Tuesday, July 26, 2011

Archeologists Argue for Multiple Domestication Events

Genome studies have resulted in different theories as to the epicenter of canine domestication, being either East Asia, the Middle East, or Africa. These conflicting results are further muddied by archeological investigations that place domestication either about 15,000 years ago, consistent with some of the genome results, or perhaps twice that far back, which can also be conformed to some largely earlier genetic studies. Two recent archeological papers and one genetics paper are worth detailed attention in these debates.

Small Dogs in Upper Paleolithic France

A team of French scientists analyzed remains of 49 small dogs (c. 12" to 17" at the withers) dating from 15,000 to 11,500 years ago that were recovered from three sites in France (Pont-d’Ambon, Montespan, and Le Closeau). The excavation sites also produced bones of red deer, wild boar, hare, and even some lions. The Montespan cave, well known for its rock art, also contained a life-size headless bear statue. The first and third pictures here from Bégouën and Casteret (1923) depict animal drawings from the Montespan cave walls, including horse, deer, bison, and perhaps hyena (lower right of the third picture). Dogs are not common in ancient cave art, though a likely instance can be seen in the lower left of the last picture below of the Magura cave in Bulgaria.

Previous excavations had found small dogs in Germany (Oberkassel), Switzerland (Hauterive-Champréveyres), southeastern France (Saint-Thibaud-de-Couz), southwestern France (Pont d’Ambon on a previous dig), and northern Spain (Erralia). The French team notes that these small dog discoveries are “frequently overlooked in the literature,” citing Savolainen and Pang as researchers guilty of this. Their article was undoubtedly in press by the time the controversy between Gray et al. and Klusch and Caprona surfaced, the subject of a prior blog on this site.

The French team considered the possibility that the recently excavated skeletons could be those of dholes, and not early small dogs, because dholes (Cuon alpinus) would be about the same size and had previously been found at a number of Pleistocene sites, though they eventually became extinct in Europe. In addition to prior anatomical studies concerning how to distinguish dholes from dogs, the researchers were able to identify ten additional distinguishing features in the skeletons of the two species. They concluded that the bones came from early dogs, not dholes or wolves (the bones were much smaller than bones of wolves of the same Late Glacial period). The picture shows two dholes at the Port Lympne Wild Animal Park in Kent, UK. The range of dholes in the wild is now restricted to Asia, particularly India and Southeast Asia.

The Montespan cave bones were dated 15,500-13,500 BP (before the present), those from Le Closeau about 13,000 BP, and those from Pont d’Ambon from 12,900 to 12,400 BP. The dog from Saint-Thibault-de-Couz could be dated 12,027 to 11,311 BP, and appears to have been even smaller than the dogs described in the present study, though whether such a decrease was correlated with time or some other factor could not be stated. “The only secure conclusion that we can draw is that these small Western European dogs are smaller than the contemporaneous large dogs in Eastern Europe, namely in Russia.”

It appears likely that dogs were sometimes eaten. Cutmarks on bones appeared in some cases to result from “butchery disarticulations.” (See Figure 6 in the paper.) The researchers cite other studies indicating dog consumption was widespread in Neolithic times and possibly earlier. They argue that the number of bones indicating butchery, at least at Montespan, suggest that eating dogs “appears to have been irregular and anecdotal in terms of subsistence strategy.” The cave dwellers preferred horse, reindeer, and chamois.

Some broken bones that were repaired “suggest complex relationships between these early dogs and the late Upper Paleolithic hunter-gatherer populations.” That is, some level of domestication had begun. The time frame suggested by the authors is consistent with domestication occurring around 16,300 years ago (Pang et al. (2009)), though the distribution of domestic dogs so far from previously suggested epicenters of domestication requires explanation.

Large Dogs in Paleolithic Belgium

Another piece of archeological research attempts to push the date of domestication back considerably further. A team of scientists from Belgium, Russian, England, and Germany, further has argued that fossil canids found in Belgium, Ukraine, and Russia, dating from 31,000 years ago, were large dogs, not wolves, though the dogs from the various excavations were not found to “form a homogenous genetic group.” The researchers thus argue for domestication as early as the Aurignacian, stating the issue as follows:

“Our hypotheses are that changes in dog morphology compared to wolf morphology appeared rather abruptly, that they were linked to the effects of domestication and that these changes became fixed in the dog population. If evidence cannot be not found to support these hypotheses, the alternative hypothesis would then be that substantial morphological differences were present between Pleistocene wolf populations, before domestication, and between lineages of wolves that led later on to recent wolves and dogs.”

Germonpre et al. analyzed skulls from a period where hunting game included mammoths and rhinoceros. Fox and wolf bones at the locations probably reflect the use of their hides in making fur clothing.

The skull morphology of the specimens was found to be similar across the studied group but distinct from the skulls of wolves. The dogs had a shorter and broader snout than wolves, shorter skulls, but a wider braincase. The researchers speculate that large dogs could have helped with “tracking, hunting or transport of large, ‘ice-age’ game, possibly mammoths on the Russian Plain.” They note that the skull shape “resembles that of the [Central Asian Shepherd dog] which was originally used as a flock guardian and as a protector against predators such as bears, striped hyenas and wolves.” I question whether transport, if this means pulling by some sort of harness system, could have occurred in this stage of the human-canine association.

