Abstract
The Old World fossil record of the family Camelidae is patchy, but a new partial cranium and some other remains of Camelus grattardi from the Mille-Logya Project area in the Afar, Ethiopia, greatly increase the fossil record of the genus in Africa. These new data – together with analysis of unpublished and recently published material from other sites, and reappraisal of poorly known taxa – allow for a comprehensive phylogenetic analysis showing that C. grattardi is the earliest (2.2–2.9 Ma) and most basal species of the genus. We also show that the lineages leading to the extant taxa C. dromedarius and C. bactrianus diverged much higher in the tree, suggesting a recent age for this divergence. A late divergence date between the extant species is consistent with the absence of any fossil forms that could be ancestral, or closely related, to any of the extant forms before the late Pleistocene, but stands in contrast to molecular estimates which place the divergence between the dromedary and the Bactrian camel between 8 and 4 million years ago.
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Alberdi MT, Morales J, Moya S, Sanchiz B (1981) Macrovertebrados (Reptilia y Mammalia) del yacimiento finimioceno de Librilla (Murcia). Estud geol 37: 307–312
Alemseged Z, Barr WA, Bobe R, Geraads D, McPherron S, Reed D, Wynn J (2016) A new late Pliocene fauna from the Mille-Logya Project (MLP) area, Afar regional state, Ethiopia. 24th annual meeting of the Paleoanthropology Society, Atlanta, GA
Arambourg C (1979) Vertébrés villafranchiens d'Afrique du Nord (artiodactyles, carnivores, primates, reptiles, oiseaux). Fondation Singer-Polignac, Paris, 141 pp
Aubekerova PA (1974) New giant camel from Pliocene deposits of Tekess depression. Materials for the history of fauna and flora of Kakakhstan. Akad Nauk SSR Kazhakstan Inst Zool 6: 74–82 [in Russian]
Baigusheva VS (1971) Fossil theriofauna of the Liventzovka sand-pit. Tr Zool Inst Akad Nauk 49: 5–29 [in Russian]
Bibi F, Rowan J, Reed K (2017). Late Pliocene Bovidae from Ledi-Geraru (lower Awash Valley, Ethiopia) and their implications for Afar paleoecology. J Vertebr Paleontol. https://doi.org/10.1080/02724634.2017.1337639
Boule M, Breuil H, Licent E, Teilhard de Chardin P (1928) Le Paléolithique de la Chine. Arch Inst paléontol hum 4: 1–138
Bremer K (1988) The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42: 795–803
Colbert EH (1935) Siwalik mammals in the American Museum of Natural History. Trans Am Philos Soc 26: 1–401
Colombero S, Bonelli E, Pavia M, Repetto G, Carnevale G (2017) Paracamelus (Mammalia, Camelidae) remains from the late Messinian of Italy: insights into the last camels of western Europe. Hist Biol 29: 509–518
Cui P, Ji R, Ding F, Qi D, Gao H, Meng H, Yu J, Hu S, Zhang H (2007) A complete mitochondrial genome sequence of the wild two-humped camel (Camelus bactrianus ferus): an evolutionary history of Camelidae. BMC Genomics 8(241). https://doi.org/10.1186/1471-2164-8-241
Falconer H, Cautley PT (1836) Note on the fossil camel of the Siwalik Hills. Asiatic Res 19: 115–134
