Abstract
The domestication of wolves is currently under debate. Where, when and from which wolf sub-species dogs originated are being investigated both by osteoarchaeologists and geneticists. While DNA research is rapidly becoming more active and popular, morphological methods have been the gold standard in the past. But even today morphological details are routinely employed to discern archaeological wolves from dogs. One such morphological similarity between Canis lupus chanco and dogs was published in 1977 by Olsen and Olsen. This concerns the “turned back” anatomy of the dorsal part of the vertical ramus of the mandible that was claimed to be specific to domestic dogs and Chinese wolves C. lupus chanco, and “absent from other canids”. Based on this characteristic, C. lupus chanco was said to be the progenitor of Asian and American dogs, and this specific morphology has been continuously used as an argument to assign archaeological specimens, including non-Asian and non-American, to the dog clade. We challenged this statement by examining 384 dog skulls of 72 breeds and 60 skulls of four wolf sub-species. Only 20 % of dog mandibles and 80 % of C. lupus chanco showed the specific anatomy. In addition, 12 % of Canis lupus pallipes mandibles showed the “turned back” morphology. It can be concluded that the shape of the coronoid process of the mandible cannot be used as a morphological trait to determine whether a specimen belongs to a dog or as an argument in favour of chanco as the progenitor to dogs.
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Introduction
The domestication of wolves into dogs is an active topic of research (Boudadi-Maligne and Escarguel 2014; Germonpré et al. 2009; Larson et al. 2012; Morey and Jaeger 2015; Thalmann et al. 2013). Where, when and from which progenitor wolf sub-species dogs originated has been investigated both by osteoarchaeologists (Aaris-Sørensen 1977; Benecke 1987, 1994; Boudadi-Maligne and Escarguel 2014; Huxley 1880; Iljin 1941; Nehring 1888; Rütimeyer 1861; Stockhaus 1965; Studer 1901; Sumiński 1975) and geneticists (Anderson et al. 2009; Ardalan et al. 2011; Axelsson et al. 2013; Brown et al. 2011; Freedman et al. 2014; Gundry et al. 2007; Ho et al. 2005; Irion et al. 2003; Karlsson et al. 2007; Khosravi et al. 2013; Kirkness et al. 2003; Klütsch and de Caprona 2010; Larson and Burger 2013; Leonard et al. 2002; Lindblad-Toh et al. 2005; Ostrander and Wayne 2005; Pang et al. 2009; Savolainen et al. 2002, 2004; Schmutz and Berryere 2007; Schoenebeck and Ostrander 2013; Thalmann et al. 2013; Tsuda et al. 1997; Vaysse et al. 2011; Verginelli et al. 2005; Vila et al. 1999, 2005; Vilà et al. 1993, 1997; Vonholdt et al. 2010; Wayne 2012; Wayne and Ostrander 1999, 2007).
Briefly there are two current views. One group of researchers proposes an origin of dogs after the Last Glacial Maximum (LGM) in Europe and during the Magdalenian, about 18,000 years ago (Thalmann et al. 2013). This evidence is based on genetic research (Ho et al. 2005; Thalmann et al. 2013), and the morphology of canine archaeological remains that is distinctively smaller than those of wolves (Altuna et al. 1984; Boudadi-Maligne and Escarguel 2014; Boudadi-Maligne et al. 2012; Célérier 1994; Célérier et al. 1999; Chaix 2000; Larson and Burger 2013; Leesch et al. 2012; Morel and Müller 1997; Napierala and Uerpmann 2012; Pionnier-Capitan 2010; Pionnier-Capitan et al. 2011; Street 2002).
The other group claims that dogs originated before the LGM, as early as in the Aurignacian and Gravettian and thus 35,000 years ago (Bocherens et al. 2014; Germonpré et al. 2009, 2012; Ovodov et al. 2011; Sablin and Khlopachev 2002). Although genetic analysis has not found any relationship between these old archaeological canine specimens (Thalmann et al. 2013) purported to be domesticated wolves and modern dogs, these researchers suggest that these animals were, however, domesticated, but did not produce surviving offspring (aborted domestication waves) (Germonpré et al. 2012; Skoglund et al. 2011). The arguments to place these pre-LGM specimens in the dog clade are based on morphology alone and mainly on wider and shorter snouts. Drake et al. (2015) have, however, demonstrated that this criterion (shorter and wider snouts) is not useful in distinguishing dogs from wolves and also identified some of the so-called pre-LGM dog fossils as wolves.
