Controversial origins of the domestic dog

My adult education course on tetrapod evolution started this week. While I think it went ok, I hope I didn’t overwhelm my students: the idea for the first teaching session was to quickly run through Palaeozoic and Mesozoic tetrapod history, looking at the major clades, so we dashed through tetrapod origins, lepospondyls, temnospondyls, the living amphibian groups, anthracosaurs, amniote origins, Palaeozoic synapsids, the turtle origins controversy, and diapsid diversity. It will be interesting to see how things progress. The next session covers Mesozoic marine reptiles (excluding plesiosaurs and ichthyosaurs). Meanwhile, I have yet again been tinkering with that big review article on British dinosaurs (now at the final stages of the publication process), and Mike P. Taylor and I have been putting the finishing touches to a paper describing a new sauropod. Other areas of recent interest have been the ‘necks for sex’ hypothesis, Nick Longrich’s paper on ‘leg-wings’ in Archaeopteryx, and gigantic feral cats. More on those subjects in future. Moving on, here at last is that text on domestic dog origins.

Most zoologists ‘know’ that the domestic dog is a domesticated wolf (or, more likely, a number of independently domesticated wolf populations) and so well known is this view that some scientists question the recognition of Canis familiaris as a species separate from C. lupus. This is the ‘mainstream’ view eloquently discussed in several good books on dogs and on domestication, including Olsen’s Origins of the Domestic Dog: the Fossil Record (1985), Clutton-Brook’s A Natural History of Domesticated Animals (1999), and Coppinger & Coppinger’s Dogs: a Startling New Understanding of Canine Origins, Behavior and Evolution (2001). But here’s the news. The ‘domestic wolf’ model is actually not as firmly established as you might think, possibly wrong, and in fact arguably inferior to an alternative model of domestic dog evolution championed by a minority of canid specialists.

Many papers published on the subject of domestic dog origins state flatly that ‘the derivation of domestic dogs from the wolf is well established on behavioural and morphological grounds’, without actually saying in detail what these behavioural and morphological grounds are. It’s certainly true that domestic dogs and wolves are morphologically and genetically similar, but they’re actually also notably different, and while they share behavioural traits, they also differ profoundly in some important respects.

My primary inspiration on all of this has been Janice Koler-Matznick, founder of the New Guinea Singing Dog Conservation Society. Besides publishing important papers on singers (and I won’t be discussing those here: perhaps another time), her experience with them has caused her to re-evaluate theories about domestic dog origins and on domestication. Arguably her most important publication on this subject is Koler-Matznick (2002: free pdf here), which you should see for a good review.

I remain open-minded on the issue of both the phylogenetic affinities of domestic dogs, and on how domestication occurred, and frankly it’s such a huge area that it’s easy to become baffled by the literature. In an effort to keep things as simple as possible I’ve tried to restrict the discussion here to a consideration of one of the central issues: are domestic dogs really part of the species Canis lupus? Let me apologise now if there are areas that I’ve screwed up or misinterpreted, and apologies also to Jan for ‘borrowing’ her ideas so heavily.

Are domestic dogs really wolves? Some very obvious things to consider

As a rough rule of thumb, the domesticated forms of wild mammal species (1) revert back to wild-type after being feral for a few generations, and (2) readily interbreed with their wild ancestors. If domestic dogs are wolves, then the many populations of feral dogs that live world-wide should theoretically have reverted back to being wolf-like in appearance and behaviour. But they haven’t. Instead, domestic dogs always end up looking like pariah dogs – the relatively small (11-16 kg), socially flexible semi-domesticated and feral dogs of the Old World tropics. Dingos and the unusual New Guinea singing dog are part of the pariah dog complex, though the singing dog is so odd in behavioural, molecular and morphological features that it might warrant specific status (Koler-Matznick et al. 2001, 2003).

