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Man’s new best friend? A forgotten Russian experiment in fox domestication

The views expressed are those of the author and are not necessarily those of Scientific American.


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Dmitri K. Belyaev, a Russian scientist, may be the man most responsible for our understanding of the process by which wolves were domesticated into our canine companions. Dogs began making for themselves a social niche within human culture as early as 12,000 years ago in the Middle East. But Belyaev didn’t study dogs or wolves; his research focused instead on foxes. What might foxes be able to tell us about the domestication of dogs?

Domesticated animals of widely different species seem to share some common traits: changes in body size, in fur coloration, in the timing of the reproductive cycle. Their hair or fur becomes wavy or curly; they have floppy ears and shortened or curly tails. Even Darwin noted, in On the Origin of Species, that “not a single domestic animal can be named which has not, in some country, drooping ears.” Drooping ears is a feature that does not ever occur in the wild, except for in elephants. And domesticated animals possess characteristic changes in behavior compared with their wild brethren, such as a willingness or even an eagerness to hang out with humans.

Belyaev and other Soviet-era biologists looked around at domesticated dogs, a species they knew had descended from wolves, and were puzzled. They could not figure out what mechanism could account for the differences in anatomy, physiology, and behavior that they saw in dogs, but they knew that they could find the answers in the principles of Mendelian inheritance. At that time in Stalinist Russia, however, Lysenkoism was state doctrine, and biologists were unable to carry out the research necessary to investigate these questions.

In the late 1920s and early 1930s, Trophim Lysenko, an agronomist with a peasant upbringing, claimed to have invented a new farming technique that could triple or even quadruple crop yields. Lysenko’s illegitimate science held that the acquired characteristics of a plant could be inherited by its offspring. Despite the fact that his technique, called vernalization, was neither new nor effective, Lysenko quickly rose through the hierarchy of the Communist Party in the Soviet Union. The Communist officials thought that if the peasants could be motivated to cultivate grains, no matter the reason, this was a positive change from the earlier days when peasants eagerly destroyed crops to keep them from the Soviet government. For this reason, while biologists were investigating the genetics of the fruit fly Drosophila melanogaster, Lysenko’s appeal to party officials was his ability to involve peasants in an “agricultural revolution.” From his position of power, Lysenko was able to pit classical geneticists against the Communist Party.

Lysenkoism was of course directly in contrast to Mendelian genetics, which declared that acquired characteristics could not be genetically passed down to offspring; the unit of inheritance was the gene, and not experience. But the slow work of academic science and genetics couldn’t provide the Communists with the same sort of political gain and therefore simply couldn’t compete with Lysenko’s non-science. Genetics was branded a “fascist science,” perhaps because of the way that Nazi Germany attempted to leverage genetics and eugenics in their attempt to build a master race. In the mid to late 1930s, many geneticists were executed or sent to labor camps. In 1948, genetics was officially declared a pseudoscience, resulting in the firing of all geneticists from their jobs.

It was in this political environment that Belyaev lost his job at the Department of Fur Animal Breeding at the Central Research Laboratoryin Moscow, because of his commitment to classical genetics. Belyaev continued to discreetly study genetics, however, by overtly studying animal physiology throughout the 1950s. In 1959, after Nikta Khrushchev rose to power and began to reverse the Communist scientific policies, Belyaev became of the director of the Institute of Cytology and Genetics of the Russian Academy of Sciences, in Novosibirsk, Russia, a post he retained until his death in 1985.

Belyaev hypothesized that the anatomical and physiological changes seen in domesticated animals could have been the result of selection on the basis of behavioral traits. More specifically, he believed that tameness was the critical factor. How amenable was an animal to interacting with humans?

Belyaev wondered if selecting for tameness and against aggression would result in hormonal and neurochemical changes, since behavior ultimately emerged from biology. Those hormonal and chemical changes could then be implicated in anatomy and physiology. It could be that the the anatomical differences in domesticated dogs were related to the genetic changes underlying the behavioral temperament for which they selected (tameness and low aggression). He believed that he could investigate these questions about domestication by attempting to domesticate wild foxes. Belyaev and his colleagues took wild silver foxes (a variant of the red fox) and bred them, with a strong selection criteria for inherent tameness.