Many morphological differences have been described between wolves and dogs in the literature since the eighteenth century (Clutton-Brock 1962; Degerbøl 1961; Nehring 1888; Stockhaus 1965; Studer 1901; Wolfgram 1894). Three morphological methods were used to examine morphological differences:
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The “obvious” visual difference in appearance (morphology, sensu stricto) (Olsen and Olsen 1977).
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The difference in size (morphometry) (Benecke 1987, 1994; Boudadi-Maligne and Escarguel 2014; Napierala and Uerpmann 2012).
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The difference in appearance (form) that cannot be recognized visually with certainty (geometric morphometrics) (e.g., Drake and Klingenberg 2010; Milenkovic et al. 2010; Pionnier-Capitan 2010; Schmitt and Wallace 2012).
The most frequently reported morphological and morphometric differences used to distinguish dogs from wolves are smaller stature and thus smaller anatomical parts (e.g., skull, teeth such as carnassials, etc.), shorter and wider snouts, tooth crowding, larger orbital angles and a “turned back” morphology of the dorsal side (apex) of the vertical ramus of the mandible (coronoid process) (Olsen and Olsen 1977, Fig. 1 and 2, p. 534–535). The latter morphological difference is based purely on difference in shape. This distinctive morphological characteristic was described in 1977 by Olsen and Olsen (Olsen and Olsen 1977). The authors state that the origin of Asian and American (New World) dogs must have originated in the Far East and proposed the Tibetan wolf (Chinese wolf, Asian wolf, Canis lupus chanco) as the dog’s ancestor (Olsen and Olsen 1977, 534). This opinion was based on the specific “turned back” morphology of the coronoid process of the mandible, claimed to be “specific to domestic dogs” and Chinese wolves, and to be “absent from other canids” (Olsen and Olsen 1977, 534). Based on this assumption, C. lupus chanco was said to be “the progenitor of dogs”, and this specific morphological trait is still used in recent publications to assign archaeological specimens to the dog clade (e.g., Ovodov et al. 2011).
We tested the statement of Olsen and Olsen (1977) by examining 384 dog mandibles of many breeds, of which six breeds are Asian or American, and 60 wolf mandibles of four sub-species. Our aim is to examine whether this “turned back” morphology is indeed present in “all” dogs and only in C. lupus chanco as hypothesized.
Materials and methods
All examined mandibles are from reputable museum collections. These had been collected in historical and recent periods and were professionally prepared. All are intact and from adult animals. In total 444 dog and wolf skulls were examined (888 mandibles) including 384 dog skulls and 60 wolf skulls. For the wolves (Table 1), 37 are from the collection of The George S. Wise Faculty of Life Sciences, Department of Zoology at Tel-Aviv University, Israel (ZMTAU). Thirty-two of these were Canis lupus pallipes and five Canis lupus arabs. Seven skulls were examined from the collection of the Natural History Museum in London, Great Britain (BMNH): six C. lupus arabs, and one C. lupus pallipes. Eleven skulls are from the collection of the Natural History Museum Bern, Switzerland (NMBE), all from Eurasian wolves (Canis lupus lupus) from Central Europe or Russia. Five specimens of C. lupus chanco from the collection of the Department of Vertebrate Zoology, Smithsonian Institution at the National Museum of Natural History, Washington DC, USA (USNM), were also examined.
We also examined 123 dog skulls from the collection of the anatomy department of the school for Veterinary Medicine, Ghent University, Belgium, and 261 skulls from the collection of The Museum of Natural History, Bern, Switzerland (total 384) (Table 2). The skulls belong to 72 different breeds, of which six breeds and 33 skulls are Asian or American. These are Alaskan malamute (5), Canadian Eskimo dog (4), Chow–Chow (16), Shar Pei (1), Tibetan Mastiff (6) and Tibetan Terrier (1).
