Ruminants reveal Eocene Asiatic palaeobiogeographical provinces as the origin of diachronous mammalian Oligocene dispersals into Europe

Faunal provincialism between the North and South parts of Eastern Asia is shown to have been in place since the late Eocene. This provincialism structured the mammalian dispersals across Eurasia for millions of years and provides insights into both palaeonvironments and palaeoclimate zonation. In addition, this study reveals the oldest record of a crown ruminant (Iberomeryx from Shinao, China). Ecologically, as well as economically, ruminant artiodactyls are one of the most important large mammal groups today. The revision of the ruminants from the Shinao Formation, from the Caijiachong marls and Xiaerhete, resulted in two new taxa and shows that the different provinces were populated by distinct taxa living in different environments, dominated by the monsoon in the South and drier conditions in the North. Evaluating this result in a Eurasian context demonstrates that the dispersals from Asia to Europe was complex. These results confirm that there were at least two dispersal events, distinct in space and time: the Grande-Coupure from Northern and Central Asia along the North ca. 34 Mya and the Bachitherium dispersal event from the Southern province along a southerly route ca. 31 Mya.

Etymology. Krabi-from Krabi Basin, where the fossils were found, and-meryx is the Greek word for ruminant. 17 ]. Small primitive ruminant with lower molars morphologically close to those of Zhailimeryx. Krabimeryx differs from Zhailimeryx in: more laterally compressed lingual cuspids in the lower molars; an entoconid displaced to anterior with respect to the hypoconid; the lack of both a paraconid and a hypoconulid in m1 and m2; a p4 with a mesolingual conid that is located more posterior and less individualized; a p4 without a distinct posterolingual conid. Krabimeryx differs from Lophiomeryx by less selenodont labial cuspids in the lower molars, the presence of a developed external postmetacristid, and by a distinct groove on the anterior side of the entoconid, the entoconidian groove. Krabimeryx can be distinguished from Iberomeryx in having a well-marked entoconidian groove; the lack of a clear external postprotocristid; the third lobe of m3 not forming a complete buckle; and a more transversely compressed hypoconulid in the m3. Krabimeryx possesses a huge notch in lingual view between the entoconid and the third lobe in the m3. Included species. Krabimeryx gracilis nov. comb. (Miao, 1982 20 ).
Based on the presence of a strong lingual cingulum in upper molars and a short anteroposteriorly oriented postprotocrista, as well as the absence of a premetacristid and an anterior fossa widely open in the lower molars, we can conclude that the specimens, IVPP V 6546-1, IVPP V 6546-2, IVPP V 6549, and IVPP V 6550, belong to Lophiomerycidae or Tragulidae 35,36 . However, the absence of a large paraconid and the absence of an elongated external postmetacristid distinguish the specimens from primitive Tragulidae 17,36 . In Zhailimeryx jingweni, the cuspids are more slender than in the herein described specimens 14 , a feature the taxon shares with K. primitivus. In Z. jingweni, m1 and m2 are of relative similar width 14 , while in K. primitivus and the herein described specimens from Shinao the m2 is clearly bigger than the m1 17 . Similarly to K. primitivus, the herein described specimens differ from Z. jingweni in its lower molar lingual cusps being more laterally compressed, and in an entoconid that is slightly shifted to anterior with respect to the hypoconid, while it is more posterior in Z. jingweni 14,17 . Furthermore, K. primitivus and the herein described specimens from Shinao both lack the rudimentary paraconid present in Z. jingweni 14,17 .
Like K. primitivus, the here-described specimens differ from Chiyoumeryx nov. gen. (described below) and the Lophiomeryx species L. mouchelini, L. chalaniati and L. angarae by having more massive and more bunomorph lower molars 16,17,24,34,37 . Furthermore, Zhailimeryx jingweni, K. primitivus, and the herein described specimens differ from Lophiomeryx by the presence of a developed external postmetacristid and by a distinct entoconidian groove on the anterior side of the compressed entoconid 14,17 . In Lophiomeryx, the back fossa of m3 is widely open due to the strong reduction of the posthypoconulidcristid 34,37 . In contrast to this, Krabimeryx primitivus possesses a clearly developed posthypoconulidcristid forming a buckle on the m3 back basin 17 , similarly to the specimens from Shinao described here.
