The rst hunting dog from Dmanisi: comments of social behaviour in Canidae and hominins

The renowned site of Dmanisi in Georgia, southern Caucasus (ca. 1.8 Ma) yielded the earliest direct evidence of hominin presence out of Africa. In this paper, we report the rst record of a large-sized canid from this site, namely dentognathic remains, referable to a young adult individual that displays hypercarnivorous features (e.g., the reduction of m1 metaconid and entoconid) that allow us to include these specimens in the hypodigm of the late Early Pleistocene European species Canis (Xenocyon) lycaonoides. Much fossil evidence suggests that this species was a cooperative pack-hunter that, unlike other large-sized canids, was capable of social care toward kin and non-kin members of its group. Interestingly, this rather derived hypercarnivorous canid attests to one of the earliest records in Dmanisi. Its dispersal from Asia to Europe and Africa followed a parallel route to that of hominins, but in the opposite direction. Hominins and hunting dogs, both recorded in Dmanisi at the beginning of their dispersal across the Old World, are the only two Early Pleistocene mammal species with proved altruistic behaviour towards their group members, an issue discussed over more than one century in evolutionary biology. Cooper’s Cave high-crowned premolars, mesial lingual of P4 protocone, buccolingual length of the taxonomical attribution with Canis (Xenocyon)’s group. resemble those of the Asian C. chihliensis, a large-sized canid possibly belonging to a hypercarnivorous lineage of Canis 10 .


Introduction
Wild dogs are medium-to large-sized canids that possess several hypercarnivorous craniodental features and complex social and predatory behaviours (i.e., social hierarchic groups and pack-hunting of large vertebrate prey typically as large as or larger than themselves). Two extant species of wild dogs survive in the Old World, the Indian dhole, Cuon alpinus (Pallas, 1811), and the African hunting dog, Lycaon pictus (Temminck, 1820). Both species are nowadays endangered or critically endangered according to the IUCN red list of threatened species 1,2 . The African hunting dog, known also as painted dog, and the dhole are among the top predators in their respective habitats 3,4 thanks to the combination of a number of dental hypercarnivorous traits, skeletal adaptations to cursorial pack hunting and their social behaviour.
The evolution of these hypercarnivorous canids is still unknown and open to debate 5,6 .
Furthermore, there is also a great deal of confusion in the taxonomy of the extinct large-sized and hypercarnivorous canids, which use to be referred to different systematic denominations (see Supp. Inform.). Such names often hint implied or proposed a nities to extant taxa, yet seldomly based on phylogenetic analyses. Considering the results of molecular phylogenies 7,8 , from which it is evident that Lycaon and Cuon are sister taxa of the crown group of Canis, and that the large-sized members of the genus Xenocyon might be related to both Lycaon and Cuon, here we preferred to avoid names suggestive of a closer relationship to any of both genera, privileging the more parsimonious denomination Canis (Xenocyon) (see the Supp. Inform. for an in-depth discussion of the taxonomical issues).
The earliest record of a species of this group of hypercarnivorous canids corresponds to Canis (Xenocyon) cf. dubius Teilhard de Chardin (1940), which is represented by a single hemimandible 6 from the Zanda Basin (3.81-3.42 Ma; Fig. 1). The species C. (Xenocyon) dubius is generally related to the lineage of Cuon 6,9 . A younger but more complete specimen from Fan Tsun (Taigu 10 ) was ascribed to Canis (Xenocyon) antonii (ca. 2.5 Ma) 11 . The latter canid is large-sized and displays evident dental features hinting to an incipient adaptation to a hypercarnivorous diet.  13 . Some of the morphologies of the holotype from Cooper's Cave (i.e., the high-crowned upper premolars, their mesial occlusal morphology, the lingual projection of P4 protocone, and the relative buccolingual length of the M1) cast doubts on its taxonomical attribution and its actual relation with Canis (Xenocyon)'s group. Moreover, the upper teeth resemble those of the Asian C. chihliensis, a large-sized canid possibly belonging to a hypercarnivorous lineage of Canis 10 .