Falconer H, Cautley PT (1846) Fauna Antiqua Sivalensis, Being the Fossil Zoology of the Sewalik Hills, in the North of India. Smith, Elder and Co, London, 590 pp
Faye B, Konuspayeva G (2012) The encounter between Bactrian and dromedary camels in Central Asia. In: Knoll EV, Burger P (eds) Camels in Asia and North Africa: Interdisciplinary Perspectives on their Past and Present Significance. Österreichische Akademie der Wissenschaften, Wien, pp 27–33
Flamand GBM (1902) Sur l'utilisation, comme instruments néolithiques, de coquilles fossiles à taille intentionnelle (littoral nord-africain). C R Assoc fr Av Sci 30: 729–734
Frick C (1921) Extinct vertebrate faunas of the badlands of Bautista Creek and San Timoteo Cañon, southern California. Univ Calif Publ Bull Dept Geol 12: 277–424
Gaur R, Raghavan P, Chopra SRK (1984) On the remains of Camelus sivalensis (Artiodactyla, Camelidae) from Pinjor Formation of upper Sivaliks. Ind J Earth Sci 11: 158–165
Geraads D (1986) Ruminants pléistocènes d'Oubeidiyeh. Mém Trav Cent Rech fr Jérus 5: 143–181
Geraads D (2014) Camelus grattardi nov. sp., a new camel from the Shungura Formation, Omo Valley, Ethiopia, and the relationships of African fossil Camelidae (Mammalia). J Vertebr Paleontol 34: 1481–1485
Geraads D, Bernoussi R (2016) Hippopotamidae, Suidae et Camelidae. In: Raynal J-P, Mohib A (eds) Préhistoire de Casablanca. 1. La Grotte des Rhinocéros (Fouilles 1991 et 1996). Villes et Sites Archéologiques du Maroc, 6, Ministère de la Culture, INSAP, Rabat, pp 133–134
Goloboff PA, Catalano SA (2016) TNT version 1.5, including a full implementation of phylogenetic morphometrics. Cladistics 32: 221–238
Goloboff PA, Farris J, Nixon K (2003) TNT, Tree analysis using New Technology [software]. www.lillo.org.ar/phylogeny/tnt
Grattard J-L, Howell FC, Coppens Y (1976) Remains of Camelus from the Shungura Formation, lower Omo Valley. In: Coppens Y, Howell FC, Isaac GLl, Leakey REF (eds) Earliest Man and Environments in the Lake Rudolf Basin. University of Chicago Press, Chicago, pp 268–274
Gray AP (1972) Mammalian Hybrids: A Check-List with Bibliography. Commonwealth Agricultural Bureaux, Slough, 262 pp
Gray JE (1821) On the natural arrangment of vertebrose animals. London Medical Repository 15: 296–310.
Haas G (1966) On the Vertebrate Fauna of the Lower Pleistocene Site 'Ubeidiya. Israel Academy of Sciences and Humanities, Jerusalem, 68 pp
Harris JM (1991) Camelidae. In: Harris JM (ed) Koobi Fora Research Project. Volume 3: The Fossil Ungulates: Geology, Fossil Artiodactyls and Palaeoenvironments. Clarendon Press, Oxford, pp 86–91
Harris JM, Geraads D, Solounias N (2010) Camelidae. In: Werdelin L, Sanders WJ (eds) Cenozoic Mammals of Africa. University of California Press, Berkeley, pp 815–820
Harrison JA (1985) Giant camels from the Cenozoic of North America. Smithson Contrib Paleobiol 57: 1–29
Heintzman PD, Zazula GD, Cahill JA, Reyes AV, MacPhee RDE, Shapiro B (2015) Genomic data from extinct North American Camelops revise camel evolutionary history. Mol Biol Evol 32: 2433–2440
