Advertisement

Zoomorphology

, Volume 135, Issue 2, pp 269–277 | Cite as

The morphology of the mandibular coronoid process does not indicate that Canis lupus chanco is the progenitor to dogs

  • Luc Janssens
  • Rebecca Miller
  • Stefan Van Dongen
Open Access
Original Paper
  • 1.2k Downloads

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.

Keywords

Dog Wolf Domestication Morphology Canis lupus chanco Mandible Coronoid process 

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:
  • The “obvious” visual difference in appearance (morphology, sensu stricto) (Olsen and Olsen 1977).

  • The difference in size (morphometry) (Benecke 1987, 1994; Boudadi-Maligne and Escarguel 2014; Napierala and Uerpmann 2012).

  • 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).
Fig. 1

Category 1: Straight caudal border of the vertical ramus. The vertical line that coincides with the ventral part of the caudal border of the vertical ramus of the mandible does not cut through the dorsal caudal ramus

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.
Table 1

List of wolf skulls used in this study

Museum ID

Genus

Species

Sub-species

Region

BMNH ZD.1891.2.5.1

Canis

lupus

arabs

Bouraida

BMNH ZD.1895.10.8.1

Canis

lupus

arabs

Aden

BMNH ZD.1899.11.6.36

Canis

lupus

arabs

Muscat

BMNH ZD.1924.8.13.1

Canis

lupus

arabs

Jeddah

BMNH ZD.1940.193

Canis

lupus

pallipes

?

BMNH ZD.1948.368

Canis

lupus

pallipes

?

