The palaeogenetics of cat dispersal in the ancient world

Ottoni, C. et al. (2017) The palaeogenetics of cat dispersal in the ancient world. Nat. Ecol. Evol. 1, 0139.

The cat has long been important to human societies as a pest-control agent, object of symbolic value and companion animal, but little is known about its domestication process and early anthropogenic dispersal. Here we show, using ancient DNA analysis of geographically and temporally widespread archaeological cat remains, that both the Near Eastern and Egyptian populations of Felis silvestris lybica contributed to the gene pool of the domestic cat at different historical times. While the cat’s worldwide conquest began during the Neolithic period in the Near East, its dispersal gained momentum during the Classical period, when the Egyptian cat successfully spread throughout the Old World. The expansion patterns and ranges suggest dispersal along human maritime and terrestrial routes of trade and connectivity. A coat-colour variant was found at high frequency only after the Middle Ages, suggesting that directed breeding of cats occurred later than with most other domesticated animals.

Dual origin for domestic dog

Frantz, L.A. F., V. E. Mullin, M. Pionnier-Capitan, O. Lebrasseur, M. Ollivier, A. Perri, A. Linderholm, V. Mattiangeli, M. D. Teasdale, E. A. Dimopoulos, A. Tresset, M. Duffraisse, F. McCormick, L. Bartosiewicz, E. Gál, E. A. Nyerges, M. V. Sablin, S. Bréhard, M. Mashkour, A. Bălăşescu,B. Gillet, S. Hughes, O. Chassaing, C. Hitte, J.-D. Vigne, K. Dobney, C. Hänni, D. G. Bradley, & G. Larson. 2016. Genomic and archaeological evidence suggest a dual origin of domestic dogs. Science, 352 (6290) 1228-1231

The geographic and temporal origins of dogs remain controversial. We generated genetic sequences from 59 ancient dogs and a complete (28x) genome of a late Neolithic dog (dated to ~4800 calendar years before the present) from Ireland. Our analyses revealed a deep split separating modern East Asian and Western Eurasian dogs. Surprisingly, the date of this . divergence (~14,000 to 6400 years ago) occurs commensurate with, or several millennia after, the first appearance of dogs in Europe and East Asia. Additional analyses of ancient and modern mitochondrial DNA revealed a sharp discontinuity in haplotype frequencies in Europe. Combined, these results suggest that dogs may have been domesticated independently in Eastern and Western Eurasia from distinct wolf populations. East Eurasian dogs were then possibly transported to Europe with people, where they partially replaced European Paleolithic dogs.

Ancient DNA supports lineage replacement in European dog gene pool

Deguilloux, M. F., Moquel, J., Pemonge, M. H., & Colombeau, G. (2009). Ancient DNA supports lineage replacement in European dog gene pool: insight into Neolithic southeast France. Journal of Archaeological Science, 36(2), 513-519.

We report palaeogenetic analysis of domesticated dog (Canis familiaris) remains excavated from three archaeological sites from southeast France and dating from Middle Neolithic. Ancient DNA analysis was attempted on teeth and bone samples taken from 11 dogs. Three 266-base-pair fragments of the mitochondrial genome Hypervariable Region I (HVR-I) could be retrieved and revealed two haplotypes belonging to HVR-I lineage C. These three sequences were compared to the sequences of Swedish and Italian Neolithic dogs and permitted to confirm that clade C was largely represented all over Western Europe during this period. One haplotype defined in Neolithic French dog was observed for the first time in Canis mtDNA, underlining the loss of mitochondrial diversity in Europe since the Neolithic. Finally, these results point out mitochondrial lineage replacement in Europe, since lineage C represents only 5% of extant European dogs. Altogether, these results support the proposition that palaeogenetic studies are essential for the reconstruction of the past demographic history and the domestication process of dogs. 

A review of dog domestication from the Paleolithic to the Iron Age

Horard-Herbin, M-P., A. Tresset & J-D.Vigne. 2014. Domestication and uses of the dog in western Europe from the Paleolithic to the Iron Age. Animal Frontiers, 4 (3) 23-31 doi: 10.2527/af.2014-0018 

This paper reviews the knowledge of the history of the dog in western Europe acquired through archaeozoology.