Summing up, the general morphology of the teeth in the herein described specimens is most similar to the one observed in K. primitivus. They both share a similar huge notch in lateral view between the third lobe of m3 and the entoconid and the entoconidian groove, features that clearly distinguishing them both from Lophiomeryx and Zhailimeryx. Thus, we attribute the specimens IVPP V 6546-1, IVPP V 6546-2, IVPP V 6549, and IVPP V 6550 to the genus Krabimeryx. However, significant differences occur with the type species, ruling out the synonymisation of K. gracilis nov. comb. and Krabimeryx primitivus. While both species are very similar in size, K. primitivus has an m3 wider than m2, while it is the converse for K. gracilis nov. comb. Moreover, the entoconid is less shifted to the anterior with respect to the hypoconid in K. gracilis nov. comb. than in K primitivus. There is no ectostylid in K. primitivus, while it is large in K. gracilis nov. comb., forming a transverse cristid between the protoconid and the hypoconid. The cingulum on the upper molars is more developed in K. gracilis nov. comb. than in K. primitivus.
Due to these differences we decided to create the new combination Krabimeryx gracilis nov. comb. Diagnosis. Chiyoumeryx nov. gen. differs from Zhailimeryx and Krabimeryx notably by the absence of the entoconidian groove. The lower teeth are more laterally compressed in Chiyoumeryx nov. gen. and the metaconid is linguo-labiallly more central than in the two other genera. The posthypoconulidcristid in the lower molars of Chiyoumeryx nov. gen. is longer than in Krabimeryx and its p4 is posteriorly extended, while this part is reduced in Krabimeryx. Chiyoumeryx nov. gen. differs from Lophiomeryx by the shape of the mandible. In Chiyoumeryx nov. gen. there is no diastema between p1 and p2 and the diastema between c and p1 is extremely reduced. The outline of the mandible in occlusal view is relatively straight in this species. Lophiomeryx possesses a long diastema between c and p1 and a small one between p1 and p2, as well as a regularly curved occlusal outline of the corpus. The lower premolars of Chiyoumeryx nov. gen. are laterally compressed giving a more elongated aspect to these teeth than in Lophiomeryx. The trigonid is smaller than the talonid in m1 and m2 Scientific Reports | (2021) 11:17710 | https://doi.org/10.1038/s41598-021-96221-x www.nature.com/scientificreports/ in Chiyoumeryx nov. gen. and the preprotocristid terminates centrally and does not reach the lingual side. In Lophiomeryx the trigonid and talonid are of similar size and the preprotocristid is longer and reaches the lingual side. Moreover, in Chiyoumeryx nov. gen., the posthypoconulidcristid is longer than in Lophiomeryx. The shape of the P4 in Chiyoumeryx nov. gen. differs from the one in Lophiomeryx: the posterolingual crista does not meet the posterolabial crista.
Type species. Chiyoumeryx nov. gen. shinaoensis (Miao, 1982 20 (Miao, 1982 20 ). Figure 1B and Figure S2. *v1982 Lophiomeryx shinaoensis-Miao: 530, Taxonomical attribution. Miao 20 attributed the here described specimens to the genus Lophiomeryx assuming that these fossils belong to a traguloid. "Lophiomeryx" shinaoensis clearly is a Lophiomerycidae: anterior and posterior fossae are open on the lower molars due to the absence of a premetacristid and the extreme reduction or absence of a postentocristid, there is no external postprotocristid, there is a mesolingual conid on the p4, the symphysis of the mandible extends backward up to the p1 2,36 . It also shares with undisputable Lophiomerycidae a reduced posthypoconulidcristid that does not enclose the third lobe lingually. "Lophiomeryx" shinaoensis differs from Zhailimeryx and Krabimeryx in the absence of the entoconidian groove 14,17 . Moreover, the teeth are more laterally compressed in "Lophiomeryx" shinaoensis and the metaconid is linguo-labially more centeral 14,17 . The posthypoconulidcristid in "Lophiomeryx" shinaoensis is more elongated than in Krabimeryx and its p4 has an extended posterior part, while it is reduced in Krabimeryx 17 .
