Tamed

by Alice Roberts

  Belyaev certainly thought that something else – not just mutations in DNA – must have been responsible for all the changes he saw happening in his increasingly tame foxes. It wasn’t just the speed of the changes that required explanation, but the striking similarity between domesticated silver foxes and dogs. It was impossible to believe that all those traits in the foxes – from tail-wagging to floppy ears – arose through new mutations and that the similarity with dogs was coincidental. It seemed unlikely that each individual trait had appeared in an entirely piecemeal fashion. Instead, it seemed more probable that one or two fundamental genetic changes were having widespread effects – that genes were working in a hierarchy, with some controlling others.

  And just possessing a particular gene is only the start of the story – genes can be switched on and off. Belyaev hypothesised that the genes which controlled behavioural variation also played an important regulatory role – affecting a cascade of other genes, switching them on or off – during development. The Russian scientists who inherited Belyaev’s experiment have suggested that the genes in question may be involved with the hormone cortisol, which mediates the body’s stress response, and the neurotransmitter serotonin. The domesticated foxes had very low levels of cortisol in their blood, and higher levels of serotonin in their brains. Low cortisol levels have also been shown in other domestic animals, while high serotonin levels are associated with an inhibition of aggression. But what’s really important here is the possible effect of these two biological signals on a developing fox-cub fetus.

  The Russian scientists suggested that maternal cortisol and serotonin could influence how many other genes are expressed, both during embryonic development and even after birth while the cubs are still suckling. By choosing foxes which were particularly tame, the Russian scientists may have been selecting individuals who had certain variants of a few, key genes relating to stress tolerance and diminished aggression. This meant that the next generation of foxes could be exposed to unusual patterns of stress hormones, in the womb, which could in turn affect the way that genes were being switched on and off in the developing fox fetus – in a way that didn’t normally happen in the wild. The programme of embryonic development, which had settled into a fairly stable state under natural selection, certainly seemed to be shaken up in some way, producing a surprising degree of variety amongst the increasingly domesticated silver foxes. The researchers suggested that just a few genetic variants could have widespread effects, introducing a range coat colours as well as oddities such as drooping ears and even curly tails. Other researchers have suggested that changes to thyroid hormones – and related genes – could have similar widespread effects on stress response, tameness, body size and coat colour. So selective breeding focusing on one particular trait, likely to be linked with genes relating to stress tolerance and tameness, could quickly affect a whole host of other characteristics.

  We’ve just begun to identify some of the genes that could be involved in creating such a range of effects and to understand how this happens at a molecular level. Geneticists have started to comb through dog genomes to look for particular regions, particular stretches of DNA, that look as though they have been subject to selection. It’s a tricky thing to do. The complicated population history of domesticated dogs, which includes migrations, the extinction of some populations, interbreeding in some places and genetic isolation in others, makes it a difficult task. Nevertheless, there are regions of the genome that stand out, and eight out of the top twenty identified regions contain genes that have important neurological functions. One of them is already known to have effects on both social behaviour and pigmentation. It’s called ASIP, the Agouti Signalling Protein gene. The protein it encodes switches the pigment-producing cells known as melanocytes in hair follicles to producing a paler version of melanin – essentially it controls how darker and paler fur develops in different areas. For good measure, ASIP affects fat metabolism as well – and has also been shown, in mice, to influence aggressiveness. This one gene illustrates quite beautifully how selectively breeding animals which exhibit a certain type of social behaviour could lead to incidental changes in colouring and metabolism. But some traits which end up being inherited together may be influenced by separate genes – that, crucially, lie in close proximity to each other on a chromosome. Strong positive selection for a particular trait, and a particular gene, will often mean that neighbouring genes come along for the ride.

