The Fan Hitch   Volume 16, Number 4, September 2014

          Journal of the Inuit Sled Dog                                    
In This Issue....

From the Editor: Chronology

In the News: An interview with Joelie Sanguya


The Arctic Domus Project


The Practice of Veterinary Medicine and Loving Kindness in Labrador

Canadian/Greenland Inuit dogs and the “domestication syndrome”

Ptarmigan Hunting with Greenland Dogs

Documentary Film on the Sirius Patrol

Book Review: A Trapper in North-East Greenland


Okpik’s Dream

IMHO: Reflections

Index: Volume 16, The Fan Hitch


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         Wild                               Aboriginal landrace                     Cultured breed
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Thinking about the Canadian/Greenland Inuit Dogs in relationship
to the domestication of animals and the “domestication syndrome”

by Dr. Adam S. Wilkins

What are the fundamental differences between Canadian/Greenland Inuit Dogs and other breeds of dogs? Another way to put this is: how genetically different are the former from the latter and how do those differences contribute to their behavior and appearance? In thinking about this matter, it might help to back up and first consider a larger question, namely what exactly is a “domesticated animal”? 

The answer to that question, at first, seems easy: a domesticated animal is one that is quite tame (hence can be readily handled by humans); lives largely under the control of people, and; breeds easily in captivity. By these criteria, it is easy to distinguish domesticated from wild animals. Nevertheless, the distinction implies that domestication is an all-or-none state. Some observations suggest that that is not so, however. Domesticated animals that have escaped from human control and begun to breed in the wild often retain some, or many of the physical traits they acquired during their long history in association with humans, and pass them on to their offspring. This suggests that the reversion to being wild is not complete. (Whether the subsequent generations are more readily tame-able than their original wild forbears is not known but would be of great interest to determine.) Conversely, if a male and a female wolf have been raised in captivity and show tameness, to the point where they breed and produce wolf cubs, are these animals (parents plus cubs) true domesticates? Most people would say no, unless the cubs, when grown up, give rise to a line of equally tame wolves that breed in successive generations in captivity as such.

To some degree, these questions about domestication come down to its genetic basis, its biological foundation. Indeed, it would be good to know if there is a shared genetic basis for the condition amongst domesticated animals. The indication that there is such a common foundation traces to the work of Charles Darwin who extensively studied domesticates and compiled the first thorough descriptions of their traits. He described these studies in his classic treatise on heredity, The Variation of Animals and Plants Under Domestication, first published in 1868 and in a revised, expanded version in 1875 [1]. What Darwin discovered, to his evident surprise, is that domesticated animals share a spectrum of traits that, amongst themselves, show little obvious connection to each other. He detailed this most thoroughly for different mammalian domesticated species but there are indications that both domesticated birds, and even fish, also possess some of these features. The list (for mammals) includes: tameness (of course), smaller jaws and teeth, smaller brains (!), floppy ears, curly tails, coat pigmentation changes (in particular, white and/or light brown patches), and more frequent female sexual cycles.


From: The “domestication syndrome” in mammals: a unified explanation based on neural crest cell behavior and
 genetics. Genetics 197: 795-808.
                        Reprinted with permission from the Genetics Society of America.

Not all domesticates share all of these features but each set of domesticated strains for a given mammalian species usually includes all of them. Today, we know that the list extends to other characteristics – in particular physiological and behavioral ones that Darwin did not, indeed could not, study. The striking thing about these characteristics, which can be collectively termed the “domestication syndrome”, is their diversity and the absence of an obvious connecting thread. Furthermore, it has remained a puzzle in the more than 145 years since Darwin discovered it. Evidently, something happens during the domestication process to produce this suite of traits but just what that something is has remained mysterious.

In principle, since there clearly is a genetic basis to the phenomenon of domestication, genetic analysis should provide the means to discover those foundations. One would cross domesticated and wild strains of the same species and identify the genetic differences associated with domestication. In practice, of course, this is difficult and identifying the chromosomal locations, the “map positions” of the genes that differ, would only be a first step toward identifying their biological effects. Another problem with this approach is that most domesticated species have accumulated layers of further genetic change, which might obscure the initial changes involved in generating the domesticated state. Furthermore, some of the first changes, if at all deleterious, might have been replaced over many generations of breeding in captivity. In contrast, comparative genomic analysis, which has become possible in the last decade for virtually all species, should be able to resolve the first problem, that is the function of the altered genes, but it might still stumble over the second complication, the background of superimposed genetic changes. For the latter, only extensive comparisons between domesticated and wild species could help to narrow the differences to the significant ones (that is, assuming that there really is a common foundation to the domestication syndrome).