Archaeological data shows that pariah dogs have a stable history, with dog skulls from 4000 year old deposits in Thailand being essentially identical to the modern dingo-like pariah dogs of the area. Until relatively recently, domestic dogs must have been free-ranging and hence would have had ample opportunity to interbreed with wolves. While this has certainly happened on many occasions (modern wolf/dog hybrids are known from North America, Italy, as well as from archaeological samples*), what is surprising is that it hasn’t happened more often. This isn’t the case in other domesticated mammals, where interbreeding with wild ancestors is widespread.

* Some coyote populations have also been shown to include genetic data from domestic dogs (Adams et al. 2003).

In Europe, wolves remain only as endangered, fragmented populations vastly outnumbered by domestic dogs, and there has long been concern that wolves will be genetically swamped through interbreeding with dogs. Actually, there is no good evidence for this, and in a recent study of Italian wolves Verardi et al. (2006) found the two to have distinct gene pools, that hybridization had occurred only very rarely, and that introgressive hybridization between the two is so limited that it doesn’t pose a threat to the genetic integrity of the wolf. Wolves and domestic dogs are in fact staying distinct. This applies globally as well as locally: despite continuous, near-global sympatry between domestic dogs and wolves, hybridization has hardly occurred and only one mtDNA type is shared. On this basis Koler-Matznick (2002) argued that domestic dogs and wolves satisfy the biological species concept and shouldn’t be regarded as conspecific.

While (to my knowledge) no-one doubts the idea that domestic dogs and wolves are close relatives, firm evidence showing that domestic dogs are nested within the species Canis lupus is lacking. Attempts to genetically link domestic dogs to living wolf populations failed to find a match, making the hypothetical wolf ancestor of the domestic dog a mystery. Morell (1997) wrote of the University of California’s Robert Wayne, a leading researcher in this area, that ‘Although he sampled as many wolves as possible, it may be that the ancestral wolf population is now extinct’ (p. 1647). Of interest here is that the wolf most often cited as a potential domestic dog ancestor, the Indian peninsular wolf C. l. pallipes, has recently been shown to represent a radically unique, divergent lineage that is quite distinct from other wolves, and from domestic dogs (Jhala & Sharma 2004).

The implication from these lines of evidence is that domestic dogs descend from an ancestral pariah-like form which was quite different from wolves and that, while domestic dogs and wolves are closely related, they are distinct. Domestic dogs seem to have an independent history of descent and do not simply merge into wolves when the opportunity arises.

Wolves are behaviorally ill-suited for domestication

According to the conventional theory of dog domestication, wolves were domesticated either to function as big game hunters, or as guards. But here there are problems. If wolves really were domesticated prior to about 10,000 years ago (more on this date below), the earliest domestic dogs would have been living alongside people that were using clubs, spears and other such tools to subdue large prey, and therefore hunting via stealth and ambush. This poses a problem for the idea that people domesticated dogs to assist in large game hunting, as the chasing behaviour instinctive to wolves would presumably hinder human hunting efforts. Even in dingos we find that they’ve apparently always been preventing from participating in aboriginal kangaroo hunts because their chasing behaviour made the hunts a failure*. People would also have to pretty much fight with wolves in order to get any game animals back off them, given that wolves are highly food-possessive.

* I know that some hunting humans are outstanding long-distance runners that pursue wounded prey over km, and might theoretically benefit from canid assistance, but there is no evidence that this hunting strategy was widespread among ancient people. So far as we know it is limited to southern Africa (correct me if you know otherwise).

The possible use of wolves as guards is also problematical, given that wild canids function poorly in this role. Rather than defend a location, they will clear off when danger threatens, even if that location is their own den (including offspring). Sure, wolves might make some useful alerting noise if intruders were to come around, but other canids and other animals do this equally well.

While they can be tamed, wolves are actually very difficult to train. This probably results from their social system: only the dominant pair in the pack reproduces, and consequently there is an imperative to employ aggression to move up the pack hierarchy. These points don’t make wolves seem like ideal animals for domestication. Indeed, the fact that domestic dogs don’t form hierarchical packs makes them decidedly unwolf-like and it has been argued that the flexible social structure and high tolerance of domestic dogs to gregariousness suggests derivation from a canid that didn’t have a wolf-like hierarchical pack (Koler-Matznick 2002) [adjacent image depicts a dingo].