  The idea that different traits can be somehow linked together, and inherited together, has been around for a long time and even predates genetics. It’s called pleiotropy (Greek for many characters) and the term was coined in the early nineteenth century. In the Origin, Darwin wrote, ‘… if man goes on selecting, and thus augmenting, any peculiarity, he will almost certainly unconsciously modify other parts of the structure, owing to the mysterious laws of the correlation of growth.’ These laws are much less mysterious today – we know that various traits are linked through genetics and development. We understand the precise basis of the correlations in at least some cases – such as that of the Agouti Signalling Protein and its widespread effects in the body. Combined with the idea of destabilising selection, where artificial breeding must be regularly bringing particular sets of genes together, pleiotropy goes a long way towards explaining why dogs are so much more variable than wolves whilst being, on the face of it, genetically very similar. New genetic mutations can have widespread – pleiotropic – effects, influencing a whole range of characters. And in some cases, you probably don’t even need a brand new mutation to spice things up, you just need to be combining particular sets of genes that don’t usually get pressed together quite so consistently in the wild. In this way, the developmental programme is destabilised – throwing up new and interesting varieties in the process. It seems very likely that even amongst early dogs, and long before any of the modern breeds emerged, there was plenty of variability – just as there is in the experimental, domesticated silver foxes.

  The initial domestication of wolves into dogs could have been – if not as fast as the transformation of wild silver foxes into domesticated ones, over just fifty years – still relatively swift. The new theories about the underlying molecular mechanism of the change reveal pleiotropy at almost every turn. The cascading and destabilising effects of specific genetic variants, picked out initially for their influence on docility and tolerance, have the potential to create widespread and potentially very rapid changes to anatomy, physiology and other aspects of behaviour. What seems like a difficult and improbable transition – from wild to domesticated – suddenly appears to be a much easier, and even likely, development. Perhaps there were many, many instances of wolves becoming dogs, or almost-dogs – even if we can only find genetic traces of just one or two of these experiments developing into lineages that survive to the present day.

  The big chill of the last glacial maximum, peaking between 21,000 and 17,000 years ago, put animals right across Eurasia under pressure. Ice sheets descended over Europe, and Siberia became incredibly cold and dry. Many lineages went extinct. Sometimes entire species succumbed. It wouldn’t be surprising if more than a few canine domestication experiments were curtailed by this environmental catastrophe. In the run-up to the glacial maximum, free food at the margins of hunter-gatherer camps could have made all the difference to some packs of wolves.

  Everyone felt the chill; humans too. And even if some lineages of ancient dogs went extinct, experts have argued that having dogs may have been a crucial survival advantage for human hunter-gatherers at the peak of the last Ice Age. Could this even explain why modern humans, though hard hit, made it through the last glacial maximum, while Neanderthals did not? It’s a neat and enticing explanation, but this always makes me nervous. I suspect it’s way too simple. History is complex, and while we can suggest hypotheses, we have to be wary when we can’t even begin to test them. Nevertheless, there seems no reason to doubt that dogs would have helped the survival and
success of some tribes of hunter-gatherers.

  After the big chill, fossil evidence of domestic dogs starts to appear all over Eurasia. By 8,000 years ago they’re found at sites stretching from western Europe to eastern Asia. As we’ve seen, the latest genetic data from ancient and modern dogs points to a single origin, so it’s extremely unlikely that all these Holocene dogs were independently domesticated from local wolf populations. Instead, dogs must have arrived with migrating humans, or were acquired from elsewhere by local human populations.

  Prehistoric dogs were still fairly wolf-like, judging from their skeletons at least. But there was probably already quite a bit of variety in coat colour, tail curliness and ear floppiness, if those Russian foxes are anything to go on. At the 8,000-year-old site of Svaerdborg in Denmark, archaeologists have found evidence for three types of dogs of different sizes. So it looks as though, even this early, there was some divergence into what might perhaps be seen as proto-breeds. Maybe our prehistoric ancestors were already trying to breed dogs that had particular skills: dogs for guarding and shepherding, dogs good at following scents, or even at pulling sledges.