Contrary to what was suggested by Métais and Vislobokova 2 , Miomeryx altaicus 24 is currently known only by its holotype, which is an upper tooth row (AMNH 20383, see Matthew and Granger 24 ). Comparable to M. altaicus, the postprotocrista reaches the premetaconulecrista on the M2 in "Lophiomeryx" shinaoensis. These two cristae fuse totally on the M3 in the here described specimens. However, even if both genera also bear a very strong cingulum, "Lophiomeryx" shinaoensis clearly differs from M. altaicus in having broader and squarer molars and straighter lingual cristae in the P4.
Miao 20 compared the here revised fossils with the seven Lophiomeryx species considered valid at that time. Unfortunately, very few specimens document most of these species and there is considerable doubt considering the genus attribution of most of them 34,[36][37][38][39] . In any case, we agree with Miao 20  www.nature.com/scientificreports/ combined with a longer preprotocristid in the European Lophiomeryx species and L. angarae 16,34,37 . The shape of the P4 in "Lophiomeryx" shinaoensis is very different from Lophiomeryx (see Brunet and Sudre 37 ,Figs. 4 and 6).
In Lophiomeryx, the posterolingual crista fuses with the posterolabial crista. In "Lophiomeryx" shinaoensis, the curved posterolingual crista does not join the distal end of the posterolabial crista but reaches the labial side. Furthermore, "Lophiomeryx" shinaoensis clearly differs from L. angarae L. mouchelini, and L. chalaniati in the shape of the mandible. These three species of Lophiomeryx possess a very elongated diastema between c and p1 and a small one between p1 and p2 24,36,37  […] On the anterior part of the mandible there are two foramen mentale." Moreover he wrote that the "p1 is always reduced and leaf-like, separated from c and p2 by diastemata. " (Mennecart 34 , p. 67). In "Lophiomeryx" shinaoensis there is no diastema between p1 and p2 and the diastema between c and p1 is extremely reduced. The p1 is relatively big considering the root size. The lower outline of the mandible in lateral view is relatively straight. "Lophiomeryx" shinaoensis shares these characteristics with "Lophiomeryx" turgaicus 40 . Miao 20 (p. 535) already noticed strong similarities between "Lophiomeryx" turgaicus and "Lophiomeryx" shinaoensis. The lower premolars of "Lophiomeryx" turgaicus and "Lophiomeryx" shinaoensis are strongly laterally compressed and the p4 is rectangular, giving the lower premolar toothrow an more elongated aspect than in L. angarae, L. mouchelini, and L. chalaniati 20,24,30,38,40 . Moreover, in these two species, the posthypoconulidcristid is of similar length, longer than in L. angarae, L. mouchelini, and L. chalaniati.
Based on these observations, we can assume that "Lophiomeryx" shinaoensis and "Lophiomeryx" turagicus cannot be assigned to the genus Lophiomeryx and may both belong to the same new Lophiomerycidae genus that we here name Chiyoumeryx nov. gen. Chiyoumeryx nov. gen. shinaoensis differs from ?Chiyoumeryx nov. gen. turgaicus nov. comb. in being lower crowned, smaller, possessing an ectostylid, having the symphysis starting under p1, and a shorter diastema.
Chiyoumeryx nov. gen. flavimperatoris nov. sp. Figure 1C and Figure S3. v1961 cf. Miomeryx sp.-Xu: 316, 323, 324 26 . v pars1982 Lophiomeryx gracilis-Miao: 532, Table 3, Fig. 9a Lophiomeryx gracilis 20 , while IVPP V 2600 from Caijiachong marls was first described as cf. Miomeryx sp. 26 . All these specimens share the same size and dental morphology, and originate from a similar stratigraphic position. That is why we attribute them to the same species. None of these specimens can be attributed to Krabimeryx or Zhailymeryx, as the entoconidian groove is absent 14,17 . Furthermore, the external postmetacristid is more marked in the considered specimens than in Krabimeryx and Zhailymeryx, forming a deep groove. The third basin is also very different in the here-described specimens from Krabimeryx and Zhailymeryx: the third lobe is a little tilted parallel with the prehypoconulidcristid and posthypoconulidcristid. The back fossa of m3 is very narrow.
