saurolophines other than Saurolophini and Kritosaurini. The small angle between the medial surface of dentary symphysis and lateral surface of dentary is commonly seen in more primitive forms such as Eotrachodon orientalis, Gilmoreosaurus mongoliensis, Bactrosaurus johnsoni, and more primitive taxa, indicative of a reversal in Yamatosaurus izanagii. The ventrally facing surface of the surangular main body is a character for derived saurolophines (e.g., Edmontosaurus and Saurolophus) and lambeosaurines (e.g., Corythosaurus and Hypacrosaurus).
In addition to the phylogenetic autapomorphies, Yamatosaurus izanagii is unique among Eolambia caroljonesa and higher taxa in the presence of only one functional tooth/row, even in the middle of the dentary dental battery (Fig. 4I-J). The dentary occlusal surface is also unique in the complete absence of the "branched ridges" 13 in any of the preserved teeth. Since the ridges are formed at the plugged pulp cavity 47,52 , the absence of the "branched ridges" may indicate a unique tooth ontogeny of Yamatosaurus izanagii. Other than the dentition, Yamatosaurus izanagii dentary exhibits derived forms. It differs from the other derived non-hadrosaurid hadrosauroids, including Eotrachodon orientalis 38 , Zhanghenglong yangchengensis 7 , and Plesiohadros djadokhtaensis 40 , in having the ventral de ection of the anterior dentary, the posterior elongation of the dental battery, and the anteromedial elongation of the symphysial process.
While the dentary possesses multiple derived features, the coracoid of Yamatosaurus izanagii resembles those of non-hadrosaurid hadrosauroids such as Eolambia caroljonesa and Gilmoreosaurus mongoliensis in its straight anterior margin, short ventral hook, and undeveloped biceps tubercle. Dilkes 53 interpreted the biceps tubercle of hadrosaurids as the origin of m. biceps, which extends to the proximal ends of the ulna and radius. Since m. biceps functions to lift the antebrachium, the presence and enlargement of the biceps tubercles in saurolophines and lambeosaurines may represent a functional change in forelimb use. The evolutionary rate analyses on pectoral girdle + forelimb phylogenetic characters demonstrate a signi cantly high evolutionary rate in the branch leading to the clade of Saurolophinae and Lambeosaurinae (Fig. 7B). Although one may concern the high evolutionary rate may be an artifact by the incompleteness of Yamatosaurus izanagii as warned by Lloyd 54 , the same trend is recovered in an analysis without Yamatosaurus izanagii ( Supplementary Fig. S1). Therefore, the pectoral girdle + forelimb morphology is likely to have experienced rapid morphological changes at the base of Hadrosauridae. The rapid pectoral girdle + forelimb modi cations may be associated with hadrosauroid gait change. Although Maidment and Barrett 55 suggested that facultative quadrupedality was acquired more basal to Gilmoreosaurus mongoliensis, the evolutionary rates of the pectoral girdle + forelimb may suggest the gait shift was accomplished in basal hadrosaurids. Previously, changes in jaw elements and dentition have been considered as the key features for the origin of Hadrosauridae, but this study adds that forelimb locomotion, resulting from shoulder and forelimb structural modi cation, is also an important feature within the origin of this family.
The biogeographic analyses resulted in higher ts in the analyses using the "starting" and the "relaxed" dispersal multiplier matrices than in the "harsh" (Supplementary Table S2). The results suggest that permitting intercontinental dispersal probabilities can explain hadrosaurid dispersal history better than considering intercontinental dispersal was nearly impossible. The results in the "starting" and the "relaxed" matrices are nearly identical to each other thus only the "starting" result is presented here (Fig. 8; see Supplementary Figs. S2 and S3 for the "relaxed" and "harsh" results). The analysis suggested that successive nodes of derived hadrosauroids from Eotrachodon orientalis to the node of Hadrosauridae were widely distributed in Asia and Appalachia, but not the intervening landmasses of Laramidia or Europe. Previous studies argued that the largely diversi ed clade of Saurolophinae and Lambeosaurinae (Hadrosauridae sensu Xing, et al. 7 ) originated in North America 11,56 or Asia 5 , but our analysis supports the Asian origin of this clade thus re ning other previous broader models of ornithopod origins in Asia 57 while also contributing to a better understanding of the origins of high latitude dinosaurs 58 . Further biogeographic resolution will be aided with additional specimens, especially from pre-Campanian Upper Cretaceous deposits, because the successive taxa of non-hadrosaurid hadrosauroids, especially from Eotrachodon orientalis to Plesiohadros djadokhtaensis, have long ghost lineages up to 20 my.
Yamatosaurus izanagii shows the longest ghost lineage duration of roughly 30 my among hadrosaurids. Interestingly, given the length of the ghost lineages of the Maastrichtian non-hadrosaurid hadrosauroids Plesiohadros djadokhtaensis from Mongolia and Tanius sinensis from China, considered with the ghost lineage represented by Yamatosaurus izanagii, it may be that eastern Asia (Japan, Mongolia and China) served as a refugium of relict hadrosauroid taxa.