To get at the underlying genetics of the domesticated state, a Soviet scientist, Dmitry Belyaev, began an experiment to determine this in 1960, once it became possible to do modern genetics in the USSR, following the long freeze on this research imposed by Stalin. Belyaev’s idea was simple but brilliant: to recreate the domesticated state by intensive breeding and follow the changes as they occurred. He and his co-workers took nearly wild silver foxes, from a number of fox farms in the USSR, and began breeding them over successive generations, selecting for ever-tamer foxes from the new kits in each generation. By the 10th generation, they not only had tamer foxes, whose offspring were far tamer than the starting farm foxes, but ones who had begun to display some of the traits of the “domestication syndrome”. With further generations of successive breeding, those traits became both more prominent and frequent [reviewed in 2]. The ultimate “elite” tame foxes show all the features of the domestication syndrome with the possible exception of reduced brain size, which in other species involves a specific reduction in the forebrain, the extent depending upon the species.  The ambiguity about this last trait for the domesticated foxes is that the original farm foxes were not completely wild but had been subject to an inadvertent degree of domestication over decades; hence, the comparisons of brain size need to be done with the “elite” foxes and truly wild foxes, caught from the wild.


Figure 2 Diagrammatic representation of the neural crest hypothesis of the domestication syndrome,
illustrating how selection for tameness, leading to decreased neural crest input into the sympathetic
and adrenal systems, would cause the other observed components of the domestication syndrome as
unselected by-products, resulting in a “mild neurocristopathy.” Arrows indicate predicted directions
of influence on traits discussed in the text, as separated into direct and indirect developmental
(mechanistic) effects.
 
From: The “domestication syndrome” in mammals: a unified explanation based on neural crest cell
behavior and genetics. Genetics 197: 795-808.
                                                       Reprinted with permission from the Genetics Society of America.

The experiments showed that domestication involves a “package” of traits and provided hints to its genetic basis, specifically that it probably involves the cumulative action of mild semi-dominant effects from a set of genes. It is thus, almost certainly, a polygenic trait; there is no single “domestication gene”. Recent genomic analysis of domesticated rabbits, compared to wild ones, has yielded, even more directly, the same conclusion [3]. Both sets of results, but particularly Belyaev’s, also answered the question posed earlier: is “domestication” an all-or-none state? Judging from degrees of tameness in the foxes, as well as the other traits of the “domestication syndrome”, the answer must be “no”. Domestication is a quantitative state, not a qualitative one.

Still, this leaves the matter only partially resolved. Ultimately, one needs to know the full set of genes involved in any case of domestication and, precisely, how their mutant forms lead to the domesticated state. In July of this year, two colleagues and I published a hypothesis in Genetics that might provide part of the answer, my coauthors being Richard Wrangham, of Harvard University, and Tecumseh Fitch, of the University of Vienna. The germ of the idea was produced by Tecumseh in 2001-2002 but then lay fallow for almost a decade. The three of us then began to develop it, starting in 2011 in South Africa, at the Stellenbosch Institute of Advanced Studies, following a chance conversation between Richard and myself that revealed our common interest in the phenomenon. We soon brought Tecumseh back into the work. The key idea is that all the traits of the domestication syndrome can be explained, in principle, as the result of the cumulative effects of mutations in genes governing a special class of embryonic multi-potential cells, the “neural crest cells” (NCC).


Figure 1 Developmental schematic of the “domestication syndrome” in relation to the neural crest.
The blue
tube indicates the approximate position of the neural crest in the early embryo, and the
blue arrows
indicate pathways of neural crest cell migration.

From: The “domestication syndrome” in mammals: a unified explanation based on neural crest cell
behavior and genetics. Genetics 197: 795-808
                                                     Reprinted with permission from the Genetics Society of America.

Some of the effects, including key behavioral ones, would be indirect effects but all can be accounted for, at least to a first degree, by the idea. In the published paper, we go through the list of traits, explaining how the hypothesis can explain each trait of the “domestication syndrome”, and, at the end, we discuss possible experimental tests of the idea. [4]