Each mandible was digitally photographed from a distance of 40–50 cm with a digital Nikon D 700 camera with a 50 mm lens. The photographs were imported in the OsiriX Imaging Software program. A straight vertical line was then drawn confluent with the straight part of the ventral caudal border of the mandible. The mandibles were divided in two categories based on the morphology of the coronoid process and by drawing a straight line (green on the figures) coinciding with the caudal border. For Category 1, the mandible has a perfect vertical straight caudal border (Fig. 1) or the uppermost part of the apex points minimally in the caudal direction, while the caudal border is straight (Fig. 2). In this category, the straight green line follows the caudal bony border of the vertical ramus and the dorsal aspect of the mandible does not cross the green line or transects only a very small part at the tip. For Category 2, the caudal border is concave over its entire length and has the form of a dolphin fin (Fig. 3). Here, the vertical line transects most of the caudal vertical ramus and the line cannot coincide with the caudal border which is concave.
Results
All left and right mandibles from the same skull show identical anatomy; therefore, frequencies are per skull, not mandible. Fifty-two wolf skulls had a straight caudal border (87 %), while eight (13 %) had a “turned back” morphology (Table 3). Eurasian wolves and C. lupus arabs all had straight mandibles. C. lupus pallipes had four specimens with mandibles with the “turned back” morphology (12 %) (Fig. 4) and C. lupus chanco four out of five mandibles with “turned back” morphology (80 %) but one with straight morphology (20 %) (Fig. 5).
Of the 384 dog skulls, 312 had a straight caudal border (81 %) and 72 mandibles had “turned back” morphology (19 %). There was no relation between the “turned back” anatomy and breed; this was spread across 37 breeds (Table 3).
Three of seven Asian and American breeds (41 mandibles) had seven “tuned back” mandibles (17 %) so most mandibles in these breeds were straight (Fig. 6).
Discussion
Three main claims are made in Olsen and Olsen’s article (1977). The first is that the Chinese wolf is progenitor to Asian and New World dogs. When Olsen and Olsen’s article (1977) was published, it was still uncertain if only the wolf was a progenitor to dogs. In addition to the wolf, Canis aureus was said to be a possible forefather of small breed dogs (Darwin 1868; Lorenz 2002). It was also uncertain if there had been only one domestication wave, or if regional and different domestication phenomena had occurred and so for example local Asian wolves could then have been directly ancestral to Asian and New World dogs and Eurasian wolves to European dogs. The article should thus be viewed in this historical perspective. The fact that C. lupus chanco is called “the Chinese wolf” in the article, not Tibetan wolf (Pocock 1946), should also be placed in the same historical perspective as the 1970s were a period of a Sino-American rapprochement (Oksenberg 1982). Recent genetic analysis has confirmed that only wolves are progenitors to dogs, contradicting older theories about different geographic domestication waves (Duleba et al. 2015; Horard-Herbin et al. 2014; Larson et al. 2012; Thalmann et al. 2013) and has revealed that New World dogs did not originate locally but invaded the continent together with early migration waves of Homo sapiens (Leonard et al. 2002; Savolainen et al. 2002).
The original article shows drawings of 13 mandibles of which only ten have sufficient intact anatomy to make interpretation possible (according to personal re-examination of the published drawings by LJ). Of these, six belong to dogs, one to C. lupus chanco and three to species other than Canis lupus. All dogs and all C. lupus chanco specimens show the “turned back” anatomy. It is not reported if more than these seven mandibles were examined. If not, it is difficult to understand why such a general statement was published. C. lupus chanco skulls are very difficult to find in zoological and natural history collections. This may explain why only one was reported in the article. We found only eleven skulls in many worldwide collections. Of these only five had intact mandibular anatomy, of which one (20 %) had a straight caudal mandibular ramus, contradicting Olsen and Olsen’s (1977) original statement.
The second assertion is that the “tuned back” morphology is absent from other canids. This statement is unsupportable as we have demonstrated the presence of the “turned back” morphology in C. lupus pallipes mandibles. Studer (1901) early on reported that from all examined wolf skulls pallipes and chanco were the most anatomically similar. This may explain why these two wolf sub-species share this “turned back” morphology, unseen in the two other wolf sub-species we examined.