BMNH ZD.1897.1.14.4

Canis

lupus

arabs

Jaquakar

NMBE1028185

Canis

lupus

lupus

Russia

NMBE1028188

Canis

lupus

lupus

Russia

NMBE1028189

Canis

lupus

lupus

Russia

NMBE1028192

Canis

lupus

lupus

Poland

NMBE1028193

Canis

lupus

lupus

Russia

NMBE1028204

Canis

lupus

lupus

Poland

NMBE1028205

Canis

lupus

lupus

Poland

NMBE1028206

Canis

lupus

lupus

Poland

NMBE1028207

Canis

lupus

lupus

Poland

NMBE1028209

Canis

lupus

lupus

Poland

NMBE1028211

Canis

lupus

lupus

Russia

USNM00607

Canis

lupus

chanco

China

USNM00610

Canis

lupus

chanco

China

USNM00613

Canis

lupus

chanco

China

USNM00616

Canis

lupus

chanco

China

USNM00619

Canis

lupus

chanco

China

ZMTAU 09439

Canis

lupus

pallipes

Golan

ZMTAU 09460

Canis

lupus

arabs

Sandiya

ZMTAU 10334

Canis

lupus

pallipes

Galilei

ZMTAU 10338

Canis

lupus

pallipes

Galilei

ZMTAU 10355

Canis

lupus

pallipes

Golan

ZMTAU 10402

Canis

lupus

pallipes

Golan

ZMTAU 10608

Canis

lupus

pallipes

Galilei

ZMTAU 10609

Canis

lupus

pallipes

Golan

ZMTAU 10610

Canis

lupus

pallipes

Golan

ZMTAU 10615

Canis

lupus

pallipes

Golan

ZMTAU 10619

Canis

lupus

pallipes

Golan

ZMTAU 10621

Canis

lupus

pallipes

Golan

ZMTAU 10682

Canis

lupus

pallipes

Golan

ZMTAU 10685

Canis

lupus

pallipes

Golan

ZMTAU 10686

Canis

lupus

pallipes

Golan

ZMTAU 10688

Canis

lupus

pallipes

Golan

ZMTAU 10692

Canis

lupus

pallipes

Golan

ZMTAU 11041

Canis

lupus

pallipes

Galilei

ZMTAU 11109

Canis

lupus

pallipes

Galilei

ZMTAU 11110

Canis

lupus

pallipes

Golan

ZMTAU 11118

Canis

lupus

pallipes

Galilei

ZMTAU 11119

Canis

lupus

pallipes

Golan

ZMTAU 11121

Canis

lupus

pallipes

Golan

ZMTAU 11250

Canis

lupus

pallipes

Galilei

ZMTAU 11275

Canis

lupus

pallipes

Galilei

ZMTAU 11417

Canis

lupus

pallipes

Galilei

ZMTAU 11418

Canis

lupus

pallipes

Golan

ZMTAU 11475

Canis

lupus

arabs

Negev

ZMTAU 11476

Canis

lupus

pallipes

Golan

ZMTAU 11479

Canis

lupus

pallipes

Galilei

ZMTAU 11516

Canis

lupus

pallipes

Golan

ZMTAU 11685

Canis

lupus

pallipes

Golan

ZMTAU 12130

Canis

lupus

pallipes

Galilei

ZMTAU 12130-2

Canis

lupus

arabs

Negev

ZMTAU 12251

Canis

lupus

arabs

Negev

ZMTAU 12254

Canis

lupus

arabs

Muscat

ZMTAU 12279

Canis

lupus

arabs

Negev

Sub-species, institute and accession numbers (ID) are reported. BMNH: British Museum of Natural History. NMBE: Natural History Museum Bern, Switzerland, USNM: Department of Vertebrate Zoology, Smithsonian Institution at the National Museum of Natural History, Washington DC, USA, ZMTAU: Department of Zoology at Tel-Aviv University, Israel

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).
Table 2

Dog skulls used in this study grouped alphabetically by breed

Breed

Nr

TB

Breed

Nr

TB

Afghan hound

13

2

Greyhound

10

1

Airedale terrier

4

1

Groenendael Belgian shepherd

18

1

Akita Inu

8

1

Hahoawu

1

 

Alaskan Malamute

5

2

Irish setter

2

 

Barzoi

11

2

Irish wolfhound

8

2

Basenji

1

 

Jagdterrier

2

 

Batak hound

11

3

Karelian Bear dog

18

3

Beagle

9

2

Kuvasc

1

 

Bearded collie

1

 

Labrador retriever

13

2

Berger de Brie

1

 

Leonberger

1

 

Berner Sennenhund

32

4

Lundehund

2

 

Bloodhound

7

1

Malinois Belgian shepherd

2

1

Border collie

5

3

Mastino Napolitano

1

 

Bouvier des Flandres

4

2

Mayar Agar

2

1

Boxer

2

 

Pariah hound

10

2

Bull terrier

1

 

Pembroke Welsh Corgi

1

 

Canaan dog

1

 

Pharaoh hound

4

 

Canadian Eskimo dog

4

 

Pointer

1

1

Chow Chow

16

3

Poodle

6

2

Cocker spaniel

4

 

Rhodesian Ridgeback

2

2

Crossbred

5

3

Rottweiler

3

 

Dalmatian

1

 

Saint Bernhard

2

 

Dingo

3

2

Saluki

2

 

Doberman pinscher

15

5

Samojeed

8

2

Entelbucher

1

 

Scottish collie

1

 

Finnish spitz

3

1

Scottish terrier

16

 

Flatcoat retriever

1

 

Shar Pei

1

 

Fox terrier

1

 

Siberian Husky

14

3

Gaint schnauzer

1

 

Sloughi

1

 

Galgo Espanjol

2

 

Swiss shepherd

1

 

German braque

3

1

Tervueren Belgian shepherd

5

 

German shepherd

10

3

Tibetan Mastiff

6

1

Golden retriever

6

1

Tibetan spaniel

1

 

Great Dane

2

 

Weimaraner

1

 

Great spitz

7

2

Whippet

4

2

Greenland dog

10

1

Wolfspitz

2

1

Total breeds

72

 

Total skulls

384

 

In bold are New World and Asian breeds. Nr refers to the number of skulls examined. TB refers to “Turned Back” morphology