Honey JG, Harrison JA, Prothero DR, Stevens MS (1998) Camelidae. In: Janis CM, Scott KM, Jacobs LL (eds) Evolution of Tertiary Mammals of North America. Volume 1. Terrestrial Carnivores, Ungulates, and Ungulatelike Mammals. Cambridge University Press, Cambridge, pp 439–462
Hooijer DA (1961) Middle Pleistocene mammals from Latamne, Orontes Valley, Syria. Ann archéol Syrie 11: 117–132
Howell FC, Fichter LS, Wolf R (1969) Fossil camels in the Omo beds, southern Ethiopia. Nature 223: 150–152
Khaveson IaI (1954) Camels from the Tertiary of the oriental hemisphere (genus Paracamelus). Trudy paleontol Inst 47: 100–162 [in Russian]
Khaveson IaI (1950) Camels of the genus Paracamelus. Dokl Akad Nauk SSSR 70: 917–920 [in Russian]
Khomenko IP (1912) Camelus bessarabiensis und andere fossile Formen Süd-Bessarabiens. Travaux de la Société des Naturalistes et des Amateurs des Sciences naturelles de Bessarabie, 3:92–127 [Russian and German]
Kostopoulos DS, Sen S (1999) Late Pliocene (Villafranchian) mammals from Sarikol Tepe, Ankara, Turkey. Mitt Bayer Staatssamml Paläontol hist Geol 39:165–202
Kozhamkulova BS (1986) The late Cenozoic two-humped (Bactrian) camels of Asia. Quartärpaläontologie 6: 93–97
Leidy J (1886) Mastodon and llama from Florida. Proc Acad Nat Sci Philadelphia 1886:11–12
Likius A, Brunet M, Geraads D, Vignaud P (2003) Le plus vieux Camelidae (Mammalia, Artiodactyla) d'Afrique: limite Mio-Pliocène, Tchad. Bull Soc géol Fr 174: 187–193
Logvynenko VM (2000) Camels (Camelidae, Tylopoda) from the Pliocene and Pleistocene of Ukraine. Vestn zool Suppl 14: 120–127 [in Ukrainian]
Logvynenko V (2001) Paracamelus minor (Camelidae, Tylopoda) – A new camelid species from the middle Pliocene of Ukraine. Vestn zool 35: 39–42
Martini P, Costeur L, Le Tensorer J-M, Schmid P (2015) Pleistocene camelids from the Syrian desert: the diversity in El Kowm. Anthropologie 119: 687–693
Martini P, Geraads D (2018) Camelus thomasi (Mammalia, Camelidae) from the type-locality Tighennif, Algeria. Geodiversitas 40: 115–134
Martini P, Schmid P, Costeur L (2017) Comparative morphometry of the Bactrian camel and dromedary. J Mammal Evol 25: 407–425
Marshall CR (2008) A simple method for bracketing absolute divergence times on molecular phylogenies using multiple fossil calibration points. Am Nat 171: 726–742.
Matthew WD, Cook HJ (1909) A Pliocene fauna from western Nebraska. Bull Am Mus Nat Hist 50: 59–210
Morales J (1984) Venta del Moro: su macrofauna de mamíferos, y bioestratigrafía continental del Mioceno terminal Mediterraneo. PhD thesis, Universidad Complutense de Madrid
Morales J, Soria D, Aguirre E (1980) Camélido finimioceno en Venta del Moro, primera cita para Europa Occidental. Estud geol 36: 139–142
Nanda AC (1978) Occurrence of Camelus sivalensis Falconer and Cautley from the Tatrot Formation of Ambala, India. J Geol Soc India 19: 160–164
Nehring A (1901) Herr A. Nehring gab eine vorläufige Mittheilung über einen fossilen Kamel-Schädel (Camelus knoblochi) von Sarepta an der Wolga. Sitz-Ber Gesell naturforsch Freunde Berlin 5: 137–144
Orlov YA (1927) Über die Reste eines fossilen Kamels aus dem Gouvernement Akmolinsk (West-Sibirien). Ežegod zool muž 28: 496–538