Starting at one month of age, and continuing every month throughout infancy, the foxes were tested for their reactions to an experimenter. The experimenter would attempt to pet and handle the fox while offering it food. In addition, the experimenters noted whether the foxes preferred to hang out with other foxes, or with humans.

Then, upon reaching sexual maturity (seven to eight months), they had their final test and assigned an overall tameness score. They rated each fox’s tendency to approach an experimenter standing at the front of its home pen, as well as each fox’s tendency to bite the experimenters when they tried to touch it. Only those foxes that were least fearful and least aggressive were chosen for breeding. In each successive generation, less than 20 percent of individuals were allowed to breed. Belyaev then began breeding a line of foxes with the opposite behavioral traits, to be fearful and aggressive, using a similar method. To ensure that tameness resulted from genetic selection and not simply from experience with humans, the foxes were not trained and were only allowed short "time dosage" contact with their caretakers and experimenters.

The result of this breeding program conducted over more than 40 generations of silver foxes was a group of friendly, domesticated foxes. These domesticated foxes, which were bred on the basis of a single selection criteria, displayed behavioral, physiological, and anatomical characteristics that were not found in the wild population, or were found in wild foxes but with much lower frequency. One of the reasons that these findings were so compelling was that the criterion used to determine whether an individual fox would be allowed to breed was simply how they reacted upon the approach of a human. Would they back away, hissing and snarling, and try to bite the experimenter? Or would they approach the human and attempt to interact?

The domesticated foxes were more eager to hang out with humans, whimpered to attract attention, and sniffed and licked their caretakers. They wagged their tails when they were happy or excited. (Does that sound at all like your pet dog?) Further, their fear response to new people or objects was reduced, and they were more eager to explore new situations. Many of the domesticated foxes had floppy ears, short or curly tails, extended reproductive seasons, changes in fur coloration, and changes in the shape of their skulls, jaws, and teeth. They also lost their "musky fox smell."

The first physiological change detected was in the hypothalamic-pituitary-adrenal axis. This system is responsible for the control of adrenaline, which is a hormone that is produced in response to stress, and controls fear-related responses. The domesticated foxes had significantly lower adrenaline levels than their undomesticated cousins. The researchers hypothesized if the foxes were not afraid of humans, they would produce less adrenaline around them. This explains the foxes’ tameness, but it doesn’t account for their changed fur coloration patterns. The scientists initially theorized that adrenaline might share a biochemical pathway with melanin, which controls pigment production in fur. Further research has since supported this initial hypothesis.

And so it was that selecting for a single behavioral characteristic— allowing only the tamest, least fearful individuals to breed—resulted in changes not only in behavior, but also in anatomical and physiological changes that were not directly manipulated.

More than 50 years have passed since Belyaev began his silver fox breeding program, and research with these foxes continues to uncover the genetic changes that occur with consequences for physiology, anatomy, behavior, and cognition, as a result of the process of domestication, though on a smaller scale. 1n 1996, the breeding population contained 700 individuals, but by 1999, it was down to 100. Because of the realities of the Russian economy and the shortage of funding for science, in order to maintain the research, some foxes had to be sold for fur, and some are now being sold as pets. Of course, domestic foxes aren’t domestic dogs. But by being raised in households as pets, with similar upbringing as dogs, these foxes could provide us with a sort of natural experiment by which we can even better understand the ancient relationship between man and man’s best friend.

Want to see videos of the different responses of the domesticated and aggressive foxes upon the approach of a human experimenter? Check them out here. 