The third statement is that “dogs have the turned back morphology”. At one point in the article this statement is made in general: “all dogs” have the turned back morphology (Olsen and Olsen 1977, 534, last paragraph), while in another location it refers to “New World and Asian dogs” (Olsen and Olsen 1977, 533, fifth paragraph), while the title of the article refers only to New World dogs. The “turned back” morphology is present in the six dog mandible drawings in the article, but the same pattern was not observed in the large group of dog mandibles we examined, not in general and not in Asian or New World dogs. Indeed, only a minority of dogs (20 %) have “turned back” morphology. In addition there are no differences in occurrence between Asian and/or New World dogs nor in the total group of dogs (18 % in these breeds vs. 20 % in total).
Conclusion
The statement that all dogs have a specific “turned back” morphology of the mandibular coronoid process, and that they share this specific morphology with only one wolf sub-species (C. lupus chanco), is untenable. This morphological trait cannot therefore be used as an argument to claim that archaeological remains belong to dogs, nor to argue that C. lupus chanco is the progenitor of dogs.
References
Aaris-Sørensen K (1977) The subfossil wolf, Canis lupus L. in Denmark. Vidensk Meddr dabsk naturhistorisch Forensen 29:129–146
Altuna J, Baldeon A, Mariezkurrena K (1984) Dépôts rituels magdaléniens de la grotte d’Erralla (Pays Basque). Munibe 36:3–10
Anderson T, Candille S, Musiani M, Greco C, Stahler D, Smith D, Padhukasahasram B, Randi E, Leonard J, Bustamante C (2009) Molecular and evolutionary history of melanism in North American gray wolves. Science 323:1339–1343
Ardalan A, Kluetsch C, Zhang A, Erdogan M, Uhlén M, Houshmand M, Tepeli C, Ashtiani S, Savolainen P (2011) Comprehensive study of mtDNA among Southwest Asian dogs contradicts independent domestication of wolf, but implies dog–wolf hybridization. Ecol Evol 1:373–385
Axelsson E, Ratnakumar A, Arendt M, Maqbool K, Webster M, Perloski M, Liberg O, Arnemo J, Hedhammar Å, Lindblad-Toh K (2013) The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 495:360–364
Benecke N (1987) Studies on early dog remains from Northern Europe. J Archaeol Sci 14:31–49
Benecke N (1994) Archäozoologische Studien zur Entwicklung der Haustierhaltung vol 64. Akademie Verlag Schriften zur Ur- und Frühgeschichte, Berlin
Bocherens H, Drucker D, Germonpré M, Lázničková-Galetová M, Nait Y, Wissin C, Brůžek J, Oliva M (2014) Reconstruction of the Gravettian food-web at Předmostí I using multi-isotopic tracking of bone collagen. Quat Int 249:1–18
Boudadi-Maligne M, Escarguel G (2014) A biometric re-evaluation of recent claims for early upper palaeolithic wolf domestication in Eurasia. J Archaeol Sci 45:80–89
Boudadi-Maligne M, Mallye J-B, Langlais M, Barshay-Szmidt C (2012) Magdalenian dog remains from Le Morin rock-shelter (Gironde, France). Socio-economic implications of a zootechnical innovation. PALEO Revue d’archéologie préhistorique 23:39–54
Brown SK, Pedersen P, Niels C, Jafarishorije S, Bannasch D, Ahrens K, Wu J, Okon M, Sacks B (2011) Phylogenetic distinctiveness of middle eastern and southeast Asian village dog Y chromosomes illuminates dog origins. PLoS One 6:e28496
Célérier G (1994) L’abri sous roche de Pont d’Ambon à Bourdeilles (Dordogne). Gallia préhistoire 36:65
Célérier G, Tisnerat N, Valladas H (1999) Données nouvelles sur l’âge des vestiges de chien à Pont d’Ambon, Bourdeilles (Dordogne). Paleobiology 11:163–165
Chaix L (2000) A preboreal dog from the northern Alps (Savoie, France). BAR Int Ser 889:49–60