  A breed apart

  After the origin and expansion of agriculture, dogs became even more widespread. And just as human diets were changing, it seems that dogs’ diets were too. Early dogs were eating meaty diets – although, one study suggests, perhaps different meat from their wild wolf cousins. Analysis of bones from the 30,000-year-old site of Prˇedmostí in the Czech Republic has shown that the canids thought to be Palaeolithic dogs were eating meat from reindeer and muskox, whereas the wolves were eating horse and mammoth meat. Once agriculture started, the menu of food available from humans would have changed. There must have been rich pickings for village dogs hanging around the rubbish dumps of newly sedentary human communities.

  Most modern dogs have multiple copies of the amylase gene, which encodes the enzyme for digesting starch. The more copies a dog possesses of this gene, the more amylase it produces in its pancreas – extremely useful if you’re finding food in the village midden or eating scraps from the table. Over time, dogs’ diets became less carnivorous, and more omnivorous – more like the diets of their human allies. But the number of copies of the amylase gene varies considerably amongst modern dogs. Most of the variation in amylase gene numbers comes down to the breed. There could be a few reasons for this. Having established that this variation wasn’t just down to chance, researchers wondered if it could be linked to phylogeny – to the ‘family history’ of breeds. But that didn’t seem to be the case. They also considered whether interbreeding with wolves might have reduced the copy number of the amylase gene in some breeds, but again that didn’t appear to adequately explain the pattern. The explanation that’s left standing is that amylase copy number reflects differences in ancient dog diets.

  Studies of isotopes of carbon and nitrogen from samples of ancient dog bones have revealed clues to ancient diets – showing just how variable those diets were. We know, for instance, that around 9,000 years ago in China, millet made up 65–90 per cent of what dogs were eating. Whereas 3,000 years ago, on the coast of Korea, dogs were devouring marine mammals and fish. In various places, dogs were being exposed to different dietary challenges. Over time, their genetic make-up changed accordingly.

  This type of change to the genome – boosting the numbers of a particular gene – happens because of mistakes during meiosis, the special type of cell division that makes egg or sperm (which contain a single set of chromosomes, as opposed to the double set contained in all other cells of the body). During meiosis, the chromosomes pair up, and then, in each pair, swap DNA with each other. Mistakes that happen during this ‘crossing over’ can result in duplications of a gene on one chromosome. Once that occurs, it actually increases the chance of a similar mistake happening in the next generation, again at meiosis, when eggs or sperm are made. Two copies of a gene on one chromosome, and one on another, make mis-pairing and gene duplication more likely. So this error can end up multiplying copies of a particular gene – and if that change is beneficial natural selection won’t weed out those mistakes but favour them.

  Dogs seem to be split into two groups – those with very low numbers of the amylase gene, and those with many copies. The modern dogs with the lowest number – just two copies, like wolves – tend to be from breeds such as the Siberian husky, Greenland sledge dog and the Australian dingo. Dogs with high copy numbers map rather neatly on to agrarian areas of the globe – where humans were farming in prehistory. The saluki, which originated in the Middle East – where agriculture first got off the ground – has a phenomenal twenty-nine copies. But this change wasn’t immediate – Neolithic dogs don’t show the major expansion in amylase genes that their later descendants, living alongside farmers, would evolve.

  It’s in the Neolithic, when humans start to farm, that dogs also start to spread beyond Eurasia for the first time. And they track the spread of farming. Dogs appear in sub-Saharan Africa after the beginning of the Neolithic there, 5,600 years ago, and take another 4,000 years to reach South Africa. Dogs appear in archaeological sites in Mexico around 5,000 years ago, coinciding with the first farmers there, but only reach the southernmost tip of South America 4,000 years later. Studies of mitochondrial DNA suggested that all those early American dog lineages were completely replaced, following the European colonisation of the Americas. But the latest genome-wide studies tell a different story: European dogs – arriving with colonisers in just the last 500 years – mixed with the indigenous New World dogs.