The team suggests that “[o]nce the Palaeolithic dogs were established, their skull morphology seems to have remained stable,” noting that other early dogs “equally display a remarkable similarity in skull shape that persevered for thousands of years.”

In addition to morphological analysis of bones, the researchers extracted DNA, and used stable isotope analysis of bone collagen, a technique for reconstructing past animal diets. The diet of wolves appears to have been more restricted than nearby humans, though analysis of two large canids that were identified in previous research as wolves indicate some consumption of marine fish. The authors of the current research raise the possibility that these canids were in fact dogs whose eating habits had begun to track those of the humans near which they were beginning to live. Such a dietary parallel, of course, would be consistent with the refuse heap argument advanced by the Coppingers regarding the process of domestication, though they would date the process from the formation of permanent settlements, much later than the dating suggested by Germonpre et al. Arguably, however, groups of wolves could have become sufficiently associated with cave-dwelling humans, who after all are in something of a permanent settlement during the long periods some caves were occupied, leading to some selection in the surrounding wolf populations, without the occurrence of a completed domestication event.

The Pleistocene dogs yielded unique mitochondrial DNA sequences, from which the study concluded:

“Belgian large canids carried a substantial amount of genetic diversity. Since dogs were domesticated from gray wolves, ultimately the first dogs would have carried a wolf-like genetic sequence, and hence will be not identifiable genetically as the first dogs. Only after isolated breeding, it is possible that certain genotypes in the Palaeolithic dogs drifted to high frequencies and might therefore be distinguishable from those of the source wolf population. Thus one would only expect to see a differentiation of dogs and wolves after several thousands of years due to the bottleneck caused by selective breeding during early domestication. At the same time certain (e.g. morphological) traits were probably expressed and selected for, or just arose by drift. After this initial phase of domestication a relaxation of constraints occurred. Wolves after the domestication (i.e. dogs) were insulated from the full force of negative selection because humans cared for them, e.g. providing food and physical protection – therefore (slightly) disadvantageous traits could still survive and produce offspring. These individuals in their natural environment would probably not have contributed to the next generation’s gene pool. Later, exponential population growth increased genetic diversity to the high levels that are observed in dogs today. Since the domestication of dogs is, in evolutionary timescales, a rather recent event, the lineages of wolves and dogs have not separated yet, and therefore do not allow rigorous identification of the analyzed specimens. Given the proposed timescale for the dog domestication of only a few ten thousands of years and the mtDNA mutation rate, this is not unexpected. However, due to extensive breeding in the last couple of hundred years, the soaring population size of dogs has provided a sufficiently large genetic background to accumulate relatively high levels of mtDNA diversity.”

Several thousand years for genetic differentiation of dogs from wolves seems rather longer than might be required considering Belyaev's foxes, even without the artificial selection used in the farm fox experiment). The authors of the first study discussed above refer to the second study and express skepticism that there could have been domestic dogs in the Aurignacian:

“In our opinion, it is not excluded that these original canids were representatives of local divergent populations of wild wolves, and, though interesting and plausible, the proposal of so early dog domestication still needs to be confirmed by further discoveries. Therefore, in the present state of knowledge, the earliest undisputable dogs do not pre-date the beginning of the Late Glacial (c. 18,000 cal BP).”

This objection would not, however, be inconsistent with the alternative hypothesis proposed by Germonpre et al., namely that “substantial morphological differences were present between Pleistocene wolf populations, before domestication, and between lineages of wolves that led later on to recent wolves and dogs.” Thus, there could have been a large proto-domestication period during which various wolf groups had sufficient proximity to, and some dependence on, human populations, resulting in some selection within those wolf groups of traits that allowed for the proximity.

Recent Dog-Wolf Hybridization in Scandinavia

A short communication released in 2010 by some of the scientists involved in the genome research pointing to an East Asian origin for canine domestication discusses some results that don’t fit into that theory. The research group built on the finding that mtDNA haplotypes of dogs were distributed in six phylogenetic groups, clades A to F. Clade D is restricted to North Europe, Siberia, Southwest Asia, and the Mediterranean, and therefore did not originate in East Asia (Pang et al. 2009). Clade D was found to consist of two subclades that separated at least 50,000 years ago, well before most estimates of domestication. Subclade d1 is found in North Eurasia and d2 in Southwest Asia and the Mediterranean, from which the group concludes that they are likely to have separate origins from wolves. Subclade d1 had a frequency above 30% in native breeds in its core distribution area in Northern Scandinavia, indicating “a major separate influx of ‘wolf genes’ into the dog gene pool.”