Clutton-Brock J (1962) Near eastern canids and the affinities of the Natufian dogs. Zeitschrift für Tierzüchtung und Züchtungsbiologie 76:326–333
Darwin C (1868) The variation of animals and plants under domestication, vol 2. John Murray, London
Degerbøl M (1961) On a find of a preboreal domestic dog Canis familiaris L. from Star Carr, Yorkshire, with remarks on other Mesolithic dogs. Proc Prehist Soc (New Ser) 27:35–55
Drake AG, Klingenberg CP (2010) Large-scale diversification of skull shape in domestic dogs: disparity and modularity. Am Nat 175:289–301. doi:10.1086/650372
Drake AG, Coquerelle M, Colombeau G (2015) 3D morphometric analysis of fossil canid skulls contradicts the suggested domestication of digs during the late palaeolithic. Sci Rep. doi:10.1038/srep08299
Duleba A, Skonieczna K, Bogdanowicz W, Malyarchuk B, Grzybowski T (2015) Complete mitochondrial genome database and standardized classification system for Canis lupus familiaris. Forensic Sci Int: Genet 19:123–129
Freedman AH, Gronau I, Schweizer R, Ortega-Del Vecchyo D, Han E, Sil P, Galaverni M, Ma P, Lorente-Galdos B (2014) Genome sequencing highlights the dynamic early history of dogs. PLoS Genet 10:e1004016
Germonpré M, Sablin MV, Stevens RE, Hedges RE, Hofreiter M, Stiller M, Després VR (2009) Fossil dogs and wolves from palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes. J Archaeol Sci 36:473–490
Germonpré M, Lázničková-Galetová M, Sablin MV (2012) Palaeolithic dog skulls at the Gravettian Předmostí site, the Czech Republic. J Archaeol Sci 39:184–202
Gundry RL, Allard MW, Moretti TR, Honeycutt RL, Wilson MR, Monson KL, Foran DR (2007) Mitochondrial DNA analysis of the domestic dog: control region variation within and among breeds. J Forensic Sci 52:562–572
Ho SY, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568
Horard-Herbin M-P, Tresset A, Vigne J-D (2014) Domestication and uses of the dog in western Europe from the paleolithic to the iron age. Anim Front 4:23–31
Huxley TH (1880) On the cranial and dental characters of the Canidæ. In: Proceedings of the zoological society of London. Wiley Online Library, 238–288
Iljin NA (1941) Wolf–dog genetics. J Genet 42:359–414
Irion D, Schaffer A, Famula T, Eggleston M, Hughes S, Pedersen N (2003) Analysis of genetic variation in 28 dog breed populations with 100 microsatellite markers. J Hered 94:81–87
Karlsson EK et al (2007) Efficient mapping of mendelian traits in dogs through genome-wide association. Nat Genet 39:1321–1328
Khosravi R, Rezaei HR, Kaboli M (2013) Detecting hybridization between Iranian wild wolf (Canis lupus pallipes) and free-ranging domestic dog (Canis familiaris) by analysis of microsatellite markers. Zoolog Sci 30:27–34
Kirkness EF, Baranowska I, Wade C, Hillbertz N, Zody M, Anderso N, Biagi T, Patterson N, Pielberg G, Kulbokas E (2003) The dog genome: survey sequencing and comparative analysis. Science 301:1898–1903
Klütsch CF, de Caprona MDC (2010) The IGF1 small dog haplotype is derived from middle eastern grey wolves: a closer look at statistics, sampling, and the alleged middle eastern origin of small dogs. BMC Biol 8:119
Larson G, Burger J (2013) A population genetics view of animal domestication. Trends Genet 29:197–205
Larson G et al (2012) Rethinking dog domestication by integrating genetics, archeology, and biogeography. PNAS 109:8878–8883
Leesch D, Müller W, Nielsen E, Bullinger J (2012) The Magdalenian in Switzerland: re-colonization of a newly accessible landscape. Quat Int 272:191–208
Leonard JA, Wayne RK, Wheeler J, Valadez R, Guillén S, Vila C (2002) Ancient DNA evidence for old world origin of new world dogs. Science 298:1613–1616
Lindblad-Toh K et al (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438:803–819