ABOUT THE AUTHOR

Jason G. Goldman is in his fourth year as a doctoral student in developmental psychology at the University of Southern California. His research focuses on the evolution and architecture of the mind and how different early experiences might affect innate knowledge systems. To investigate these issues, he conducts studies in three populations: human adults, nonhuman adult animals, and nonhuman infant animals. Studies of each population allow unique questions to be asked about the evolution and development of cognition. He is also psychology and neuroscience editor at ResearchBlogging.org and is the editor of the 2010 edition of Open Lab, the yearly anthology of the best science writing on the web. He writes the Thoughtful Animal blog.

Image of Belyaev and his foxes; source unknown but probably from the Belyaev lab.

The views expressed are those of the author and are not necessarily those of Scientific American.






Comments 38 Comments

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  1. 1. mtntennispro99 10:48 am 09/6/2010

    Fascinating article. Makes sense to me that foxes can be domesticated. Not pleasant to be reminded how politics in the former Soviet Union crushed scientific research.

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  2. 2. doug l 11:02 am 09/6/2010

    Care to speculate whether something similar would happen if we trid this with coyotes? Or even more interesting, if we could do this with chimps.

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  3. 3. Evil_Si 12:09 pm 09/6/2010

    Good article – hardly a "forgotten" experiment though as readers of Richard Dawkins will be well aware!

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  4. 4. theDangerousQuestion 12:15 pm 09/6/2010

    Cats don’t have floppy ears. Does this mean they are not domesticated?

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  5. 5. jtdwyer 1:19 pm 09/6/2010

    doug l – Interesting thought, but it seems to me that human civilizations have been effectively domesticating their members for many thousands of years, with varying degrees of success…

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  6. 6. jasongoldman 1:42 pm 09/6/2010
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  7. 7. jasongoldman 2:10 pm 09/6/2010

    Evil_SI: Indeed, not exactly forgotten, but not exactly well-known either. "A mostly-unknown experiment" wouldn’t have been quite as snappy a title :-)

    Doug 1: One one hand, it might make sense that a species in which some subset of individuals weren’t afraid or anxious around humans could be domesticated. And in the early days of Belyaev’s research, he had some success with minks and river otters, in addition to foxes. There is also now a group of domesticated rats collaboratively studied by the Belyaev lab and a group at Max Planck, who are trying to uncover the molecular genetic bases of domestication.

    theDangerousQuestion: not being a cat person (i’m very allergic) i can’t directly say, but my understanding is domesticated cat ears are floppier, even if not totally droopy. i imagine there’s some variation within and between breeds.

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  8. 8. Spear_Wolf 2:37 pm 09/6/2010

    doug l: Coyotes are very, very closely related to wolves. I’ve even heard some go as far to claim that they might be the same species, just different breeds of the same species in the same way that there’s different breeds of the same species of dogs or house cats. Based on this, it’s a pretty easy assumption that the same thing would most likely happen with coyotes.

    theDangerousQuestion: Some cats DO have floppy ears. For example, the Scottish Fold.

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  9. 9. Spear_Wolf 2:39 pm 09/6/2010

    doug l: Coyotes are very closely related to wolves. I’ve even heard some go as far to say that they’re the same species, only different breeds, much in the same way that cats and dogs are all the same species with large variations of differences from the various breeds. Based on this, I would assume that the same thing would happen with coyotes as what happened with wolves and with the foxes mentioned in this article.

    theDangerousQuestion: Some cats DO have floppy ears. For example, the Scottish Fold.

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  10. 10. rickofudall 11:07 pm 09/6/2010

    Rather than work with coyotes, why not work with Jindo dogs? As the oldest line of dogs with an unbroken heritage, one can look at a domestication regimen that is almost completely different from that of other breeds but still retains the wild "self programming" ability.

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  11. 11. Fairportfan 11:36 pm 09/6/2010

    The Scottish Fold is an aberration – and the ears of most domestic cats are no more floppy than those of their wild cousins.

    SA ran an article a couple of years back about the probable beginnings of cats living with humans, and the average domestic shorthair doesn’t look all that different from the Middle Eastern wildcats that appear to have been the first to domesticate humans.