Furthermore, the here-described specimens can be distinguished from K. gracilis (previously attributed to the same species), by a smaller size and a slenderer shape. The ectostylid is smaller than in K. gracilis. The anterior cingulid in the lower molars is stronger in K. gracilis than in the here-considered specimens. The small postentocristid (especially on m3) of the here-described specimens is absent in K. gracilis.
The here-described specimens possess all characteristics in the lower molars that are typical for Chiyoumeryx nov. gen. and distinguish this genus from Lophiomeryx 24,34,37 . Furthermore, as in Chiyoumeryx nov. gen. shinaoensis, the p4 is laterally compressed giving it a more elongated aspect than in Lophiomeryx 24,34,37 . Therefore, we consider it justified assigning the here-described specimens to Chiyoumeryx nov. gen. However, they differ from Chiyoumeryx nov. gen. shinaoensis in as smaller size and the morphology of the p4: (1) the anterior conid is oblique while it is labio-lingually oriented in Chiyoumeryx nov. gen. shinaoensis. (2) There is a tiny anterior cingulid that is absent in Chiyoumeryx nov. gen. shinaoensis.

Diagnosis (modified from Mennecart et al. 36 ). Small-sized ruminant with upper molars possessing
the following combination of characters: well-marked parastyle and mesostyle in small-column shape; strong paracone rib; metacone rib absent; metastyle absent; unaligned external walls of metacone and paracone; strong postprotocrista stopping against the anterior side of the premetaconulecrista; continuous lingual cingulum, stronger under the protocone. Lower dental formula is primitive (3-1-4-3) with non-molarized premolars. Tooth c is adjacent to i3. Tooth p1 is single-rooted, reduced and separated from c and p2 by a short diastema. The premolars have a well-developed anterior conid. Teeth p2-p3 display a distally bifurcated mesolabial conid. Tooth p3 is the largest premolar. Tooth p4 displays no mesolingual conid and a large posterior valley. Regarding the lower molars, the trigonid and talonid are lingually open with a trigonid more tapered than the talonid. The anterior fossa is open, due to a forward orientation of the preprotocristid and the presence of a paraconid. The internal postprotocristid is oblique and the external postprotocristid reaches the prehypocristid. The internal postprotocristid, postmetacristid and preentocristid are fused and Y-shaped. Protoconid and metaconid display a weak Tragulus fold and a well-developed Dorcatherium fold, respectively. The mandible displays a regularly concave ventral profile in lateral view, a marked incisura vasorum, a strong mandibular angular process, a vertical ramus, and a stout condylar process. Gabunia, 1964 43 from Benara (Georgia), late Oligocene 44 .

Diagnosis.
Iberomeryx with a very large paraconid, which is smaller in Iberomeryx minor and Iberomeryx parvus. The metastylid is not strong but is more developed than in the other species. The ectostylid is big on m1, smaller on m2 and absent on m3, while I. minor displays an ectostylid on all molars and I. parvus none at all. Iberomeryx miaoi nov. sp. is of similar size to I. minor and its m2 is smaller than the one of I. parvus. It differs from I. minor by a thin anterior cingulid. Moreover, its protoconid is positioned slightly more anterior than in I. parvus. The molars appear to be more massive and bulkier in this species than in I. minor and I. parvus.
Holotype. IVPP  Taxonomical attribution. This minute ruminant was referred to Lophiomeryx gracilis? by Miao 20 . However, he already noticed that the size of this individual was smaller than in the other specimens attributed to Lophiomeryx gracilis. Miao 20 excluded an attribution of IVPP V 6551 to "Lophiomeryx" gaudryi due to a closed posterior section of the posterior fossa on the m3. However, in both teeth, the posterior fossa is still open by the reduction of the postentocristid. The here-described specimen clearly differs from Lophiomeryx by the presence of an external postmetacristid forming a slight Dorcatherium fold, a developed external postprotocristid (clearly visible at least on m2), and a large paraconid 36 . Furthermore the external postprotocristid and prehypocristid are connected on their distal ends and the third basin of m3 forms a well-formed buckle, unlike the condition in Lophiomerycidae 14,16,33,36,37 . The combination of these characters is typical for Tragulidae 36 .