Lorenz K (2002) Man meets dog. Psychology Press, Taylor and Francis group, Routeledge, London, New York
Milenkovic M, Šipetic VJ, Blagojevic J, Tatovic S, Vujoševic M (2010) Skull variation in Dinaric–Balkan and Carpathian gray wolf populations revealed by geometric morphometric approaches. J Mammal 91:376–386
Morel P, Müller W (1997) Hauterives-Champréveyres, 11. Un campement magdalénien au bord du lac de Neuchâtel: étude archéozoologique (secteur 1). Archéologie neuchâteloise, 23. Neuchâtel
Morey D, Jaeger R (2015) Paleolithic dogs: why sustained domestication then? J Archaeol Sci: Rep 3:420–428
Napierala H, Uerpmann HP (2012) A ‘new’ palaeolithic dog from central Europe. Int J Osteoarchaeol 22:127–137
Nehring A (1888) Zur Abstammung der Hunde-Rassen. Zoologische Jahrbücher Abtheilung Systematik, Geographie und Biologie 3:51–58
Oksenberg M (1982) Reconsiderations: a decade of Sino-American relations. Foreign Aff 61:190
Olsen SJ, Olsen JW (1977) The Chinese wolf, ancestor of new world dogs. Science 197:533–535
Ostrander EA, Wayne RK (2005) The canine genome. Genome Res 15:1706–1716
Ovodov ND, Crockford SJ, Kuzmin YV, Higham TF, Hodgins GW, van der Plicht J (2011) A 33,000-year-old incipient dog from the Altai mountains of Siberia: evidence of the earliest domestication disrupted by the last glacial maximum. PLoS One 6:e22821
Pang JF, Kluetsch C, Zo X, Zhang A, Lue L, Angleby H, Ardalan A, Ekström C, Sköllerm A, Lundeber J (2009) mtDNA data indicate a single origin for dogs south of Yangtze river, less than 16,300 years ago, from numerous wolves. Mol Biol Evol 26:2849–2864
Pionnier-Capitan M (2010) La domestication du chien en Eurasie: étude de la diversité passée, approches ostéoarchéologiques, morphométriques et paléogénétiques. PhD thesis, l’Université de Lyon
Pionnier-Capitan M, Bemilli C, Bodu P, Célérier G, Ferrié J, Fosse P, Garcià M, Vigne JD (2011) New evidence for upper palaeolithic small domestic dogs in South-Western Europe. J Archaeol Sci 38:2123–2140
Pocock R (1946) External and cranial characters of some rare Asiatic mammals recently exhibited by the society. Proc. Zoolog. Soc. Lond 3:310–318
Rütimeyer L (1861) Die Fauna der Pfahlbauten der Schweiz. Geschichte der Wilden und der Haus-Saugetiere. Neue Denkschrift der Algemeinne Schweizerische Geselschaft der ges. Naturwissenschaft, 19, Basel, Switzerland
Sablin M, Khlopachev G (2002) The earliest ice age dogs: evidence from Eliseevichi 11. Curr Anthropol 43:795–799
Savolainen P, Y-p Zhang, Luo J, Lundeberg J, Leitner T (2002) Genetic evidence for an East Asian origin of domestic dogs. Science 298:1610–1613
Savolainen P, Leitner T, Wilton AN, Matisoo-Smith E, Lundeberg J (2004) A detailed picture of the origin of the Australian dingo, obtained from the study of mitochondrial DNA. PNAS 101:12387–12390
Schmitt E, Wallace S (2012) Shape change and variation in the cranial morphology of wild canids (Canis lupus, Canis latrans, Canis rufus) compared to domestic dogs (Canis familiaris) using geometric morphometrics International. J Osteoarchaeol 24:42–50
Schmutz S, Berryere T (2007) Genes affecting coat colour and pattern in domestic dogs: a review. Anim Genet 38:539–549
Schoenebeck JJ, Ostrander EA (2013) The genetics of canine skull shape variation. Genetics 193:317–325
Skoglund P, Götherström A, Jakobsson M (2011) Estimation of population divergence times from non-overlapping genomic sequences: examples from dogs and wolves. Mol Biol Evol 28:1505–1517
Stockhaus K (1965) Metrische Untersuchungen an Schädeln von Wölfen und Hunden. J Zoolog Syst Evol Res 3:157–258
Street M (2002) Ein wiedersehen mit dem hund von Bonn-Oberkassel. Bonner Zoologische Beitrage 50:269–290