The first part examines the question of domestication of the wolf during the Upper Paleolithic, by highlighting the sometimes contradictory archeological and genetic findings. It also briefly lays out the different controversies regarding the site or sites of domestication of the dog in the world and the presumed dates of this major phenomenon in human history.

The second part deals with the evolution of canine morphology from the Paleolithic to the Iron Age, integrating, for example, the latest discoveries regarding domestic coat colors in the Mesolithic.

Finally, the presumed and attested uses of dogs throughout European pre- and protohistory are presented, including certain practices that lasted over time.

Two studies on Paleolithic dogs and a controversy

Germonpré, M., Sablin, M. V., Stevens, R. E., Hedges, R. E., Hofreiter, M., Stiller, M., & Després, V. R. (2009). Fossil dogs and wolves from Palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes. Journal of Archaeological Science, 36(2), 473-490.

Using multivariate techniques, several skulls of fossil large canids from sites in Belgium, Ukraine and Russia were examined to look for possible evidence of the presence of Palaeolithic dogs. Reference groups constituted of prehistoric dogs, and recent wolves and dogs. The fossil large canid from Goyet (Belgium), dated at c. 31,700 BP is clearly different from the recent wolves, resembling most closely the prehistoric dogs. Thus it is identified as a Palaeolithic dog, suggesting that dog domestication had already started during the Aurignacian. The Epigravettian Mezin 5490 (Ukraine) and Mezhirich (Ukraine) skulls are also identified as being Palaeolithic dogs. Selected Belgian specimens were analyzed for mtDNA and stable isotopes. All fossil samples yielded unique DNA sequences, indicating that the ancient Belgian large canids carried a substantial amount of genetic diversity. Furthermore, there is little evidence for phylogeographic structure in the Pleistocene large canids, as they do not form a homogenous genetic group. Although considerable variation occurs in the fossil canid isotope signatures between sites, the Belgian fossil large canids preyed in general on horse and large bovids.

Dorsal view of the skulls from (a) Goyet (dog); (b) Trou Balleux (wolf); (c) Trou des Nutons (wolf),
showing the relative wide braincase of the Goyet dog 

Germonpré, M., Lázničková-Galetová, M., & Sablin, M. V. (2012). Palaeolithic dog skulls at the Gravettian Předmostí site, the Czech Republic. Journal of Archaeological Science, 39(1), 184-202.

Whether or not the wolf was domesticated during the early Upper Palaeolithic remains a controversial issue. We carried out detailed analyses of the skull material from the Gravettian Předmostí site, Czech Republic, to investigate the issue. Three complete skulls from Předmostí were identified as Palaeolithic dogs, characterized by short skull lengths, short snouts, and wide palates and braincases relative to wolves. One complete skull could be assigned to the group of Pleistocene wolves. Three other skulls could not be assigned to a reference group; these might be remains from hybrids or captive wolves. Modifications by humans of the skull and canine remains from the large canids of Předmostí indicate a specific relationship between humans and large canids.

Highlights

► Accepting an Aurignacian beginning of the domestication of the wolf is controversial. ►The Gravettian canid skulls from Předmostí were studied to check for the presence of dogs. ►Ancient dogs are characterized by short skulls and snouts, and wide palates and braincases. ►Using these criteria three Předmostí skulls were singled out as Gravettian dogs. ►Human modifications of the skulls hint at a specific human/large canid relationship.

Susan J. Crockford, S.J. & Y.V. KuzminComments on Germonpré et al., Journal of Archaeological Science 36, 2009 “Fossil dogs and wolves from Palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes”, and Germonpré, Lázkičková-Galetová, and Sablin, Journal of Archaeological Science 39, 2012 “Palaeolithic dog skulls at the Gravettian Předmostí site, the Czech Republic” Journal of Archaeological Science, 39(8):2797–2801. DOI: 10.1016/j.jas.2012.04.033

Issues related to the identification of Late Pleistocene dogs from different sites in Eurasia, triggered by recent publications (see Germonpré et al., 2009, 2012; Ovodov et al., 2011), are discussed. The main focus is the problem of how to distinguish wolves from early dogs on the basis of skull and teeth morphology. The studies by 18 and 19, reporting so-called ‘Palaeolithic dogs’ from Předmostí, Goyet, and other sites in Eastern and Central Europe, have some serious deficiencies. In our opinion, more work needs to be done to understand the biological mechanisms involved in wolf domestication and until then, it is premature to classify these Palaeolithic canids as fully domesticated dogs or even incipient dogs.