To return to the initial question with which this article began, about the Inuit Dogs of Canada and Greenland, how domesticated are these dogs and can one relate this state to anything in their genetics? All the evidence indicates that they, amongst a relatively small number of “aboriginal land race dogs”, are distinct in their origins from the European-derived dogs that comprise the majority of dogs found in North America and that they probably derived from the dogs brought over by the original migrants from Asia into North America, 15,000 or so years ago [5,6]. The precise times of that human migration are controversial as is the question of whether there was one single migration or several, possibly over a period of several thousand years; the genetic evidence is generally taken to imply that there was more than one migration [7]. If, however, the ancestors of the Inuit Dogs were brought over in one of those ancient Asian migrations, then there is a good chance that they are closer, genetically and evolutionarily, to the original wolf ancestors of the dog. (A further controversial question is whether dogs evolved from wolves just once or from two or more wolf stocks independently.)
If the Inuit Dogs indeed have an ancient Asian origin, and if the deduction that domestication is a polygenic trait involving primarily genes of the NCC, then the prediction is that the Inuit Dogs have some but fewer NCC genes altered than the bulk of European-derived dogs, almost all of which are the product of intensive breeding and further domestication during the past two centuries.
Fortunately, this prediction is potentially testable through the detailed comparisons of their genomes with both Asian wolves and other, European-ancestry domestic dogs. Dog genomics is quite sophisticated and this approach should be fruitful for resolving this question as it has been for sorting out the evolutionary history of dogs generally [8, 9]. This would be a good test of our hypothesis and, whatever the results, should shed light on genetic foundations of the domesticated state in animals. Thus, if few or no NCC genes are found to be altered in the domesticated stocks, our hypothesis would be ruled out. Yet, if some but fewer NCC genes are altered in the Inuit Dogs than in the European-derived special modern breeds, the hypothesis would be supported.

If this research should strengthen the results that indicate a distinctive genetics (and origin) of these aboriginal landrace dogs [6], it should also provide support to efforts to make sure that these wonderful dogs are perpetuated.

It’s a funny thing about the domestication of animals. On the one hand, it was a major advance in the history of Homo sapiens and certainly contributed to the rise of complex human societies, with, correspondingly, a certain distancing from the life lived in Nature by our more distant, hunter-gatherer, ancestors. Yet, by having to relate to animals, even livestock, our connections with the natural world, through interactions with these other creatures, deepened in some sense. After all, one cannot keep and breed animals without attending to, and being aware of, their needs. Thus, as we became the kind of humans who could do this, our animals helped domesticate us.

Glossary
Forebrain: The forwardmost part of the vertebrate brain. In general, the forebrain processes cognitive, auditory, sensory, and visual information, as well as being involved in the forming and storage of memory and emotion

Genome: a full set of chromosomes; all the inheritable traits of an organism

Mutation: a sudden departure from the parent type in one or more heritable characteristics, caused by a change in a gene or a chromosome.

Mutant: of, relating to, undergoing, or resulting from change or mutation

Neurocristopathy: a diverse class of pathologies that may arise from defects in the development of tissues containing cells commonly derived from the embryonic neural crest cell lineage.

Polygenic: any of a group of genes that each produce a small quantitative effect on a particular characteristic of the phenotype, such as height

Quantitative: of or pertaining to the describing or measuring of quantity

Qualitative: involving or relating to distinctions based on quality or qualities

Bibliography
    1.   Darwin, C. (1868). The Variation of Animals and Plants under Domestication. John Murray, London

    2.   Trut, L., I. Oskina, A. Kharmalova (2009). Animal evolution during domestication: the domesticated fox as a model. BioEssays 31: 349-360.

    3.    Carneiro, M., C-J. Rubin, F. Di Palma, F.W. Albert, J. Alfoldi et al. (2014). Rabbit genome analysis reveals a polygenic basis for phenotypic change during domestication. Science 345: 1074-1079.

    4.    Wilkins, A.S., R.W. Wrangham, W. T. Fitch (2014). The “domestication syndrome” in mammals: a unified explanation based on neural crest cell behavior and genetics. Genetics 197: 795-808.

    5.    MacRury,I.K. (1991). The Inuit Dog: Its provenance, environment and history. Master’s thesis, University of Cambridge, Cambridge.

    6.    Van Asch, B., A-b. Zhang, M. C.R. Oskarsson, C.F.C. Kluetsch, A. Amorin, P. Savolainen (2013). Pre-Columbian origins of Native American dog breeds, with only limited replacement by European dogs, confirmed by mtDNA analysis. Proc. Roy. Soc. B 280: 20131142.

    7.    Oppenheimer, S. (2003). Out of Africa’s Eden: the peopling of the world. Jonathan Ball Publishers: Johannesburg.

    8.    Toh-blad, K., C.M. Wade, T.S. Mikkelson, E.K. Karlsson, D.B. Jaffee (2005). Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438: 803-819.

    9.    Vonholdt, B.M., J.P. Pollinger, K. E. Lohmueller, E. Han, H.G. Parker et al. (2010). Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464: 898-902. 

Dr. Adam S. Wilkins is the former editor of the general biology review journal BioEssays. His published books include advanced texts in developmental genetics and evolutionary developmental biology and his present book is on the evolution of the human face. Currently he is at the Institute of Theoretical Biology, Invalidenstr. 43, D-10115 Berlin, Germany.

* * *

The Fan Hitch wishes to express enormous gratitude to Dr. Wilkins for his time and effort in contributing this article; and to the Genetics Society of America for granting permission to use Figs. 1 and 2 and Table 1 as seen in The “domestication syndrome” in mammals: a unified explanation based on neural crest cell behavior and genetics.  Ed.
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