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.
Fig. 2

Category 2: Straight caudal border with minimal tip curvature. The vertical line that coincides with the ventral part of the caudal border of the vertical ramus of the mandible coincides with the caudal border and does only cut through the tip of dorsal caudal ramus

Fig. 3

Turned back morphology. The vertical line at the caudal border of the vertical ramus of the mandible does not coincide with the border and cuts through a large part of the dorsal ramus

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).
Table 3

Morphological categories of the coronoid process of the mandible

 

Dogs

Canis lupus

Canis lupus

Canis lupus

Canis lupus

Wolves

pallipes

arabs

chanco

Eurasian

Total

Total number

384

37

7

5

11

60

Category 1: straight morphology

81 % (312)

88 % (33)

100 % (7)

20 % (1)

100 % (11)

52

Category 2: “Turned back” morphology

19 % (72)

12 % (4)

 

80 % (4)

 

8

Fig. 4

A Canis lupus pallipes mandibular specimen with “turned back” morphology. Accession number ZMTAU1110 (George Wise faculty of Life Sciences, Israel)

Fig. 5

The Canis lupus chanco mandibular specimen without the “turned back” morphology. Accession number 18B458- NHB 2015- USNM00610 (Smithsonian Institution, USA). Photo: D. E. Hurlbert

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).
Fig. 6

A mandibular specimen of an Asian/American dog without the “turned back” morphology. Top Alaskan Malamute specimen. Accession number 1051378-313/78 (Museum of Natural History, Bern, Switzerland). Bottom Akita Inu specimen. Accession number 1051382-523/82 (Museum of Natural History, Bern, Switzerland)

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.

Notes

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.