Highlights


► We discuss issues related to so-called ‘Palaeolithic dogs’ from sites in Eurasia. ► Our comments pertain to studies described in 18 and 19. ► We suggest it is premature to classify these Palaeolithic canids as fully domesticated dogs.

Germonpré, M., Sablin, M. V., Després, V., Hofreiter, M., Lázničková-Galetová, M., Stevens, R. E., & Stiller, M. (2013). Palaeolithic dogs and the early domestication of the wolf: a reply to the comments of Crockford and Kuzmin (2012). Journal of Archaeological Science, 40(1), 786-792.

This is a response to the comments of Crockford and Kuzmin (2012) on our identification of Palaeolithic dogs from different European Palaeolithic sites. In their comments Crockford and Kuzmin (2012) present some errors, misunderstandings and misrepresentations that we remedy here. In our opinion, the early wolf domestication must be regarded as an intimate relationship between humans and canids including the breeding of the latter by prehistoric people, resulting in the European Palaeolithic dogs.

Highlights

► Accepting an Aurignacian beginning of the domestication of the wolf is controversial. ► Crockford and Kuzmin (2012) conjecture such an early domestication. ► This is a response to the comments of Crockford and Kuzmin (2012) on our identification of European Palaeolithic dogs. ► Two large canid types occur in certain European Palaeolithic sites. ► This is explained by the presence of Palaeolithic dogs and Pleistocene wolves.

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33,000 years old incipient dog from Siberia

Ovodov, N. D., Crockford, S. J., Kuzmin, Y. V., Higham, T. F., Hodgins, G. W., & 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(7), e22821.

Background

Virtually all well-documented remains of early domestic dog (Canis familiaris) come from the late Glacial and early Holocene periods (ca. 14,000–9000 calendar years ago, cal BP), with few putative dogs found prior to the Last Glacial Maximum (LGM, ca. 26,500–19,000 cal BP). The dearth of pre-LGM dog-like canids and incomplete state of their preservation has until now prevented an understanding of the morphological features of transitional forms between wild wolves and domesticated dogs in temporal perspective.

Methodology/Principal Finding

We describe the well-preserved remains of a dog-like canid from the Razboinichya Cave (Altai Mountains of southern Siberia). Because of the extraordinary preservation of the material, including skull, mandibles (both sides) and teeth, it was possible to conduct a complete morphological description and comparison with representative examples of pre-LGM wild wolves, modern wolves, prehistoric domesticated dogs, and early dog-like canids, using morphological criteria to distinguish between wolves and dogs. It was found that the Razboinichya Cave individual is most similar to fully domesticated dogs from Greenland (about 1000 years old), and unlike ancient and modern wolves, and putative dogs from Eliseevichi I site in central Russia. Direct AMS radiocarbon dating of the skull and mandible of the Razboinichya canid conducted in three independent laboratories resulted in highly compatible ages, with average value of ca. 33,000 cal BP.

Conclusions/Significance

The Razboinichya Cave specimen appears to be an incipient dog that did not give rise to late Glacial – early Holocene lineages and probably represents wolf domestication disrupted by the climatic and cultural changes associated with the LGM. The two earliest incipient dogs from Western Europe (Goyet, Belguim) and Siberia (Razboinichya), separated by thousands of kilometers, show that dog domestication was multiregional, and thus had no single place of origin (as some DNA data have suggested) and subsequent spread.

Determining the antiquity of dog origin

Raisor, M. J. (2004). Determining the antiquity of dog origins: canine domestication as a model for the consilience between molecular genetics and archaeology (Doctoral dissertation, Texas A&M University).