  The modern breeds that we know so well take much longer to arrive. They are very recent inventions. Dog genes reflect this history. There are signs of two prominent genetic bottlenecks amongst the ancestors of dogs: one at the origin of domestication, and another when modern breeds emerged, in just the last 200 years. Breeders began to focus closely on promoting particular traits, producing dogs that were wonderfully obedient, providing invaluable help with hunting and herding. But the malleability of characteristics under selective breeding became an allure in itself, and so dogs were also bred with specific shapes, sizes, colours and textures. The morphological variety amongst modern dog breeds exceeds that in the whole of the rest of the family Canidae, which includes foxes and jackals as well as wolves and dogs.

  There are nearly 400 breeds of dogs today, and most of them – in all their wonderful diversity – have really only been around since the nineteenth century. This is when the strict breeding needed to create and conserve the kinds of strains recognised by kennel clubs really got going. The breeds that appear to be most ancient, with the most deep-rooted lineages on the dog family tree, are actually found in places where dogs only arrived relatively recently. Dogs arrived in the islands of south-east Asia 3,500 years ago and in South Africa around 1,400 years ago and yet these areas are home to a number of ‘genetically ancient’ breeds: basenjis, New Guinea singing dogs and dingoes. This pattern shows that these lineages have been isolated for longer than most other breeds. The deep roots don’t mean that their lineages were the first to branch off, but rather that out on the periphery they have stayed the most genetically distinct.

  Analysis of the genomes of various dog breeds has been used to build a very detailed family tree. Within that family tree, there are twenty-three clusters or clades, each one containing a set of branches which represent a group of closely related breeds. European terriers, for instance, form one clade; basset, fox and otter hounds, together with dachshunds and beagles, form another. Spaniels, retrievers and setters are also a closely related cluster. Strict control of breeding has kept these clades largely separate – but a few breeds contain DNA from two or more clades, revealing how different dogs with particular traits have been recently crossed to create new types. For instance, while the pug dog has genetic connections with other Asian toy breeds, as expected, it’s also part of the tight cluster containing European toy dogs. This suggests that pugs were exported from Asia, and then deliberat
ely crossed with European dogs to create new, diminutive breeds. Although the genetic data reflects the creation of strictly separate breeds in the last 200 years, it’s also clear that these breeds weren’t drawn from a homogeneous population – selection for distinct traits had already separated dogs into types which were suited to particular functions, and those older distinctions form the basis for those twenty-three clades in the dog family tree.

  Lots of breeds with supposedly ancient roots, however, turn out to be recent recreations. Wolfhounds were, as their name suggests, used to hunt their wild cousins – very successfully. By 1786 there were no wolves left in Ireland, and so no need for wolfhounds. By 1840, the Irish wolfhound had also gone extinct. But then a Scotsman living in Gloucestershire, Captain George Augustus Graham, resurrected the ‘Irish wolfhound’ by breeding what he thought was a wolfhound of some kind with Scottish deerhounds. Today’s population of Irish wolfhounds comes from a very small group of ancestors so that, like many breeds, they are inbred. And while this helps to maintain the characteristics of the breed, it also increases the risk of particular diseases with a strong genetic component. Around 40 per cent of Irish wolfhounds suffer from some form of heart disease, and 20 per cent from epilepsy. They’re not the only pedigree with problems. Many dog breeds plummeted to near-extinction in the twentieth century, during the world wars, and were resurrected by outbreeding with other types of dog. Very strict breeding since then has produced extremely inbred populations, with little genetic diversity within breeds and an increased risk of diseases – ranging from heart disease and epilepsy, to blindness and particular cancers. Specific breeds are predisposed to certain afflictions: Dalmatians have a high risk of deafness; Labradors often suffer from hip problems; cocker spaniels are prone to developing cataracts.