    And, yes, that’s a cat-owner’s joke, but it’s very likely true – cats first moved into human society (and domiciles) because human agriculture and grain storage attracted easy prey for them, and it’s probable that the "domestication" of cats was about fifty-fifty, with each side bringing something useful to the other to the deal.

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  12. 12. Fairportfan 11:47 pm 09/6/2010

    I suspect that Darwin (like many Englishmen of his age) did not consider cats "proper domestic animals" because they’re lazy and sneaky and won’t come when called, not subservient, loyal and brave, like a proper pet like a dog.

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  13. 13. SHAWAM!!! 12:44 am 09/7/2010

    My 3 year old Tuxedo cat may be lazy and sneaky at times (just like any dog) but he always comes to me when I call him, he’s very subservient to me, and he’s very loyal to me. As a matter of fact, he’s the most dog-like cat I’ve ever seen. He licks my hands and face, rolls over at my feet, loves to lie on his back and expose his tummy for a belly rub, and he does tricks for his treats.

    And as for cats not being brave, I’ve seen cats attack and scare off dogs five times their own size. I used to have a roommate with a dog and my cat would regularly attack it and send it running with its tail between its legs. Oh, and unlike a dog, I can leave my plate of food unattended around my cat and not have to worry about him stealing my food while I’m gone. I suspect that you just don’t know very much about cats.

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  14. 14. Apolloz 4:11 am 09/7/2010

    theDangerousQuestion : humans didn’t domesticate cats, Rather cats domesticated humans =]

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  15. 15. Forlornehope 5:59 am 09/7/2010

    It is interesting that Dawkins rather plays down the role of Mendel in the understanding of evolution. Perhaps this has something to do with a fact that may have influenced the Soviets. Mendel, as is well known, was a monk who only gave up his scientific work when he became abbot. Like many gifted scientists he ended up as an administrator!

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  16. 16. MCMalkemus 6:50 am 09/7/2010

    Indeed. It is disturbing.

    Reminds me of the new ‘Lysenkoism’ currently happening in the US to squelch research efforts in stem cells, sway the general non scientific public away from the findings of climatic scientists, etc, etc.

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  17. 17. David N'Gog 8:06 am 09/7/2010

    Humans had pointy ears like elves until they were domesticated by cats.

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  18. 18. glengach 11:12 am 09/7/2010

    My father and I dug a runt/abandoned coyote pup out of a den in 1990. We initially thought it would die before we even made it back to the house, but he miraculously survived. That puppy was raised by a beagle and was my loving companion for almost 17 years. He never showed any aggression towards a human, and his favorite greeting for strangers was a lick in the face.

    I do not think it would take many generations to replicate the fox experiment’s outcome with coyetes.

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  19. 19. SteveinOG 12:05 pm 09/7/2010

    One difference between dogs, domesticated from wolves, and all the other animals discussed here (including foxes) is that wolves are social animals and have a pack mentality. When raised by humans, they seem to assume they are part of the human pack, which they seek to please, and aggressively defend. I think that is the main reason why dogs are so widely domesticated and live in our homes, rather than our barns.

    Cats are a completely different case. They were allowed to be around the home for pest control reasons. My observation is that people like to project dog-like behavior on them, but they actually behave quite differently: for their own benefit rather than that of the family (or pack.)

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  20. 20. David N'Gog 1:35 pm 09/7/2010

    There is a difference between dogs and cats obviously- but it is a common misconception that cats are not social animals.

    They may prefer to hunt alone but feral cats will form "packs" and social bonds with other cats, generally sleeping and living together- establishing a hierarchy, etc.

    Anyone who has kept multiple cats will witness that they do socialise with each other in the home.

    Cats, like people though, get along better with some than others.

    Any two dogs kept together will almost certainly become friends. Not true with cats- they’re more picky about who becomes their "friend".