Archaeologists have favored a date of 14,000-15,000 years before present (BP) for canine domestication. However, recent studies of mutations in the mitochondrial DNA sequence by molecular geneticists have implied that dogs were domesticated over 100,000 years ago, which has challenged traditional theory. Geneticists have further hypothesized that dogs originated from wolf ancestors based upon the number of substitutions observed in dog and wolf haplotypes. Although both disciplines provide substantial evidence for their theories, the origin of dog domestication remains controversial. Several areas continue to be debatable. First, both geneticists and archaeologists incorrectly use the term domestication to describe events that clearly can not be proven to under human control. Second, the evolutionary development of canines is viewed by molecular biologists as well as archaeologist to be indicators of domestication without any further exploration of other probable causes. Third, the studies in canine genetics are so complex that most archaeologists have difficulty in providing evidence that would be contradictory to molecular theory. Fourth, both fields of study continually ignore innate behavioral characteristics of wolves that would make domestication highly improbable. Fifth, geneticists rely heavily on data gathered from sequencing of mitochondrial DNA, which has been assumed to maternally inherited. However recent human studies have shown that this assumption has now been proven to be incorrect. And finally, not only are morphological traits of fossilized dogs and wolves so similar that making a taxonomic identification improbable, but also the amount of archaeological remains available are too sparse and fragmented for accurate affiliation. An alternate theory of canine domestication will be proposed utilizing data gathered from the archaeological record and molecular research. I hypothesize that dogs diverged naturally from wolves 100,000 years ago as a result of the natural course of evolution, not human intervention, and had already evolved into a dog prior to being domesticated by humans 14,000-15,000 years ago. Evidence will be presented to clearly show that this hypothesis is a more accurate scenario of canine domestication.

Eurasian origin of American dogs

Leonard, J. A., Wayne, R. K., Wheeler, J., Valadez, R., Guillén, S., & Vila, C. (2002). Ancient DNA evidence for Old World origin of New World dogs. Science,298 (5598), 1613-1616.

Mitochondrial DNA sequences isolated from ancient dog remains from Latin America and Alaska showed that native American dogs originated from multiple Old World lineages of dogs that accompanied late Pleistocene humans across the Bering Strait. One clade of dog sequences was unique to the New World, which is consistent with a period of geographic isolation. This unique clade was absent from a large sample of modern dogs, which implies that European colonists systematically discouraged the breeding of native American dogs.

Cat responsible of extinctions on Mangere Is.

Tennyson, A. J. D., & Millener, P. R. (1994). Bird extinctions and fossil bones from Mangere Island, Chatham Islands. Notornis, 41(supplement), 165-178.

Fossil bones and earlier observations indicate that up to 22 species of bird have become extinct on Mangere Island. The extinctions appear to have been primarily a result of predation by cats, but human hunting and bush clearance are likely to account for the disappearance of some species. A crested penguin Eudyptes ?n.sp., two species of Pterodroma petrel, a shelduck Tadorna ?n.sp., Dieffenbach's Rail Gallirallus dieffenbachii, and a kaka Nestor ?n.sp. are present in fossil deposits on Mangere Island, but have not been reported from the island before. The relative proportion of remains in the deposits suggest that Blue Penguins Eudyptula minur, Broad-billed Prions Pachyptila vinata and Sooty Shearwaters Puffinus griseus have become more common on the island. Any such increases on Mangere Island, could have been a response of a few species to the large decrease in numbers and diversity that has affected seabirds as a whole at the Chatharns. Some seabird species mav have been able to increase because of reduced competition for-food.

Cats domesticated themselves

Hu, Y., Hu, S., Wang, W., Wu, X., Marshall, F. B., Chen, X., Hou, L. & Wang, C. (2013). Earliest evidence for commensal processes of cat domestication. Proceedings of the National Academy of Sciences, 201311439.