The researchers studied 328 female lineages of Scandinavian and Arctic Spitz breeds, including Lapponian Herder, Jämthund, Finnish Lapphund, Norwegian Elkhound, finding he proportion carrying d1 to be, respectively 75%, 74%, 65%, and 46%, but Swedish Vallhund and Norwegian Buhund did not have the haplotype at all. They find this distribution remarkable and “the only example of a mtDNA haplogroup found only in a specific type of dogs from a restricted geographical area and in the majority of the individuals in this area.” Neolithic dog samples from southern Sweden did not include any evidence of Clade D. Because the study is of mitochondrial DNA, this indicates crossbreeding between female wolf and male dog, whereas identified crossbreeding between the two groups has more often involved male wolves and female dogs.

Based on frequency of mutation estimates, the research team concluded that haplogroup d1 originated between 480 and 3,000 years ago, resulting from crossbreeding of wolves with an already established dog population, not from independent domestication. The researchers take a stab at correlating this with human history:

“The sharing of the d1 haplotypes between the Lapphund breeds associated with the non-Indo-European speaking and nomadic Sami and some hunting breeds connected to Indo-European speaking farmers … is notable. Possibly, efficient hunting and herding dogs were items of trade between the two populations. The direction of this trade is not clear, but an origin of d1 among the Sami related breeds is indicated, as all these breeds have d1 haplotypes, while only some breeds linked to the Indo-Europeans have this haplotype….”

This kind of analysis is going to be increasingly important if domestication is to be put in an anthropological context. It must be determined not just when the dogs were interacting with humans, but who those humans were, where migratory patterns took them, and what other human populations interacted with them.

Archaeology vs. Genetics

Pionnier-Capitan et al., the first paper discussed above, consider how their findings may correlate with the series of genome studies seeking the time and place of domestication. Contrasting the single domestication event argued for by Savolainen et al. with the multiple event findings of vonHoldt et al., the French team states that the morphological diversity of early dogs “are in accordance more with a multiple origin than a unique common East Asian origin.”

The French team refers to the “large morphological diversity” of the Late Glacial Western Eurasian dogs, noting the medium size of some (17" to 24" at the withers), such as the Natufian dogs, the large size of others, such as those found at Eliseevichi I (greater than 24" at the withers), and the small to very small dogs described in their own study and others (12" to 17" at the withers). A connection of the small dog haplotype to Middle Eastern gray wolves was argued recently, to which the East Asian camp has responded. The fact that dogs crossing over the land bridge appear to be the only source of domesticated dogs in the Americas indicates that separate domestication events do not easily happen, but the archeological evidence remains to be fully correlated with the work of the geneticists.

Sources: M. Pionnier-Capitan, C. Bemilli, P. Bodu, G. Celerier, J.-G. Ferrie, P. Fosse, M. Garcia, and J.-D. Vigne (September 2011). New Evidence for Upper Palaeolithic Small Domestic Dogs in South-Western Europe. Journal of Archaeological Science, 38(9), 2123-2140; E.L. Jones (November 2009). Climate Change, Patch Choice, and Intensification at Pont d’Ambon (Dordogne, France) During the Younger Dryas. Quaternary Research, 72(3), 371-6 (finding intensified rabbit use during a period of climate change by the inhabitants of Pont d’Ambon); R. Bégouën and N. Casteret (1923). La Caverne de Montespan . Revue Archéologique de Picardie, 33; M. Germonpre, M.V. Sablin, R.E. Stevens, R.E.M. Hedges, M. Hofreiter, M. Stiller, and V. Despres (2009). Fossil Dogs and Wolves from Paleolithic Sites in Belgium, the Ukraine and Russia: Osteometry, Ancient DNA and Stable Isotopes. Journal of Archaeological Science, 36(2), 473-490; M.V. Sablin and G.A. Khlopachev (2002). The Earliest Ice Age Dogs: Evidence from Eliseevichi I. Current Anthropology, 43(2), 795-799 (“the idea of a single locus of domestication is not supported (Morell 1997). It seems probable that humans tamed wolf pups in many parts of the world and therefore that several subspecies of wolf contributed to the ancestry of the dog. We suggest that the specimens of dogs reported here [in the Dnieper basin on the Sudost River] were domesticated in situ from local northern wolves.”); R. and L. Coppinger (2001). Dogs: A Startling New Understanding of Canine Origin, Behavior & Evolution. New York, Scribner; J.-F. Pang, C. Kluetsch, X.-J. Zou, et al. (2009). mtDNA Indicate a Single Origin for Dogs South of Yangtze River, Less Than 16,300 Years Ago, From Numerous Wolves. Molecular Biology and Evolution, 26, 2849-64. See also C. Vila, P. Savolainen, J. Maldonado, et al. (1997). Multiple and Ancient Origins of the Domestic Dog. Science, 276, 168-9 (showing Savolainen had earlier accepted a multiple origins approach); R. Hawkins, A. Jansen & Waidman (2004). Arrianus: De Lange Jacht en Lurecoursing. Eburon, Amsterdam (in Dutch) (discussing instances of multiple domestication events for other species besides dogs).

Thanks to Hans Hillewaert for permission tor reprint the picture of the dhole. Thanks to I, Nk, and Wikipedia for permission to use the Magura cave photograph.

Thanks to Richard Hawkins and Brian Duggan for ever generous wisdom and advice.

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