Very few taxa are so far known in the early evolution of the Tragulidae. Only Archaeotragulus, Iberomeryx, and Nalameryx are recognized as potential Paleogene Tragulidae 17,36,46 , of which Archaeotragulus is currently the oldest representative described 17,47 . Archaeotragulus possesses lower molars with a broadened talonid in comparison to the trigonid and displays an entoconidian groove 36 . In the case of IVPP V 6551, the trigonid and talonid are of similar size and no specific entoconidian groove can be observed. Mennecart et al. 36 considered Nalameryx a Tragulidae notably based on the presence of the M structure (the external postmetacristid, the internal postmetacristid, the internal postprotocristid, and the external postprotocristid are interconnected forming a M in occlusal view), including the Tragulus fold and Dorcatherium fold, and the absence of a rounded mesolingual conid in the p4 35 . IVPP V 6551 differs from Nalameryx in having an m3 wider than m1 and similar m1 and m2 widths 17 . In size proportions and molar morphology, IVPP V 6551 resembles the genus Iberomeryx. In IVPP V 6551, the relative size of the m2 is more similar to I. minor. In Iberomeryx minor, the anterior cingulid is big 36,46 , while in Iberomeryx parvus the cingulid is thin 48 like in IVPP V 6551. The teeth of IVPP V 6551 appear to be more massive and bulkier than in I. minor and I. parvus 36,48 . Similarly to I. minor, the protoconid of IVPP V 6551 is a little more anterior than in I. parvus 36,48 . IVPP V 6551 clearly differs from I. parvus and I. minor by the presence of a very large paraconid, which is smaller in the two other species 36,48 . Moreover, the metastylid in IVPP V 6551 is slightly more developed than in I. minor and not present in I. parvus 43,48 . Iberomeryx minor displays an ectostylid on all molars 36 , while this structure is absent from I. parvus 48 . The ectostylid in IVPP V 6551 is large on m1 to absent on m3. Based on these differences we decided to erect the new species Iberomeryx miaoi nov. sp.

Origin of crown Ruminantia and dispersal pattern of Paleogene Eurasian ruminants. So far
five families and 13 genera of Ruminantia are known during the middle and late Eocene in Eurasia 2,18,19 . Based on molecular data, the origin of crown ruminants should be searched for between the latest late Paleocene (56.5 Ma) and the latest early Oligocene (29 Ma) 49,50 . With the description of stem Tragulidae from the early Oligocene of Western Europe (Iberomeryx) and the late Eocene from Southern Thailand (Archaeotragulus) 17 , Mennecart et al. 26 and Mennecart and Métais 51 verified that the oldest crown ruminants date back at least to the latest Eocene (34 Mya). The presence of the tragulid genus Iberomeryx in Shinao, Southern China, further confirms this and may actually represent the oldest fossil of a Tragulidae known and thus of a crown Ruminantia (37-35 Mya, Fig. 1), since no Pecora is known during the Eocene so far 51 .
The here presented reassesment of the Shinao ruminants in combination with literature data reveals a clear pattern in the distribution of Eocene ruminants. Among Archaeomerycidae, Archaeomeryx and Miomeryx are found in Northern and Central Asia [Kazhakstan, Mongolia, and northern part of China 2,21,53 (see Fig. 2)]. The lophiomerycid Lophiomeryx (as Lophiomeryx angarae) as well as the Asiatic Praetragulidae (Praetragulus) occupy the same area 2 . The Mongolian Lophiomeryx angarae is most likely closely related to the European species Lophiomeryx mouchelini. Due to the strong morphological similarities, some specimens of L. mouchelini were actually first described as Lophiomeryx cf. angarae 54 . Lophiomeryx mouchelini or its ancestors arrived in Europe with the Grande-Coupure dispersal event at the Eocene-Oligocene transition ca. 34 Mya ago (oldest European records: Calaf, Spain, MP22; Möhren 9, Germany, MP21-22; age comprised between the German localities Haag2 MP21 and Möhren 13 MP22 34,37,53 ). The close relationship of these European and the Mongolian species confirms that the origin of the Grande-Coupure cohort may be deeply anchored in the Eocene of Central-Northern Asia (Fig. 2).