References

  1. Aaris-Sørensen K (1977) The subfossil wolf, Canis lupus L. in Denmark. Vidensk Meddr dabsk naturhistorisch Forensen 29:129–146Google Scholar
  2. Altuna J, Baldeon A, Mariezkurrena K (1984) Dépôts rituels magdaléniens de la grotte d’Erralla (Pays Basque). Munibe 36:3–10Google Scholar
  3. 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 323:1339–1343CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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 1:373–385CrossRefPubMedPubMedCentralGoogle Scholar
  5. 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 495:360–364CrossRefPubMedGoogle Scholar
  6. Benecke N (1987) Studies on early dog remains from Northern Europe. J Archaeol Sci 14:31–49CrossRefGoogle Scholar
  7. Benecke N (1994) Archäozoologische Studien zur Entwicklung der Haustierhaltung vol 64. Akademie Verlag Schriften zur Ur- und Frühgeschichte, BerlinGoogle Scholar
  8. 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 249:1–18Google Scholar
  9. Boudadi-Maligne M, Escarguel G (2014) A biometric re-evaluation of recent claims for early upper palaeolithic wolf domestication in Eurasia. J Archaeol Sci 45:80–89CrossRefGoogle Scholar
  10. 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 23:39–54Google Scholar
  11. 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:e28496CrossRefPubMedPubMedCentralGoogle Scholar
  12. Célérier G (1994) L’abri sous roche de Pont d’Ambon à Bourdeilles (Dordogne). Gallia préhistoire 36:65CrossRefGoogle Scholar
  13. Célérier G, Tisnerat N, Valladas H (1999) Données nouvelles sur l’âge des vestiges de chien à Pont d’Ambon, Bourdeilles (Dordogne). Paleobiology 11:163–165Google Scholar
  14. Chaix L (2000) A preboreal dog from the northern Alps (Savoie, France). BAR Int Ser 889:49–60Google Scholar
  15. Clutton-Brock J (1962) Near eastern canids and the affinities of the Natufian dogs. Zeitschrift für Tierzüchtung und Züchtungsbiologie 76:326–333Google Scholar
  16. Darwin C (1868) The variation of animals and plants under domestication, vol 2. John Murray, LondonGoogle Scholar
  17. 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) 27:35–55CrossRefGoogle Scholar
  18. 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 CrossRefPubMedGoogle Scholar
  19. 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 Google Scholar
  20. 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 19:123–129CrossRefGoogle Scholar
  21. 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:e1004016CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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 36:473–490CrossRefGoogle Scholar
  23. Germonpré M, Lázničková-Galetová M, Sablin MV (2012) Palaeolithic dog skulls at the Gravettian Předmostí site, the Czech Republic. J Archaeol Sci 39:184–202CrossRefGoogle Scholar
  24. 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 52:562–572CrossRefPubMedGoogle Scholar
  25. 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 22:1561–1568CrossRefPubMedGoogle Scholar
  26. 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 4:23–31CrossRefGoogle Scholar
  27. Huxley TH (1880) On the cranial and dental characters of the Canidæ. In: Proceedings of the zoological society of London. Wiley Online Library, 238–288Google Scholar
  28. Iljin NA (1941) Wolf–dog genetics. J Genet 42:359–414CrossRefGoogle Scholar
  29. 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 94:81–87CrossRefPubMedGoogle Scholar
  30. Karlsson EK et al (2007) Efficient mapping of mendelian traits in dogs through genome-wide association. Nat Genet 39:1321–1328CrossRefPubMedGoogle Scholar
  31. 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 30:27–34CrossRefPubMedGoogle Scholar
  32. 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 301:1898–1903CrossRefPubMedGoogle Scholar
  33. 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 8:119CrossRefPubMedPubMedCentralGoogle Scholar
  34. Larson G, Burger J (2013) A population genetics view of animal domestication. Trends Genet 29:197–205CrossRefPubMedGoogle Scholar
  35. Larson G et al (2012) Rethinking dog domestication by integrating genetics, archeology, and biogeography. PNAS 109:8878–8883CrossRefPubMedPubMedCentralGoogle Scholar
  36. Leesch D, Müller W, Nielsen E, Bullinger J (2012) The Magdalenian in Switzerland: re-colonization of a newly accessible landscape. Quat Int 272:191–208CrossRefGoogle Scholar
  37. 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 298:1613–1616CrossRefPubMedGoogle Scholar
  38. Lindblad-Toh K et al (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438:803–819CrossRefPubMedGoogle Scholar
  39. Lorenz K (2002) Man meets dog. Psychology Press, Taylor and Francis group, Routeledge, London, New YorkGoogle Scholar
  40. 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 91:376–386CrossRefGoogle Scholar
  41. Morel P, Müller W (1997) Hauterives-Champréveyres, 11. Un campement magdalénien au bord du lac de Neuchâtel: étude archéozoologique (secteur 1). Archéologie neuchâteloise, 23. NeuchâtelGoogle Scholar