During the late Early Pleistocene (i.e., Calabrian; 1.8-0.8 Ma), while other more primitive species remained in Africa [e.g., Canis (Xenocyon) atrox Broom 14 in Kroomdrai A; Fig. 1] a more derived form of Canis (Xenocyon) appeared and became widespread across the whole Old World (Fig. 1). Canis (Xenocyon) lycaonoides (Kretzoi, 1938) was a large-sized canid that resembled C. (Xenocyon) gr. falconeri but with more derived craniodental features (e.g., the P4 protocone tends to attach to the tooth; the M1 metaconule is crest-like; the M1 talon is reduced; the m1 hypoconid is enlarged and tends to be centred in the talonid; the entoconid is reduced, being represented by a small crest-like cuspulid; and the m3 is single cusped). Its earliest record appears to be that of Tamagawa River near Tokyo (Japan, 15; Fig. 1). This locality is loosely dated to 2.1-1.6 Ma, based on the associated fauna and ichnofauna 16 . In spite of its uncertain chronology, this early occurrence suggests an eastern Asian origin for this hypercarnivorous species. Subsequently, during the late Early Pleistocene and the base of the Middle Pleistocene, from 1.8 to 0.7 Ma, C. (Xenocyon) lycaonoides became one of the most common and important members of the carnivoran palaeoguild of Eurasia (Fig. 1). Moreover, C. (Xenocyon) lycaonoides dispersed also in Africa, where it is documented in the northern and eastern part of the continent (e.g., Olduvai Bed II; Fig. 1).
Considering the overall cranial morphology and its dental features, which con rm the original interpretation by Kretzoi 17 , Martínez-Navarro & Rook 5 deemed C. (Xenocyon) lycaonoides as strictly related to extant L. pictus. Similar conclusions were shared by several other scholars 10,18 , who supported also a Eurasian origin for the living African hunting dog.
Among extant Carnivora, Lycaon pictus has one of the most complex, structured and unique social behaviours 3 . As one of the closest relatives to L. pictus, C. (Xenocyon) lycaonoides, the Eurasian hunting dog, might have had comparable complex sociality. Carbone and co-authors 19 showed that the metabolic energy requirements for large-sized species (< 21.5 kg) force them to hunt prey larger than themselves and thus, in hypercarnivorous Canidae, cooperatively. As such, this element allows us to gure the social behaviour of extinct hypercarnivorous canids, even with limited direct evidence. Nevertheless, apart from indirect and inferred evidence, direct proof of social behaviour in the Eurasian hunting dog have been proposed 20,21 .
Here we report the rst occurrence of wild dogs from the Georgian site of Dmanisi ( Fig. 1 22 . This locality preserves an outstanding fossil record, both in terms of abundance, completeness of skeletal remains and preservation status, as testi ed by the recently described molecular phylogeny based on a fossil rhino tooth 23 . In this paper, we describe the newly discovered remains, identifying them taxonomically and interpreting in the frame of Early Pleistocene diversity of Canis (Xenocyon). Moreover, the site of Dmanisi yielded the earliest direct evidence of hominin presence out of Africa in their dispersal throughout Eurasia 24,25 with also indication of complex sociality among individuals of this population 26,27 . The co-occurrence of two highly social species in the same site at 2.0-1.8 Ma, a time of extreme diversi cation and expansion of the two clades 5,6 from their centre of origin, raises interest in the role played by social behaviour and by mutually-bene cial cooperation and reciprocity in the geographic expansion of these species. Questions to be explored in this paper.

Results
Implications for fossil Hunting dogs Diversity. The discovery of a large-sized canid in the Georgian site of Dmanisi represents an important discovery adding valuable information to the current knowledge of canid radiation during the second half of the Early Pleistocene (early Calabrian). Despite the fragmented nature of the specimens, the set of features possessed by D6327 ( Fig. 2A-F and Augmented Reality content) allow a con dent attribution to Canis (Xenocyon) lycaonoides (see Supplementary Information), the plausible ancestor of extant African hunting dog 5,18 . As such, this record is the oldest occurrence of Eurasian hunting dog, and it precedes burst of dispersion that the species experienced across the entire Old World during the Calabrian 5,10,15 .