The Southern part of Asia presents a totally different ruminant community at the genus level and includes the Archaeomerycidae Indomeryx and Notomeryx, the Lophiomerycidae Krabimeryx and Chiyoumeryx nov. gen., the Bachitheriidae Bachitherium and the Tragulidae Archaetrogulus and Iberomeryx 2,17-19,21,53 (see Fig. 2). The oldest Bachitherium is currently known from the Balkan area during the Eocene 18,19 . The Tethys Ocean separated this area from Western Europe until its progressive disappearance during the Oligocene, ca. 31 Mya 55,56 . Bachitherium and a cohort of rodents (Pseudocricetodon, Paracricetodon, and the Melissodontinae) 19 did not reach Western Europe prior to the opening of this passage. Similarly to the genus Bachitherium, Iberomeryx arrived in Western Europe after the drying out of the Tethys Ocean ca. 31 Mya, during the Bachitherium dispersal event 18,19,36 . Iberomeryx is mainly known from the middle early Oligocene of Western Europe 34,36,57 and the late Oligocene of Anatolia and Georgia 43,48,58 . Discovering Iberomeryx in the Eocene of Eastern Asia confirms an Asiatic origin of this genus. The close relationship between South-eastern Europe and South-eastern Asia is furthermore supported by anthracotheriids (extinct artiodactyls related to hippopotamids) and rhinocerotoids 59,60 .
Mennecart et al. 18,19 proposed that mammals originating from Asia arrived in Western Europe during the early Oligocene in two faunal events: the Grande-Coupure, ca. 33 www.nature.com/scientificreports/ ca. 31 Mya. These two faunal events imply two different and diachronous ways of dispersal. The fact that Eocene taxa from South-eastern Asia did not arrive in Western Europe prior to 31 Mya indicates that the Bachitherium dispersal Event cohort might be deeply anchored in the Eocene of Southern Asia (Fig. 2), while genera recorded from the Eocene of Central Asia are known to have arrived already during the Grande-Coupure and thus originated from a different palaeobiogeographic province. The Grande-Coupure was a dispersal event using a Northern way over the closed Turgai Strait and probably originating from Central Asia (Fig. 2). The Bachitherium dispersal event is a stepwise story with a first dispersion from Southern Asia to South-eastern Europe along the Southern path (Fig. 2) and then the dispersal throughout Europe thanks to the closure of the Tethyian Ocean 18,19 . The south-eastern part of Asia has shown very few changes from a warm and humid climate and environment since the Eocene 4 , while Northern Asia underwent a transition from warm and humid subtropical environments during the Eocene to steppe environments in the Pliocene, e.g. [3][4][5] . In this light it is not surprising that an increasing number of paleontological and geological studies indicate that Asia had already experienced a strong latitudinal environmental zonation during the middle and the late Eocene, e.g. 6,13 .
These different climatic and environmental conditions in Central and South Asia led to two distinct palaeobiogeographical provinces clearly traceable in assemblages of herbivores like ruminants that was already apparent during the Eocene. The Central Asian ruminants were living in a more arid environment than the ones from South-eastern Asia (see Fig. 2). The tropical and wet environments from the South-eastern Asia led to the emergence of the Tragulidae (Iberomeryx and Archaeotragulus) and of the anthracotheriids.

Materials and methods
Materials. The fossils are housed at the Institute of Vertebrate Paleontology and Paleoanthropology of the Chinese Academy of Sciences in Beijing. Precise descriptions and measurements of the species can be found in Supplementary data 1.

Methods.
Measurements have been realized thanks to a calliper (precision 0.2 mm) and can be found in Table S1. The dental nomenclature was modified after Bärmann and Rössner 61 (see Fig. 1).
Conventional abbreviations used in front of the year in the synonymy list follow Matthews 62 : * = the work validates the species; v = the authors have seen the original material of the reference; pars = the reference applies