Hadrosauroid materials have been reported from the Upper Cretaceous deposits of Japan 20 , and the youngest occurrence is Kamuysaurus japonicus from the early Maastrichtian marine deposits of the Hakobuchi Formation in Mukawa Town in Hokkaido Prefecture 19 , which is equivalent age to Yamatosaurus izanagii. Although paleo-latitudes of Mukawa Town and Sumoto City during the Cretaceous are estimated to be similar to the current position (approximately 1,100 km apart), it is clear that these dinosaurs were present at the same geologic time. It was suggested that the non-hadrosaurid hadrosauroid Plesiohadros djadokhtaensis in late Campanian was replaced by hadrosaurids such as Saurolophus angustirostris and Barsboldia sicinskii in Maastrichtian in Mongolia, indicating that the coexistence of hadrosaurid and non-hadrosaurid hadrosauroid is unlikely in the uvial depositional environments 40 . The replacement of hadrosauroids by more derived members during the Maastrichtian is suggested in Laurasia 40 but not in Europe (Telmatosaurus transsylvanicus and Tethyshadros insularis) because the European archipelago persisted as island relicts 3,59,60 . The occurrence of Yamatosaurus izanagii and Kamuysaurus japonicus from the time equivalent formations shows the contemporaneous existence of a derived and a basal hadrosaurid in Asia for the rst time (Fig. 1G). This contemporaneous occurrence may be due to a different paleoenvironment preserved where Japan was more coastal in nature and richer in vegetation with plants such as plane trees (Platanus sp.), elm (Ulmus sp.), and cycads (Zamiophyllum sp.) than the uvial environments preserved in the mainland Asian continent. An alternative scenario is that these dinosaurs did not co-occur and instead there was some level of provinciality within the coastal environments of this part of Asia where Kamuysaurus japonicus occupied a northern area and Yamatosaurus izanagii was restricted to a more southern area.

Materials And Methods
Phylogeny. Phylogenetic analysis was conducted on the data matrix modi ed from Takasaki, et al. 61 , using TNT ver 1.5 62 . The immature Edmontosaurus OTUs were removed from the original data matrix since their phylogenetic relationships are out of the scope of this study. Nanyangosaurus zhugeii was also excluded from the analysis because of its poor preservation. Protohadros byrdi is included in the data matrix by scoring the phylogenetic characters based on the published literature 63 . Lophorhothon atopus was re-scored based on the recently published paper by Gates and Lamb 64 . The resultant data matrix consists of 71 OTUs and 354 characters (Supplementary Data S1). A phylogenetic analysis was conducted using TNT ver. 1.5 62 , with the Ouranosaurus nigeriensis set as the outgroup. All of the characters were equally weighted and unordered. The maximum number of trees was set to 99,999 in memory. A traditional search with 10,000 replicates of Wagner trees using random additional sequences, followed by the TBR branch swapping that held 10 trees per replicate was performed. Supports for the clade were evaluated by bootstrap resampling using standard absolute frequencies (1,000 replicates) and Bremer decay indices calculations.
Evolutionary rates. Branch evolutionary rates of the phylogenetic characters related to pectoral girdle + forelimb were examined using R package Claddis version 0.6.5 54 in R v.4.0.3 65 , based on the current morphological data matrix and the phylogenetic hypothesis. OTUs with character completeness less than 50% are pruned prior to the analyses since missing data leads to extreme results 54 . Removal of the taxa with low character completeness also provides much better resolution to the phylogenetic tree. The remaining polytomies are randomly resolved prior to the branch partition analyses then given branch lengths of 10 − 6 of the total tree lengths. One-hundred time-calibrated phylogenetic trees which incorporate the ranges of the time of rst and last appearances are constructed based on the equal method 66 using the R package paleotree 67 . The analysis was repeated twice, with and without Yamatosaurus izanagii. The trees were calibrated based on the rst and the last appearances of each OTUs (Supplementary Data S2). The analysis was repeated twice, with and without Yamatosaurus izanagii. The analyses are conducted using the R script provided as the Supplementary Data S3.
Ancestral range reconstruction. Ancestral habitat ranges were reconstructed using R package BioGeoBEARS 68 in R v.4.0.3 65 using the R script in the Supplementary Data S4. Although recent biogeographic works generally conduct analyses over multiple models 56,69 , Ree and Sanmartín 70 recently pointed out conceptual problems in "+J" models. Since our interest is on habitat range reconstruction rather than model selection, this study conservatively performed only the DEC analysis following the suggestions by Ree and Sanmartín 70 . A phylogenetic hypothesis based on the majority consensus tree was used. The remaining polytomies were resolved then given branch lengths of 10 − 6 of the total tree lengths. To incorporate the ambiguities in time ranges of the OTUs, 100 time-calibrated phylogenetic trees were produced using the R package paleotree 67 , based on the "equal" method 66 . The marginal probabilities at each node are averaged over the 100 time-calibrated trees. Three analyses with the "starting", "harsh", and "relaxed" dispersal multiplier matrices were conducted following Poropat, et al. 71 . In the "starting" and the "relaxed" matrices, the dispersal multiplier values between the following continents are set to 0.5 and 1, respectively: Asia and Laurasia, Asia and Europe, Laramidia and Appalachia, Laramidia and South America, Appalachia and Europe, and Europe and Africa