  42. Morey D, Jaeger R (2015) Paleolithic dogs: why sustained domestication then? J Archaeol Sci: Rep 3:420–428Google Scholar
  43. Napierala H, Uerpmann HP (2012) A ‘new’ palaeolithic dog from central Europe. Int J Osteoarchaeol 22:127–137CrossRefGoogle Scholar
  44. Nehring A (1888) Zur Abstammung der Hunde-Rassen. Zoologische Jahrbücher Abtheilung Systematik, Geographie und Biologie 3:51–58Google Scholar
  45. Oksenberg M (1982) Reconsiderations: a decade of Sino-American relations. Foreign Aff 61:190CrossRefGoogle Scholar
  46. Olsen SJ, Olsen JW (1977) The Chinese wolf, ancestor of new world dogs. Science 197:533–535CrossRefPubMedGoogle Scholar
  47. Ostrander EA, Wayne RK (2005) The canine genome. Genome Res 15:1706–1716CrossRefPubMedGoogle Scholar
  48. 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:e22821CrossRefPubMedPubMedCentralGoogle Scholar
  49. 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 26:2849–2864CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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 LyonGoogle Scholar
  51. 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 38:2123–2140CrossRefGoogle Scholar
  52. Pocock R (1946) External and cranial characters of some rare Asiatic mammals recently exhibited by the society. Proc. Zoolog. Soc. Lond 3:310–318Google Scholar
  53. 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, SwitzerlandGoogle Scholar
  54. Sablin M, Khlopachev G (2002) The earliest ice age dogs: evidence from Eliseevichi 11. Curr Anthropol 43:795–799CrossRefGoogle Scholar
  55. Savolainen P, Y-p Zhang, Luo J, Lundeberg J, Leitner T (2002) Genetic evidence for an East Asian origin of domestic dogs. Science 298:1610–1613CrossRefPubMedGoogle Scholar
  56. 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 101:12387–12390CrossRefPubMedPubMedCentralGoogle Scholar
  57. 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 24:42–50CrossRefGoogle Scholar
  58. Schmutz S, Berryere T (2007) Genes affecting coat colour and pattern in domestic dogs: a review. Anim Genet 38:539–549CrossRefPubMedGoogle Scholar
  59. Schoenebeck JJ, Ostrander EA (2013) The genetics of canine skull shape variation. Genetics 193:317–325CrossRefPubMedPubMedCentralGoogle Scholar
  60. 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 28:1505–1517CrossRefPubMedGoogle Scholar
  61. Stockhaus K (1965) Metrische Untersuchungen an Schädeln von Wölfen und Hunden. J Zoolog Syst Evol Res 3:157–258CrossRefGoogle Scholar
  62. Street M (2002) Ein wiedersehen mit dem hund von Bonn-Oberkassel. Bonner Zoologische Beitrage 50:269–290Google Scholar
  63. Studer T (1901) Die prähistorischen Hunde in ihrer Beziehung zu den gegenwärtig lebenden Rassen. Zurcher und Furrer, ZurichGoogle Scholar
  64. Sumiński P (1975) Morphologische Unterscheidungsmerkmale zwischen Wolfs-(Canis lupus L.) und Hundeschädel (Canis familiaris L.). Zeitschrift für Jagdwissenschaft 21:227–232Google Scholar
  65. 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 342:871–874CrossRefPubMedGoogle Scholar
  66. 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 72:229–238CrossRefPubMedGoogle Scholar
  67. 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:e1002316CrossRefPubMedPubMedCentralGoogle Scholar
  68. 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 22:2541–2551CrossRefPubMedGoogle Scholar
  69. Vila C, Maldonado JE, Wayne RK (1999) Phylogenetic relationships, evolution, and genetic diversity of the domestic dog. J Hered 90:71–77CrossRefPubMedGoogle Scholar
  70. Vila C, Seddon J, Ellegren H (2005) Genes of domestic mammals augmented by backcrossing with wild ancestors. Trends Genet 21:214–218CrossRefPubMedGoogle Scholar
  71. Vilà C, Urios V, Castroviejo J (1993) Tooth losses and anomalies in the wolf (Canis lupus). Can J Zool 71:968–971CrossRefGoogle Scholar
  72. 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 276:1687–1689CrossRefPubMedGoogle Scholar
  73. 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 464:898–902CrossRefPubMedPubMedCentralGoogle Scholar
  74. Wayne RK (2012) Evolutionary genomics of dog domestication. Mamm Genome 23:3–18CrossRefPubMedGoogle Scholar
  75. Wayne RK, Ostrander EA (1999) Origin, genetic diversity, and genome structure of the domestic dog. BioEssays 21:247–257CrossRefPubMedGoogle Scholar
  76. Wayne RK, Ostrander EA (2007) Lessons learned from the dog genome. Trends Genet 23:557–567CrossRefPubMedGoogle Scholar
  77. Wolfgram A (1894) Die Einwerkung der Gefangenschaft auf die Gestaltung des Wolfschädels. Zoologisches Jahrbuch (Abteilung fur Systematik) 7:773–822Google Scholar

Copyright information

© The Author(s) 2016

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Department of ArchaeologyLeiden UniversityLeidenThe Netherlands
  2. 2.Service of PrehistoryUniversity of LiègeLiègeBelgium
  3. 3.Department of Evolutionary EcologyUniversity of AntwerpAntwerpBelgium

Personalised recommendations