Domestic cats are one of the most popular pets globally, but the process of their domestication is not well understood. Near Eastern wildcats are thought to have been attracted to food sources in early agricultural settlements, following a commensal pathway to domestication. Early evidence for close human–cat relationships comes from a wildcat interred near a human on Cyprus ca. 9,500 y ago, but the earliest domestic cats are known only from Egyptian art dating to 4,000 y ago. Evidence is lacking from the key period of cat domestication 9,500–4,000 y ago. We report on the presence of cats directly dated between 5560–5280 cal B.P. in the early agricultural village of Quanhucun in Shaanxi, China. These cats were outside the wild range of Near Eastern wildcats and biometrically smaller, but within the size-range of domestic cats. The δ13C and δ15N values of human and animal bone collagen revealed substantial consumption of millet-based foods by humans, rodents, and cats. Ceramic storage containers designed to exclude rodents indicated a threat to stored grain in Yangshao villages. Taken together, isotopic and archaeological data demonstrate that cats were advantageous for ancient farmers. Isotopic data also show that one cat ate less meat and consumed more millet-based foods than expected, indicating that it scavenged among or was fed by people. This study offers fresh perspectives on cat domestication, providing the earliest known evidence for commensal relationships between people and cats.

Domestic dogs and SE European wolves

Verginelli, F., Capelli, C., Coia, V., Musiani, M., Falchetti, M., Ottini, L., Palmirotta, R., Tagliacozzo, A., de Grossi Mazzorin, I. & Mariani-Costantini, R. (2005). Mitochondrial DNA from prehistoric canids highlights relationships between dogs and South-East European wolves.Molecular biology and evolution, 22(12), 2541-2551.

The question of the origins of the dog has been much debated. The dog is descended from the wolf that at the end of the last glaciation (the archaeologically hypothesized period of dog domestication) was one of the most widespread among Holarctic mammals. Scenarios provided by genetic studies range from multiple dog-founding events to a single origin in East Asia.
 The earliest fossil dogs, dated ≈17–12,000 radiocarbon (¹⁴C) years ago (YA), were found in Europe and in the Middle East. Ancient DNA (a-DNA) evidence could contribute to the identification of dog-founder wolf populations. To gain insight into the relationships between ancient European wolves and dogs we analyzed a 262-bp mitochondrial DNA control region fragment retrieved from five prehistoric Italian canids ranging in age from ≈15,000 to ≈3,000 ¹⁴C YA. These canids were compared to a worldwide sample of 547 purebred dogs and 341 wolves. The ancient sequences were highly diverse and joined the three major clades of extant dog sequences. Phylogenetic investigations highlighted relationships between the ancient sequences and geographically widespread extant dog matrilines and between the ancient sequences and extant wolf matrilines of mainly East European origin. The results provide a-DNA support for the involvement of European wolves in the origins of the three major dog clades. Genetic data also suggest multiple independent domestication events. East European wolves may still reflect the genetic variation of ancient dog-founder populations.

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Introduction of dogs in Australia and the Pacific

Savolainen, P., Leitner, T., Wilton, A. N., Matisoo-Smith, E., & Lundeberg, J. (2004). A detailed picture of the origin of the Australian dingo, obtained from the study of mitochondrial DNA. Proceedings of the National Academy of Sciences of the United States of America, 101(33), 12387-12390.

To determine the origin and time of arrival to Australia of the dingo, 582 bp of the mtDNA control region were analyzed in 211 Australian dingoes sampled in all states of Australia, 676 dogs from all continents, and 38 Eurasian wolves, and 263 bp were analyzed in 19 pre-European archaeological dog samples from Polynesia. We found that all mtDNA sequences among dingoes were either identical to or differing by a single substitution from a single mtDNA type, A29. This mtDNA type, which was present in >50% of the dingoes, was found also among domestic dogs, but only in dogs from East Asia and Arctic America, whereas 18 of the 19 other types were unique to dingoes. The mean genetic distance to A29 among the dingo mtDNA sequences indicates an origin ≈5,000 years ago. From these results a detailed scenario of the origin and history of the dingo can be derived: dingoes have an origin from domesticated dogs coming from East Asia, possibly in connection with the Austronesian expansion into Island Southeast Asia. They were introduced from a small population of dogs, possibly at a single occasion, and have since lived isolated from other dog populations.

Oskarsson, M. C., Klütsch, C. F., Boonyaprakob, U., Wilton, A., Tanabe, Y., & Savolainen, P. (2012). Mitochondrial DNA data indicate an introduction through Mainland Southeast Asia for Australian dingoes and Polynesian domestic dogs.Proceedings of the Royal Society B: Biological Sciences, 279(1730), 967-974.