Dietary preferences of Dmanisi Hunting dog. In order to test the dietary adaptations of the Dmanisi hunting dog and other Early Pleistocene forms, a linear discriminant analysis was performed over the extant canids (31 species, 244 specimens; craniodental measurements kindly provided by B. Van Valkenburgh), which were grouped in two feeding groups: (i) omnivores (i.e., meso-and hypocarnivores; 27 extant species, 210 specimens), in which vertebrate esh represents less than 70% of their dietary requirements; and (ii) hypercarnivores (four extant species, 34 specimens), which diet consists almost entirely of vertebrate esh and are pack-hunters of prey as large as or larger than themselves. Seven metric variables of this dataset for which the measurements were available in the Dmanisi specimens were used in the analysis: length and breadth of the third lower premolar (p3L and p3B, respectively), length and breadth of the trigonid basin of the lower carnassial (m1trigL and m1trigB, respectively), length and breadth of the talonid basin of the lower carnassial (m1talL and m1talB, respectively), and jaw depth measured at the limit between p3 and p4 (JDp4). The linear discriminant function, obtained with cross validations using the leave one out method, correctly allocated 98.8% of the specimens to their feeding group (Fig. 3). Indeed, all omnivores and all hypercarnivores, apart from the four specimens of the small-sized S. venaticus, were correctly classi ed (Fig. 3). According to the loadings of the variables in the discriminant function, the hypercarnivores show third premolars that are relatively mesiodistally shorter and buccolingually narrower compared to those of omnivorous species, as well as a carnassial with an enlarged trigonid blade and a reduced talonid basin, and a deeper, more stoutly-built corpus, which is in agreement with previous analyses of adaptations in canids towards hypercarnivory 28,29 . This function reclassi ed unequivocally the individual from Dmanisi (values of the variables obtained from D6327) in the group of hypercarnivores (Fig. 3), with a probability of pertinence of 0.97. The two specimens of C. (Xenocyon) lycaonoides from Venta Micena (a site that is slightly younger in age than Dmanisi, ca 1.6 Ma) for which these measurements were available were also classi ed as hypercarnivores. However, they show higher scores in the discriminant function, close to the group centroid of hypercarnivores. Similarly, the specimen from Untermassfeld, a site of Jaramillo age, (ca. 1.0 Ma), shows the highest scores among the fossil hunting dogs, which re ects its more advanced adaptations towards hypercarnivory, similar to those of extant African hunting dogs. These results con rm that the craniodental morphological features of the Eurasian hunting dog from Dmanisi (Fig. 2) were well suited for a diet consisting exclusively of vertebrate esh. Moreover, it shows that there was a gradual evolution of these craniodental adaptations in C. (Xenocyon) lycaonoides from the oldest members of the lineage to the most derived ones, con rming the morphological evidence, as pointed out by other scholars 5,10,18,30 .

Discussion
Dmanisi, located near the crossway between Africa and Eurasia, is a key site to explain the dispersal large mammal species, in a time of great faunal turnovers in the whole Old World 31,32 . This Georgian site also records the earliest direct evidence of hominin out of Africa and into Eurasia, at ca. 1.8 Ma. Here, we report the record of the Eurasian hunting dog, C. (Xenocyon) lycaonoides, which testi es to the beginning of the dispersal of this more derived, frankly hypercarnivorous canids from its eastern Asia region of origin, similarly to Canis borjgali Bartolini Lucenti et al., 2020 (the mesocarnivorous, wolf-like species also recorded in Dmanisi 33 ). During the Calabrian C. (Xenocyon) lycaonoides became a common element of the entire Old-World faunas during the late Early-early Middle Pleistocene 18 , when it even reached North America 10 . In this dispersal, the Eurasian hunting dog followed at the same time the same dispersal pattern of hominids, just in the opposite direction. The co-occurrences of both species along their dispersal routes together with some other large-sized carnivore taxa, for instance the dirk-toothed cat of African origin Megantereon whitei (Broom, 1937), suggest that the ecological conditions favoured the dispersal of these species at that time. Large-sized carnivorans like this felid has been recognized as important supplier of scavengeable resources for the hominins in direct competition with the supercarrion-eater Pachycrocuta brevirostris 34,35 .