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  21. 21. SHAWAM!!! 4:08 pm 09/7/2010

    And have you ever owned a cat? What’s so altruistic about a dog wanting its belly rubbed versus a cat wanting its belly rubbed? I’ve owned many cats and many dogs and while it is generally true that cats aren’t as relentlessly affectionate as dogs are, there are exceptions to the rule. The cat I have now is very talkative and affectionate and playful. That’s not a projection of dog like behavior; that’s just plain fact.

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  22. 22. doug l 8:35 am 09/9/2010

    Thanks for your response, Jason. I had not heard of the other experiments. My question regarding selection for non-aggression might be better rephrased as selection for hormonal levels as I’ve heard that aggression is closely correlated to adreanal levels.
    And the thought experiment for primates, bonobos and chimps in particular, might be very intersting as well, though the long maturity and other ethical aspects make it unpractical, I’d think…but how about rhesus or macaques?.
    Any literature on the domesticated rats? If they are already domesticated the expression of neotony as seen in the foxes, I suspect would have already happened, but interesting none the less.
    PS…enjoy your column on SciBlogs as well. Cheers.

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  23. 23. doug l 8:41 am 09/9/2010

    My curiousity is related to a question I have as to the morphology of the brain. If we see outward changes to the selected subjects offspring, might there not also be changes we don’t see such as in brain development and hormonal expressions. One thing that seperates humans from nearly all other animals, even the ones we consider to be fairly social, is the degree to which we tolerate strangers of our own species. Is it because we simply have lower adrenal levels or could it be due to our possession of a theory of mind which grants us insight into the intent of others and therefore are not as likely to respond with defensive/aggressive behavior geared towards avoiding or overcoming a threat. In humans it appears we have both, but I wonder if self-selection might have been a mechanism that contributed to that trait’s becoming a signature characteristic of our species.

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  24. 24. mightythor 7:01 am 09/12/2010

    I’m intrigued by the exchange between SteveinOG and DavidN’Gog. There’s no question that domesticated cats do form dominance hierarchies when they live in crowded domestic (or even feral) situations. But they don’t form packs in the sense that dogs do, where the subordinate members of the pack spend nearly all their time paying attention to the alpha animal and following it around. Domesticated cats are not completely asocial but they are not as social, or at any rate not social in the same way, as dogs. Interestingly, among the large cats, lions live and hunt in packs, whereas the other large cats are mostly loners. Does anyone know where Middle Eastern wild cats, in the wild, fit on this spectrum of behavior. I’m wondering if domestic cats didn’t acquire some rudimentary social behavior as part of the process of their domestication.

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  25. 25. doug l 9:50 am 09/12/2010

    That’s an interesting observation regarding the social hierarchy of cats in the wild. Presumably that is to a large part instinctive and hard-wired, but considering the habitat of lions, living out on the savannah where their prey consists of large and potentially dangerous ungulates in an open and largely treeless landscape, having a pack might be the only way for them to fit that niche. Other cats tend to rely on singular ambush (with some notable exceptions such as with cheetahs). As to development and expression of these behavioirs, it is insterested to note that all cats are social when they are young and among their litter-mates. Adult lions seem to maintain that characteristic to a degree as it benefits them, and I seem to recall reading that tigers do too in some situations in the wild, though not to the degree that lions do. It is interesting that lion prides are formed from siblings and cousins, accustomed to being within the same pride, so their social instincts are in the wild a product of their growing up in the same structure and recognizing each other as part of that same self identity.

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  26. 26. johndavis189 2:40 am 09/13/2010

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  27. 27. huweber 6:04 pm 09/13/2010

    I like this summary of Belyaev’s neglected silver fox taming project. Yes, Richard Dawkins has described it. He may also have mentioned the appearance of blue eyes in the tame foxes. Blue eyes often occur in old dog breeds, e.g. dogs kept by Eskimos or for sheep-herding. Coyotes could probably be tamed with similar results; they can mate with dogs, I believe. In Seattle I knew a dog that was thought to have coyote genes as judged by appearance and behavior. Unlike silver foxes, coyotes don’t have commercial value and, therefore, it would be rather difficult to attract funding for a taming project.