It is becoming increasingly recognized that dogs are remarkable among mammals in exhibiting human-like social skills and communicative behaviour (Hare et al. 2002). More so even than chimpanzees, dogs can reliably interpret human acoustic and visual cues (e.g., pointing or nodding), they have an inherent understanding of human perception, and they can even use human-like gestures, such as pointing. The presence of these social skills in domestic dogs might suggest that humans and wolves developed a communicative bond early on, and that this facilitated or initiated domestication. However, wolves have been studied in this context and have been found to lack the social skills and communicative behaviour that characterizes domestic dogs, so the social skills of domestic dogs presumably arose during domestication. This is supported by the fact that the domesticated foxes bred by Dmitry Belyaev and his team match domestic dogs in their ability to recognise human visual cues (I don’t want to discuss Belyaev’s fascinating experiment here as it would involve adding too many words: see Trut 1999).

Might wolves have domesticated themselves?

In view of these problems and others, those workers supporting the wolf hypothesis have argued that wolves domesticated themselves: by scavenging around camps and villages they became human commensals and eventually evolved into pariah dogs. As a relatively large (20-55 kg) predator it is difficult to imagine that wolves might have integrated into human society in this way. Notably, those carnivoran species that have become human commensals are all generalized omnivores smaller than most wolves: raccoons Procyon lotor, Red foxes Vulpes vulpes, Golden jackals Canis aureus and coyotes C. latrans.

Furthermore, it has been argued that the human camps hypothesized as the earliest places frequented by hypothetical commensal wolves would not have produced the waste that a large predator would require in order to make that fundamental niche shift. It is also worth noting that wolves were almost certainly a very real danger to prehistoric people and that they would have been regarded as enemies, not as potential friends.

Given that domestic dogs were apparently domesticated multiple times in various places, it is difficult to accept that so many wolf populations became amenable to domestication when these problems exist.

Morphologically, are domestic dogs really wolf-like?

It has long been recognised that domestic dogs differ from wolves in a number of detailed skull characters. Compared to wolves, domestic dogs are smaller and have proportionally smaller teeth, a wider palate, broader braincase and higher frontals, and smaller, less rounded auditory bullae. Mostly these differences have been explained as the result of either reduced selection under domestication (Björnerfeldt et al. 2006), or artificial selection for neotenous characters. There are however a few features present in domestic dogs (and not in wolves) that can’t be easily explained this way, such as the difference in the shape of the mandibular coronoid process.

While these characters might result from reduced selection under domestication, or artificial selection for neotenous characters, it’s interesting that many of them recall the conditions seen in non-wolf canids, such as jackals and dholes. Indeed some authors have concluded that domestic dogs are less like wolves than they are like these other wild canids (Manwell & Baker 1983, Wayne 1986, Koler-Matznick 2002). In fact we don’t know that the apparent neotenic features of domestic dogs result from artificial selection, given that neoteny can arise via other means, and it should at least be considered that the unwolf-like characters present in domestic dogs indicate derivation from a non-wolf ancestor.

A fairly logical assumption that one might make, were the ‘domestic wolf’ model valid, is that the most primitive domestic dogs (viz, those that had been exposed to the least amount of artificial selection) would be the most wolf-like of them all. This would apply both to fossils, and to the most primitive living breeds. As hinted at above however, archaeological specimens show that old dogs are pretty much the same as modern pariah dogs - there isn’t a series of specimens morphologically intermediate between wolves and domestic dogs - while the most primitive living domestic dogs, the dingos and New Guinea singing dogs for example, are not wolf-like but quite distinct from them behaviourally, socially and morphologically.

Domestic dogs: ancient and genetically distinct

If domestic dogs are wolves, you would expect the two to be very close genetically, certainly closer than universally recognised non-domesticated carnivoran taxa. Surprisingly for the dogs-are-wolves model, this is not true. In fact domestic dogs and wolves are (based on allozyme electrophoresis) further apart genetically than are leopards and jaguars, and (based on DNA hybridization) further apart than some bear species (Wayne et al. 1991).