Social behaviour of Canis (Xenocyon) and Homo in the late Early Pleistocene. "There is, at the same time, as much, or perhaps even more, of mutual support, mutual aid, and mutual defense: Sociability is as much a law of nature as mutual struggle" 36 . Probably, the most relevant common feature between the extinct hominins and the fossil hunting dogs is the fossil evidence on the mutually-bene cial cooperation, reciprocity and social behaviour 37 of both species. This is well documented in Dmanisi by the nding at this site of an edentulous individual of Homo erectus (composite skull D 3444/D 3900) who lost all but one of its teeth several years before the time of its death, as evidenced by extensive bone loss in the maxilla and mandible due to resorption of the tooth alveoli. This old individual could not chew its hard or coriaceous food by itself, which means that its survival after the loss of the majority of its teeth probably relied on the assistance from other members of the family group 26 (Fig. 4A). As it has been noted 26,27 this kind of altruistic behaviour is beyond forms of biological altruism, proper of non-primate mammals or even "non-human primates" 27 . This suggests that altruistic behaviour and care of the elderly might have developed very early in hominins, at least two million years ago 26,27 . Among Carnivora, social behaviour is frequent, considering the numerous bene ts that cooperation offers to carnivorans (increased breeding success and individual survival; enhanced hunting success; ability to kill on larger prey; deterrent and strength against kleptoparasites; help for the rearing of pups 38,39 . Canidae have some of the best-known examples of social organization of all mammals (e.g., the grey wolf, C. lupus 40 ). Probably less known, yet interesting is the case of the African hunting dogs. This hypercarnivore species display a more complex and peculiar set of behaviour, unique among Canidae, if not carnivorans. This includes exclusive cooperative hunt, obligate cooperative breeding 41 and prioritized access of the pups to the kills 3 . Many authors 42 noted a reduced degree of aggressivity between pack members in comparison to other social Canidae (C. lupus and Cuon alpinus 40 ) even during the consumption of the kill 3 . 19 proved the necessity for large canids, weighing more than 21.5 kg, to hunt cooperatively to kill on prey larger than themselves. The C. (Xenocyon) lycaonoides is indeed a large-sized hypercarnivorous species. Body-size estimates suggests that this canid was similar to L. pictus (whose average weight is 20-25 kg (44)) if not larger (estimated weight of C. (Xenocyon) lycaonoides = 28 kg, (20)). The individual from Dmanisi, despite being a young adult, would have been rather robust (around 30 kg, applying the regression equation of Van Valkenburgh 45 ). Such a body mass, coupled with its marked hypercarnivorous features, support the idea that C. (Xenocyon) lycaonoides adopted cooperative hunting strategies, similar to the extant canids, C. lupus, C. alpinus and L. pictus. Further support of a highly social group organization is provided by fossil pathological specimens. Recently, Tong et al. 21 described injuries in the sample of Shanshenmiaozui, Nihewan Basin, dated to 1.2 Ma. One of them records a dental infection likely in icted by processing hard food, such as bone; the other suffered a displaced fracture of its tibia and, despite such a severe injury (which would represent a death sentence for a solitary predator) it managed to survive the trauma to heal. The long period that was presumably required for healing the compound fracture, as well as the incapacitating nature of this trauma for a cursorial predator during the rest of its life (as the healed tibia was considerably shortened), suggests social hunting strategies and provision by other members of the family/pack (primarily food-sharing). Similar pathologies have been also detected in the Late Pleistocene population of Canis dirus Leidy, 1858 from La Brea tar pits in southern California 46 . This is not surprising considering that packs of extant canids temporarily support wounded or sick members of their group, as reported by many authors in both extant C. lupus and L. pictus 39 , despite the cost in terms of e ciency of the group 47 . Nevertheless, in the case of African hunting dogs, several studies describe the tolerance by group members not only for injured, but also for disabled or old individuals at the kills 39,48 . Furthermore, disabled or old African hunting dogs receive food by fellow pack members via regurgitation 39,49 , a way of food-sharing that other canids reserve exclusively to kin, very rarely non-kin, pups and to the breeding female. The fossil record yields evidence of similar behaviour in extinct hunting dog as well. An altruistic behaviour of food provisioning to disabled individuals was documented in