Orlov YA (1929) Über die Reste der fossilen Cameliden aus dem Gouv. Akmolinsk (Westsibirien). Ežegod zool muž 30: 549–587
Patnaik R (2013) Indian Neogene Siwalik mammalian biostratigraphy. An overview. In: Wang X, Flynn LJ, Fortelius M (eds) Fossil Mammals of Asia: Neogene Biostratigraphy and Chronology. Columbia University Press, New York, pp 423–444
Pavlow M (1904) Procamelus du gouvernement de Kherson. Mém Soc Nat nouv Russie 25: 113–133
Pickford M, Morales J, Soria D (1995) Fossil camels from the upper Miocene of Europe: implications for biogeography and faunal change. Geobios 28: 641–650
Pomel A (1893) Paléontologie - Monographies - Caméliens et Cervidés. Carte géologique de l'Algérie, Alger, 50 pp
Przewalski NM (1878) From Kul’dzha through Tyan’-Shan’ to Lob-Nor. St Petersburg [in Russian]
Rădulescu C, Burlacu D (1993) On the presence of Paracamelus alutensis (Gr. Ştefănescu) (Camelidae, Mammalia) at Frăteşti (Giurgiu Dept., Romania). An Univ Bucureşti Geol 42: 65–68
Robinson JR, Rowan J, Campisano CJ, Wynn JG, Reed KE (2017) Late Pliocene environmental change during the transition from Australopithecus to Homo. Nature Ecol Evol 1(159) doi:https://doi.org/10.1038/s41559-017-0159
Rowan J, Locke EM, Robinson JR, Campisano CJ, Wynn JG, Reed KE (2016) Fossil Giraffidae (Mammalia, Artiodactyla) from Lee Adoyta, Ledi-Geraru, and late Pliocene dietary evolution in giraffids from the lower Awash Valley, Ethiopia. J Mammal Evol. https://doi.org/10.1007/s10914-016-9343-z
Rowan J, Martini P, Likius A, Merceron G, Boisserie J-R (2018) New Pliocene remains of Camelus grattardi (Mammalia, Camelidae) from the Shungura Formation, lower Omo Valley, Ethiopia, and the evolution of African camels. Hist Biol. https://doi.org/10.1080/08912963.2017.14234852018
Rybczynski N, Gosse JC, Harington CR, Wogelius RA, Hidy AJ, Buckley M (2013) Mid-Pliocene warm-period deposits in the high arctic yield insight into camel evolution. Nature Comm 4(1550). doi:https://doi.org/10.1038/ncomms2516
Sahni MR, Khan E (1988) Pleistocene Vertebrate Fossils and Prehistory of India. Books and Books, New Dehli, 80 pp
Schlosser M (1903) Die fossilen Säugethiere Chinas. Abh k bayer Akad Wiss Math-Phys Kl 22:1–220
Sen S (2010) Camels do not occur in the late Miocene mammal locality of Çobanpinar, Turkey. Russ J Theriol 9: 87–91
Simionescu I (1930) Les vertébrés pliocènes de Măluşteni (Roumanie). Publ Fond Vasile Adamachi 9: 1–69
Simionescu I (1932) Tertiäre und pleistozäne Camelidae in Rumänien. Bull Sect sci Acad roum 15: 1–8
Ştefănescu G (1895) Le chameau fossile de Roumanie. Anu Mus Geol Paleontol 1894: 91–123
Ştefănescu G (1910) Le chameau fossile de Roumanie est l'ancêtre des chameaux dromadaire et du chameau sauvage d'Afrique. Anu Mus Geol Paleontol 4: 48–69
Steiger C (1990) Vergleichend morphologische Untersuchungen an Einzelknochen des postkranialen Skeletts der Altweltkamele. PhD thesis, Tierärztlichen Ludwig-Maximilians Universität, München
Strauss D, Sadler PM (1989) Classical confidence intervals and Bayesian probability estimates for ends of local taxon ranges. Math Geol 21: 411–427.