A major analysis of mitochondrial DNA in domestic dogs worldwide (sampling 67 breeds as well as wolves from 27 localities) found most domestic dogs to belong to a ‘divergent monophyletic clade* sharing no sequences with wolves’, but with some domestic dog clades including some wolf haplotypes, apparently resulting from recent hybridization (Vilà et al. 1997). These authors concluded from mitochondrial and nuclear genes that domestic dogs were ancient, and that they had repeatedly interbred with wolves at various times and places throughout their history. This could be consistent with a derivation of domestic dogs from wolves, but equally it could merely show that hybridization has occurred at various times and places and it may be uninformative as regards ancestry. Indeed we know that several wolf-like domestic dog breeds (e.g., Saarloos wolfhound, Czech wolfhound, American tundra shepherd, American timber shepherd) were produced by deliberate crossing with wolves.

* The term ‘monophyletic clade’ is redundant given that a clade, by definition, is monophyletic. Included especially for Mike P. Taylor :)

The hardest bit of this story to accept is just how ancient these authors propose domestic dogs to be: the answer is more than 100,000 years old. Well, we modern members of Homo sapiens are meant to be about that old (give or take 50,000 years), so if that date is accurate, we must have started domesticating dogs as soon as we got out of Africa. Archaeological evidence for domestic dogs extends back to 14,000 years (based on a jaw from Germany) and other studies have suggested an origin at about 15,000 years ago (Savolainen et al. 2002). Less securely identified alleged domestic dogs from Russia are perhaps 17,000 years old, but there are no remains approaching 100,000 years in age.

While there are good reasons for thinking that the domestication of dogs probably extends beyond 15,000 years ago (perhaps to, say, 40,000 years or so), the lack of domestic dog prototypes in the archaeological and fossil record has been a problem. Some supporters of the ‘domestic wolf’ model have argued that we haven’t discovered wolf-dog intermediates because, prior to about 15,000 years ago, domestic dogs were morphologically indistinguishable from wolves. Unfortunately that is totally incompatible with the idea that wolves became domesticated after adopting a jackal-like commensal niche, as strong reduction in size is a requirement for the latter theory.

What might be a domestic dog prototype is known from strata extending back to 200,000-500,000 years however, and this is the extinct Chinese canid named C. l. variabilis Pei, 1934. Though classified as a small wolf, this form resembles domestic dogs in small size, detailed mandible shape and other features. Intriguingly, it appears to have been common and morphologically distinct for tens of thousands of years over a wide geographical area, despite sympatry with ‘normal’ C. lupus (Olsen 1985, Koler-Matznick 2002). Olsen has noted (pers. comm. cited in Koler-Matznick 2002) that the referral of C. l. variabilis to C. lupus was never satisfactory, and given the features mentioned here it is conceivable that this dog-like form was not really a wolf, but either a separate species ancestral to the domestic dog, or an early representative of C. familiaris.

If domestic dogs aren’t wolves, what are they?

All of this begs the question: if domestic dogs aren’t wolves, what are they? The answer seems to be that Canis familiaris is a distinct species with its own independent history. Prior to domestication, it presumably existed as a relatively small, generalized canid that voluntarily adopted the commensal pariah niche still occupied by many dog populations today. This is supported by the morphological and molecular distinctiveness of domestic dogs, by the anatomy and behaviour of primitive domestic dog breeds, and by the archaeological and fossil record.

If this is true then the truly wild ancestors of modern domestic dogs are extinct. True, there are wild pariah-type dogs in various places around the world (there are wild populations of New Guinea singing dogs and dingos, for example), but they’ve been introduced by people. However, the lack of the original wild form in a species that has become domesticated or at least semi-domesticated is not unprecedented nor unusual: Dromedaries Camelus dromedarius, for example, only exist in the wild today in feral form, and are otherwise entirely domesticated, and the wild ancestors of modern domestic horses and cattle are entirely extinct. In fact the eradication of the wild ancestors of a domestic form is thought by some to one of the key historical events that occurs during the domestication process (Dobney & Larson 2006).