In the late stages of the global dispersal of dogs, dingoes appear in the Australian archaeological record 3500 years BP, and dogs were one of three domesticates brought with the colonization of Polynesia, but the introduction routes to this region remain unknown.

This also relates to questions about human history, such as to what extent the Polynesian culture was introduced with the Austronesian expansion from Taiwan or adopted en route, and whether pre-Neolithic Australia was culturally influenced by the surrounding Neolithic world. We investigate these questions by mapping the distribution of the mtDNA founder haplotypes for dingoes (A29) and ancient Polynesian dogs (Arc1 and Arc2) in samples across Southern East Asia (n = 424) and Island Southeast Asia (n = 219). All three haplotypes were found in South China, Mainland Southeast Asia and Indonesia but absent in Taiwan and the Philippines, and the mtDNA diversity among dingoes indicates an introduction to Australia 4600–18 300 years BP. These results suggest that Australian dingoes and Polynesian dogs originate from dogs introduced to Indonesia via Mainland Southeast Asia before the Neolithic, and not from Taiwan together with the Austronesian expansion. This underscores the complex origins of Polynesian culture and the isolation from Neolithic influence of the pre-Neolithic Australian culture.

Antiquity of dog introduction on California's Channel Islands

Rick, T. C., Walker, P. L., Willis, L. M., Noah, A. C., Erlandson, J. M., Vellanoweth, R. L., Braje, T.J. & Kennett, D. J. (2008). Dogs, humans and island ecosystems: the distribution, antiquity and ecology of domestic dogs (Canis familiaris) on California's Channel Islands, USA. The Holocene, 18(7), 1077-1087.

Archaeologists have made significant contributions to our understanding of ancient island environments, including the timing and implications of the introduction of non-native animals (pigs, chickens, rats, etc.) by humans.
Here, we focus on the historical ecology and biogeography of domestic dogs (Canis familiaris) on California's Channel Islands during the Holocene. Dogs are the only animal known unequivocally to have been introduced by Native Americans to the islands, but relatively little is known about their distribution, antiquity or influence on native island fauna and flora. We identified a minimum of 96 dogs from 42 archaeological sites on six of the eight islands. Dogs were present for at least 6000 years and appear to have increased in abundance through time. Our analysis suggests that dogs, along with humans and island foxes (Urocyon littoralis), would have had an impact on native animals and ecosystems, especially breeding birds and marine mammals. Dogs and island foxes likely competed with one another for food, however, and the impacts of dogs on island ecosystems may have been reduced by the presence of island foxes and the symbiotic relationship between dogs and humans. Dogs have been removed from all but one of the islands today, eliminating one of the few terrestrial carnivores present for most of the Holocene.

Pets or food?

Vigne J.-D. & Guilaine J. 2004. Les premiers animaux de compagnie, 8500 ans avant notre ère ? … ou comment j’ai mangé mon chat, mon chien et mon renard. Anthropozoologica 39 (1) : 249-273. 

The earliest pets, 8500 BC ? …or how I ate my cat, my dog and my fox.

Because they are of little interest economically, the carnivore mammals provide especially favourable characteristics for the archaeological study of the social and symbolic aspects of domestication in the early Neolithic periods. A short review of available data on the beginnings of the domestication of the dog, the cat and other carnivores, mainly in the Near East, allows us to ask questions about the conditions of their domestication.

Recent discoveries from the Preceramic Neolithic of Cyprus shed new light on these questions. They confirm that dog (Canis familiaris), fox (Vulpes vulpes) and cat (Felis s. lybica) were voluntarily brought to the island, and that this took place during the second half of the 9th millennium, the first half and the second half of the 8th millennium, respectively. This introduction suggests taming and appropriation of the animals by the human beings. A burial associating a human and a cat even suggests that these animals were kept as pets. But an important proportion of the bone remains of the three carnivores indicate that people did eat them. Moreover, several clues suggest that all or a part of these animals escaped human control and lived in feral groups. It seems that few dogs or none at all lived in the immediate vicinity of human dwellings. These observations, which conflict with our modern occidental conventions, suggest, for these early Neolithic phases, that the boundary between domestic and wild was fine and variable.


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