Studer T (1901) Die prähistorischen Hunde in ihrer Beziehung zu den gegenwärtig lebenden Rassen. Zurcher und Furrer, Zurich
Sumiński P (1975) Morphologische Unterscheidungsmerkmale zwischen Wolfs-(Canis lupus L.) und Hundeschädel (Canis familiaris L.). Zeitschrift für Jagdwissenschaft 21:227–232
Thalmann O, Shapiro B, Cui P, Schuenemann VJ, Sawyer SK, Greenfield DL, Germonpré MB, Sablin MV, López-Girálde F, Domingo-Roura X (2013) Complete mitochondrial genomes of ancient canids suggest a European origin of domestic dogs. Science 342:871–874
Tsuda K, Kikkawa Y, Yonekawa H, Tanabe Y (1997) Extensive interbreeding occurred among multiple matriarchal ancestors during the domestication of dogs: evidence from inter-and intra-species polymorphisms in the D-loop region of mitochondrial DNA between dogs and wolves. Genes Genet Syst 72:229–238
Vaysse A, Ratnakumar A, Derrien T, Axelsson E, Pielberg G, Sigurdsson S, Fall T, Seppälä E, Hansen M, Lawley C (2011) Identification of genomic regions associated with phenotypic variation between dog breeds using selection mapping. PLoS Genet 7:e1002316
Verginelli F, Capelli C, Coia V, Musiani M, Falchetti M, Ottini L, Palmirotta R, Tagliacozzo A, Mazzorin I, Mariani-Costantin R (2005) Mitochondrial DNA from prehistoric canids highlights relationships between dogs and South-East European wolves. Mol Biol Evol 22:2541–2551
Vila C, Maldonado JE, Wayne RK (1999) Phylogenetic relationships, evolution, and genetic diversity of the domestic dog. J Hered 90:71–77
Vila C, Seddon J, Ellegren H (2005) Genes of domestic mammals augmented by backcrossing with wild ancestors. Trends Genet 21:214–218
Vilà C, Urios V, Castroviejo J (1993) Tooth losses and anomalies in the wolf (Canis lupus). Can J Zool 71:968–971
Vilà C, Savolainen P, Maldonado J, Amorim I, Rice J, Honeycutt R, Crandall K, Lundeberg J, Wayne R (1997) Multiple and ancient origins of the domestic dog. Science 276:1687–1689
Vonholdt B, Pollinger J, Lohmueller K, Han E, Parker H, Quignon P, Degenhardt J, Boyko A, Earl D, Auton A, Reynolds A (2010) Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464:898–902
Wayne RK (2012) Evolutionary genomics of dog domestication. Mamm Genome 23:3–18
Wayne RK, Ostrander EA (1999) Origin, genetic diversity, and genome structure of the domestic dog. BioEssays 21:247–257
Wayne RK, Ostrander EA (2007) Lessons learned from the dog genome. Trends Genet 23:557–567
Wolfgram A (1894) Die Einwerkung der Gefangenschaft auf die Gestaltung des Wolfschädels. Zoologisches Jahrbuch (Abteilung fur Systematik) 7:773–822
Acknowledgments
We would like to thank Shai Meiri and Daniel Berkowic from Israel, Roberto Portela Miguez from the Natural History Museum in London, Paul Schmid and Marc Nussbaumer from Switzerland and Paul Simoens from Belgium for allowing us to use their collections for research. We thank Kristen Quarles from the Smithsonian institution for assistance with their collection and thank Thijs Van Kolfschoten for critical comments. David Jaggar is thanked for linguistic help. We are grateful to the anonymous reviewers of the article for improvements. Finally Christien De Paepe is thanked for assistance with the graphics.
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Communicated by A. Schmidt-Rhaesa.
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Janssens, L., Miller, R. & Van Dongen, S. The morphology of the mandibular coronoid process does not indicate that Canis lupus chanco is the progenitor to dogs. Zoomorphology 135, 269–277 (2016). https://doi.org/10.1007/s00435-015-0298-z
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DOI: https://doi.org/10.1007/s00435-015-0298-z