The theory that domestic dogs descend, not from wolves, but from a wild Canis familiaris remains unpopular and overlooked, and even today relatively few zoologists are aware of the literature on this ‘alternative’ view of domestic dog origins. As mentioned earlier, my primary inspiration in this area has been Janice Koler-Matznick and her papers, and I have only scratched the surface in terms of the information she has provided. I’ve also avoided discussion of many other fascinating areas involved with this debate, such as Belyaev’s farm-fox experiment and the morphological and physiological changes observed in his domesticated foxes, theories on the domestication and/or transportation of grey foxes, South American foxes and other species, the diversity of the different domestic dog clades, controversies over the origin of pre-contact American dogs such as the Xoloitzcuintli, and David Paxton’s theory that the incorporation of dogs into human society resulted in morphological changes in humans.

It’s a lot to think about.

PS - you might have noticed that the font size and font type varies in the text above. I have NO idea why this is and have done all that I can to correct it (I've spent an hour trying to iron things out by messing with the html).

For the latest news on Tetrapod Zoology do go here.

Refs - -

Adams, J. R., Leonard, J. A. & Waits, L. P. 2003. Widespread occurrence of a domestic dog mitochondrial DNA haplotype in southeastern US coyotes. Molecular Ecology 12, 541-546.

Björnerfeldt, S., Webster, M. T. & Vilà, C. 2006. Relaxation of selective constraint on dog mitochondrial DNA following domestication. Genome Research 16, 990-994.

Dobney, K. & Larson, G. 2006. Genetics and animal domestication: new windows on an elusive process. Journal of Zoology 269, 261-271.

Hare, B., Brown, M., Williamson, C. & Tomasello, M. 2002. The domestication of social cognition in dogs. Science 298, 1634-1636.

Jhala, Y. & Sharma, D. K. 2004. The ancient wolves of India. International Wolf Summer 2004, 15-16.

Koler-Matznick, J. 2002. The origin of the dog revisited. Anthrozoös 15, 98-118.

- ., Brisbin, I. L., Feinstein, M. & Bulmer, S. 2003. An updated description of the New Guinea singing dog (Canis hallstromi, Troughton 1957). Journal of Zoology 261, 109-118.

- ., Brisbin, I. L. & McIntyre, J. K. 2001. The New Guinea singing dog: a living primitive dog. In Crockford, S. J. (ed). Dogs Through Time: An Archaeological Perspective. BAR International Series 889. Archaeopress (Oxford), pp. 239-247.

Manwell, C. & Baker, C. M. A. 1983. Origin of the dog: from wolf or wild Canis familiaris? Speculations in Science and Technology 6, 213-224.

Morell, V. 1997. The origin of dogs: running with the wolves. Science 276, 1647-1648.

Olsen, S. J. 1985. Origins of the Domestic Dog: The Fossil Record. The University of Arizona Press, Tucson.

Savolainen, P., Zhang, Y.-p., Luo, J., Lundeberg, J. & Leitner, T. 2002. Genetic evidence for an east Asian origin of domestic dogs. Science 298, 1610-1613.

Trut, L. N. 1999. Early canid domestication: the farm-fox experiment. American Scientist 87, 160-169.

Verardi, A., Lucchini, V. & Randi, E. 2006. Detecting introgressive hybridization between free-ranging domestic dogs and wild wolves (Canis lupus) by admixture linkage disequalibrum analysis. Molecular Ecology 15, 2845-2855.

Vilà, C., Savolainen, P., Maldonado, J. E., Amorim, I. R., Rice, J. E., Honeycutt, R. L., Crandall, K. A., Lundeberg, J. & Wayne, R. K. 1997. Multiple and ancient origins of the domestic dog. Science 276, 1687-1689.

Wayne, R. K. 1986. Cranial morphology of domestic and wild canids: the influence of development on morphological change. Journal of Morphology 187, 301-319.

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