Stromer E (1902) Wirbeltierreste aus dem mittleren Pliocän des Natrontales und einige subfossile und recente Säugetierreste aus Aegypten. Z dtsch geol Ges 54: 108–115
Svistun VI (1971) New findings of camel (Tylopoda, Camelidae) remains in Pontian deposits of the south of the USSR European part. Vestn zool 1: 64–68 [in Russian]
Swofford DL (2003) PAUP* phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland. Version 4.01 (build 163)
Teilhard de Chardin P, Piveteau J (1930) Les mammifères fossiles de Nihowan, Chine. Ann Paléontol 19: 1–134
Teilhard de Chardin P, Trassaert M (1937) The Pliocene Camelidae, Giraffidae, and Cervidae of south-eastern Shansi. Palaeontol Sin C 1 (102): 1–68
Titov VV (2003) Paracamelus from the late Pliocene of the Black Sea region. In: Petculescu A, Ştiucă E (eds) Advances in Vertebrate Paleontology 'Hen to Panta'. Emil Racoviţǎ Institute of Speleology, Bucharest, pp 17–24
Titov VV (2008) Habitat conditions for Camelus knoblochi and factors in its extinction. Quaternary Int 179: 120–125
Titov VV, Logvynenko V (2006) Early Paracamelus (Mammalia, Tylopoda) in Eastern Europe. Acta zool cracov 49A: 163–178
Topachevskiy VA (1956) Remains of small camel (Paracamelus alutensis) from the upper Pliocene deposits of the south of Ukraine. Akad Nauk Ukr RSR, Tr Inst Zool 13: 93–100 [in Ukrainian]
Van der Made J, Morales J (1999) Family Camelidae. In: Rössner GE, Heissig K (eds) The Miocene Land Mammals of Europe. Pfeil, München, pp 221–224
Van der Made J, Morales J (2013) Camelids do not occur in the late Miocene mammal locality of Çoban Pinar, Turkey – Omissions and contradictions. Russ J Theriol 12: 39–40
Van der Made J, Morales J, Sen S, Aslan F (2002) The first camel from the upper Miocene of Turkey and the dispersal of the camels into the Old World. C R Palevol 1: 117–122
World Association of Veterinary Anatomists (1973) Nomina Anatomica Veterinaria, second ed. A Holzhausen's successors, Vienna, 218 pp
Wu H, Guang X, Al-Fageeh MB, Cao J, Pan S, Zhou H, Zhang L, Abutarboush MH, Xing Y, Xie Z, Alshanqeeti AS, Zhang Y, Yao Q, Al-Shomrani BM, Zhang D, Li J, Manee MM, Yang Z, Yang L, Liu Y, Zhang J, Altammami MA, Wang S, Yu L, Zhang W, Liu S, Ba L, Liu C, Yang X, Meng F, Wang S, Li L, Li E, Li X, Wu K, Zhang S, Wang J, Yin Y, Yang H, Al-Swailem AM, Wang J (2014) Camelid genomes reveal evolution and adaptation to desert environments. Nature comm 5 (5188): 1–9
Zdansky O (1926) Paracamelus gigas Schlosser. Palaeontol Sin C2 (4): 1–44
Acknowledgments
We thank the Authority for Research and Conservation of Cultural Heritage and the Afar Regional State for permission to conduct field work in the Mille-Logya area. We also express our gratitude to the people of the Mille and Logya towns and environs for permission and logistical support. We are grateful to C. Argot and J. Lesur (MNHN), G. Baryshnikov (ZIN), D. Berthet (CCEC), P. Brewer (NHMUK), J. Galkin (AMNH), T. Getachew and Y. Assefa (NME), M. Muungu (KNM), and E. Robert (UCBL) for access to collections, to J.-P. Brugal, Y. Chaïd-Saoudi, B. Kear, T. Krakhmalnaya, P. Martini, J. Morales, R. Patnaik, N. Podoplelova, G. Rössner, and V. Titov for photos and other data on fossil collections, to P. Loubry for the photos of Fig. 4, to V. Codrea, P. Martini, and N. Spassov for their help with foreign literature, and to S. Colombero and J. Rowan, whose comments significantly improved the manuscript. Funding to conduct field work was provided by Margaret and Will Hearst.
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Supplementary Information 1
3D reconstruction of NME-MLP-1346 (made with Agisoft Photoscan). (PDF 2071 kb)
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Description of the characters used in the parsimony analysis; matrix and character list, in TNT format. (DOCX 1975 kb)
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Raw measurements used in Supplementary Information 1 (XLSX 47 kb)
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Matrix used in the parsimony analysis, in Nexus format. (NEX 14 kb)
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Geraads, D., Barr, W.A., Reed, D. et al. New Remains of Camelus grattardi (Mammalia, Camelidae) from the Plio-Pleistocene of Ethiopia and the Phylogeny of the Genus. J Mammal Evol 28, 359–370 (2021). https://doi.org/10.1007/s10914-019-09489-2
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DOI: https://doi.org/10.1007/s10914-019-09489-2