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  28. 28. huweber 6:16 pm 09/13/2010

    Nice summary of Belyaev’s neglected research project. Yes, Richard Dawkins wrote about it. Blue eyes could be another result of taming (did Dawkins mention this?). In dogs, blue eyes often occur in old breeds such as those used by Eskimos or for herding. I’m confident that coyotes could be tamed with similar results; they are members of the dog family. Since they lack commercial value, it would be difficult to attract funding for a multi-generational funding project.

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  29. 29. ysgadbois 9:33 pm 09/13/2010

    I am not sure why Belyaev’s work is labelled a "forgotten" experiment as it is extensively cited by a many current scientists, including some that took over the research program (e.g. Trut).
    In response to one of the comments, coyotes (Canis latrans) are a different species than wolves (Canis lupus). This is not a "breed" of the same species. The Northeastern US and Easter Canada have an hybrid (see http://www.jstor.org/pss/2409486 or Kays, Curtis, Kirchman (2010) in "Biology Letters"). You may be thinking of the Red Wolf (Canis rufus) confusing status?

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  30. 30. hotblack 6:51 pm 09/17/2010

    My grandfather was a trapper in Ontario. He always had foxes as summer trail dogs. Really, really smart, personable, and very aware & responsive of human moods & behavior.

    Had a couple wolves over the years as well, but they were very needy.

    As for cats, we had a lynx one year I was there, but it was like a lion. Tame 90% of the time, but upset it, and suffer the wrath.

    There was always some animal coming or going from rescue there. Wild animals have very distinct personalities when they aren’t busy running for their lives.

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  35. 35. JDahiya 2:25 am 01/1/2011

    David N’Gog, that is one insightful comment which actually made me laugh out loud. Way to go!

    Continuing the thought, would you say Vulcans are therefore contemporary but feral (they certainly don’t act as affectionate as humans)? Elves, by all accounts other than Tolkien, weren’t a friendly and non-aggressive species. I can also see why cats also reduced the longevity of the elf species to create humans–you can’t do good breeding if the members take twice as long to mature and breed.

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  36. 36. LMac4 1:07 am 05/2/2012

    Cats and dogs followed very different paths towards domestication. Cats were utilized primarily as rodent hunters on farms to preserve the crop harvest from scavenging animals. Dogs were bred to be hunt along side humans and therefore individuals who exhibited more dependence on humans were selected for. The physical characteristics exhibited by both dogs and domesticated foxes are a by-product of selecting for neoteny – the retention of juvenile traits in adults, such as floppy puppy ears, dome shaped head, large eyes etc. The desire for animals that displayed more dependence on humans selected for these traits. Because cats were selected for jobs that involved more independence, selection was less intense which is why cats exhibit different traits of domesticity than dogs.

    The reason the cat breed Scottish folds have curved over ears is because they all descend from one litter of kittens born in the 1960s who had a genetic mutation causing folded ears. The owner decided it was cute and they were inbred extensively. In this case it isn’t really a trait linked with the domestication of the species.

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  37. 37. Delta Fox 01 2:12 pm 05/3/2012

    I honestly think this experiment back in the 50′s is the best thing in the study of how humans and animals can coincide with each other and how they both change. The ears laying down unlike the wild suggests that the animal feels safe and not having to be on alert to any sudden changes. the fur and the tails I am not so sure about why they change, but it must have something to do with the new environment and less stress. I myself am looking to own a Fennec fox in the not to distant future.

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  38. 38. LunaKay 9:45 pm 05/10/2012

    Unfortunately, the project is broke and when it needs money but can’t sell a fox as a pet, it sells them for their fur. Many states in the U.S. do not allow these animals as pets. I believe this should be changed and have created a petition to legalize domestic foxes in ALL U.S. states. The more people that can have them, the more foxes we can save. Please sign and pass along! http://www.change.org/petitions/domestic-fox-legalization

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