C. (Xenocyon) lycaonoides at the site of Venta Micena (Fig. 4B). Here a nearly complete cranium with a mandible preserved in anatomical connection were unearthed (skull VM-7000) 20 . This skull belonged to a 7-8 years-old individual (considering the moderate-heavy dental wear of its teeth). By far the most sticking features of this specimen are the high degree of cranial uctuating asymmetry and several tooth anomalies, including dental agenesia of the upper right canine, the P3 and m3. These teeth were not broken or lost during the life of the individual, as showed by CTscans and radiographs of the cranium 20 . The dental alveolus of the right upper canine is completely absent, as for the other teeth 20 . Moreover, the right m2 is missing and its alveolus is partially reabsorbed. The malformations of the C. (Xenocyon) lycaonoides from Venta Micena were probably due to developmental instabilities resulting from a high level of genetic homozygosity in the relatively small population of wild dogs that inhabited the Baza Basin during late Early Pleistocene times 20 . However, despite the numerous congenital disabilities, the individual VM-7000 was able to reach adulthood, which probably affected or even precluded its ability in the pack-hunting activities (Fig. 4B). This suggests that cooperative behaviour and food provisioning from other members of the family group were the only way for this individual to survive until this age 20 . Similarly, to the old human from Dmanisi, who managed to reach such an old age thanks to the altruistic help and care of other family members (Fig. 4A), this hunting dog reached adulthood. Therefore, these ndings apparently suggest that increased cooperation and altruistic behaviour may have been important factors for the survival and dispersal of both humans and large social carnivorans in the open environments of Africa, Eurasia and North America. Interestingly, hunting dogs and hominids are up to now the only late Early Pleistocene highly-social species with proved altruistic behaviour towards other members of their group, including food sharing to group members. Such a behaviour is specially developed in extant African hunting dogs, where individuals with limitations resulting from genetic abnormalities, pathologies and/or advanced age are helped and sustained by the other members of the family group 39,41,42 . Canis (Xenocyon) lycaonoides showed a similar pattern cooperative and altruistic behaviour towards pack-members 20,21 . The occurrence of the Eurasian hunting dog in Dmanisi marks one the rst and better chronologically-constrained record of this large-sized, pack-hunter canid.

Sociality in fossil canids had been investigated by numerous authors 43 and Carbone and coauthors
The success of this wide-ranging dispersion across continents 5,10 , unprecedented and never reached by any other large-sized canids, might be correlated also to the advantages of the mutually-bene cial cooperation and altruistic nature of these fossil hunting dogs, as the result of an evolutionary tendence leading to co-operation among members of a species: "the best pathway to advantage for individuals" 50 .
It would not be necessary, but we have here a new evidence of the importance of Dmanisi for that, paraphrasing Dawkins 51 , Homo and highly social Canidae both are descended from highly social ancestors and their ancestors lived in groups; this was not an option but an essential survival strategy and from this mutual aid arose.

Materials And Methods
The present study is based on the comparative morphological analysis of the large-sized Canis (Xenocyon) from Dmanisi and other Plio-Pleistocene hypercarnivorous canids of the Old World. The described fossils are housed at the S. Janashia Museum of Georgia, Georgian National Museum (Tbilisi) (MG-GNM). As comparative fossil material, the Villafranchian and Epivillafranchian canids from the Old World and North America housed at AMNH, AUT, ICP, IGF, and MNHN (see abbreviations below) were studied. This fossil comparative sample includes specimens of Canis (Xenocyon) dubius from Zhoukoudian 52 11 . The relevant literature on these canids was reviewed 6,10,13,14,30,52,54-55,58-59 . Extant specimens housed at the AMNH, MZUF, ICP, RMCA and MG-GNM (see abbreviations below) were also used for morphological and metrical comparisons. We examined specimens of Canislupus Linnaeus, 1758, and Lycaonpictus (Temminck, 1820). Moreover, a wide data set of craniodental measurements taken in modern canids (244 specimens from 31 species) by Prof. Blaire Van Valkenburgh was used also in some statistical comparisons, including a discriminant analysis between omnivorous (i.e., meso-and hypocarnivorous) and hypercarnivorous canids, in order to deliver palaeoecological inferences for the Dmanisi wild dogs and also for others from different (and younger) sites, like Venta Micena in Spain and Untermassfeld in Germany.