In the last post in this series, we looked at how artificial selection played an important role in Darwin’s conception of natural selection. One example of artificial selection that Darwin drew upon was the domestication of dogs – a process that has recently been greatly informed by genomics comparisons between dogs and their closest wild relatives, wolves.
(Slowly) becoming man’s best friend
The domestic dog has the distinction of being the only known animal to be domesticated by humans prior to the advent of agriculture. As such, dogs are not only man’s best friend in the animal kingdom, but also his oldest one. Though the precise origin of dogs was a mystery in Darwin’s day, Darwin drew on them as an example of artificial selection that would be familiar to his readers, since the practice of shaping breeds over time was familiar to his audience:
But when we compare the dray-horse and race-horse, the dromedary and camel, the various breeds of sheep fitted either for cultivated land or mountain pasture, with the wool of one breed good for one purpose, and that of another breed for another purpose; when we compare the many breeds of dogs, each good for man in very different ways… We cannot suppose that all the breeds were suddenly produced as perfect and as useful as we now see them; indeed, in several cases, we know that this has not been their history. The key is man’s power of accumulative selection: nature gives successive variations; man adds them up in certain directions useful to him. In this sense he may be said to make for himself useful breeds.
Note that Darwin is careful to point out that the variation itself is due to heredity: while humans can “add up” variation over time through selective breeding, they cannot produce the variation upon which they act. This point was important for Darwin to make, since he would later argue that natural selection also acts on that same heritable variation over time in a cumulative way.
Darwin’s use of dogs as an example was hindered, however, by his not knowing whether all dogs were descended from one ancestral species or if different breeds had been independently domesticated from different species. Darwin (erroneously, as we will soon see) suspected the latter, perhaps in part because of the dramatic morphological differences between dog breeds. He does, however, contemplate the possibility that some widely divergent dog breeds were derived from a common stock, and notes that, if demonstrated, such a finding would be significant evidence that “closely allied” species in nature were, in fact, related:
When we attempt to estimate the amount of structural difference between the domestic races of the same species, we are soon involved in doubt, from not knowing whether they have descended from one or several parent-species. This point, if it could be cleared up, would be interesting; if, for instance, it could be shown that the grey-hound, bloodhound, terrier, spaniel, and bull-dog, which we all know propagate their kind so truly, were the offspring of any single species, then such facts would have great weight in making us doubt about the immutability of the many very closely allied and natural species—for instance, of the many foxes—inhabiting different quarters of the world. I do not believe, as we shall presently see, that all our dogs have descended from any one wild species; but, in the case of some other domestic races, there is presumptive, or even strong, evidence in favour of this view…
The whole subject must, I think, remain vague; nevertheless, I may, without here entering on any details, state that, from geographical and other considerations, I think it highly probable that our domestic dogs have descended from several wild species.
As it turns out, Darwin was wrong on this point—we now know that all dog breeds are derived from only one wild species, the gray wolf (Canis lupis). Genome sequencing studies place dogs and gray wolves as extremely close relatives, which is hardly surprising, since they remain fully capable of interbreeding. Beyond establishing wolves as the closest wild relatives to dogs, genome comparisons are also beginning to reveal how human artificial selection brought dogs into being.
Teasing out the genetic basis for the domestication process has become increasingly possible now that the dog genome has been completely sequenced (published in 2005). This complete sequence allows for detailed comparisons between dogs and gray wolves, as well as comparisons between dog breeds. Both studies shed light on how artificial selection shaped dogs over their shared history with humans. Comparisons to wolves allow us to determine what selection steps took place during the early domestication process, whereas comparisons within breeds allow us to examine the selection steps that gave each breed its unique suite of characteristics.
From wolf to dog: the early domestication process
Though the wolf and dog genomes are overwhelmingly similar to one another, there are subtle differences between them. Recent research has sought to identify regions of the dog genome that were selected for during the domestication process. These regions are expected to show less variation than what is seen in the rest of the dog genome at large. Recall from our prior discussion that selection reduces the variation in a population by picking out certain variants and favoring their reproduction over others. As we scan through the dog genome, we can thus look for regions that show very little variation (i.e. all, or almost all, dogs have the same sequence in that area) in contrast to other regions where dogs, as a population, have more variation present. We can also then compare these putative selected regions with the wolf genome, to find the regions that not only have reduced variation within dogs but also differ from what we see in wolves (since we are interested in regions that contribute to the differences we see between wolves and dogs). Having found the regions of the dog genome that meet these criteria, it is then possible to examine the sorts of genes found in them, and generate hypotheses for why selection on those specific genes may contribute to the morphological and behavioral differences we observe.
The results of this analysis were striking in that the main category of genes found in such “candidate domestication regions” were genes involved in nervous system development and function. These results support the hypothesis that the primary focus of the early domestication process was selecting for behaviors, such as reduced aggression and willingness to submit to an altered, human-dominated social structure.
Small genetic changes add up
At both early stages of dog domestication (and as we will see, at later stages of breed creation), similar conclusions can be drawn: small changes at the genome level can have very large effects on morphology and behavior for the organism as a whole. We have discussed this point before in the context of comparing the human and chimpanzee genomes, and drawn the same conclusion—small perturbations to a complex system can effect substantial change over relatively “short” timescales. (By short, I mean short from a geological perspective.) Dogs and wolves have been in the process of separating for about 100,000 years, meaning that the dog domestication process and the subsequent creation of dog breeds occurs in a blink of an eye geologically speaking. If future paleontologists were to find a dachshund in the fossil record, it would seem to appear out of nowhere and have only a distant relationship to wolves, despite the fact that we know dogs and wolves are part of the same species (with all the inherent “fuzziness” that the term “species” entails).
Selection, artificial or natural, is selection
The power of artificial selection was a useful argument for Darwin in the 1850s, since it demonstrated the remarkable flexibility a species could have under differing selective environments, and revealed the inherent variation within populations that could be acted on to drive significant change over time. Here in the early 21st century we are beginning to see the genetic underpinnings of artificial selection at a genome-wide level, and the results are absolutely in keeping with Darwin’s ideas: that populations contain significant diversity, and that artificial selection can act on that diversity over time to promote the reproduction of certain variants over others, and thus shift average characteristics of a population. And just as Darwin drew parallels between artificial and natural selection, so to can we: the evidence we have suggests that natural selection acts in essentially the same way as artificial selection—by favoring the reproduction of certain variants over others.
In the next post in this series, we’ll examine how artificial selection shaped the creation of specific dog breeds, and examine how natural selection has also shaped the dog genome during the domestication process.
For further reading:
Lindblad-Toh, K., et al. (2005). Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438; 803 – 818 (link).
Axelsson, E., et al. (2013). The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 495; 360 – 364 (link).