Red Fox Genome Is Sequenced

The Russian farmed fox experiment is yielding interesting results—about foxes.

Posted Aug 26, 2018

With August wearing down and National Dog Day looming. I was determined finally to write something on a study of the dogs of Native Americans before and after “Contact,” which appears to be a nice word for “Conquest,” that had appeared in Science magazine in early July.  The paper is such a directionless muddle that I was having a hard time deciding where to begin when there flashed across my computer screen notification that Nature Ecology and Evolution for August was publishing a comparison of the recently completed sequence of the red fox genome and comparison of it to genomes from the so-called farm  fox experiment begun nearly sixty years ago by Dmitri Belyaev at the Institute of Cytology and Genetics of the Russian Academy of Sciences in Novosibirsk, Siberia.

Amy Bassett and JAB Canid Education and Conservation Center
Russian domesticated fox
Source: Amy Bassett and JAB Canid Education and Conservation Center

There in 1959, Belyaev started breeding a line of “tame” silver foxes, a variety of red fox, in order, he said, to uncover the genetic basis of domestication, especially of wolves to dogs.  Belyaev declared the foxes “virtually wild,” even though they had been captive bred at a fur farm for a number of years.  In the late 1960s, he started breeding another line of foxes solely for “aggression” toward humans. That line was supplemented in the 1990s by foxes drawn from the pool population, called “normal” that was breeding freely.  Following protocols established to guarantee that the only grounds for breeding foxes was their “tameness” or later their “aggressiveness,” Belyaev was declaring a major success in producing doglike foxes by the eighth generation—that is tame foxes who would actively seek the attention of strangers approaching their cage.

The claims immediately became headline news as science journalists and some scientists made the trek to Siberia to announce that the question of how wolves became dogs had been answered once and for all: They domesticated themselves.  According to this theory, wolves feeding on the trash heaps of Mesolithic villagers interbred until they became tame around people—that is they would not stop eating or run away if discovered at the dump. These interbreeding dump-divers would take on the behavioral characteristics and appearance of juvenilized wolves. They were insatiable attention seekers, although whether they would tolerate being hit without fighting back, the way some dogs will, is unclear. ‘Some of the foxes, but not all, had floppy ears; piebald coats; shortened, widened snouts on narrower skulls; and curled tails, among other morphological and behavioral changes—tameness, for example—that seemed common to all domesticated versions of a wild species. Thus, the farm fox experiment was interpreted to prove that humans had nothing to do with creation of the dog. Rather, the dog was a gift—a wild species that colonized a new humanmade ecological niche by natural selection and then turned its fate over to our forebears.

The dog fell into our laps, so to speak and all we had to do was figure out what to do with its wolfish talents, which we purportedly found threatening That there was little physical evidence to support this argument by analogy and that in fact what evidence did exist seemed to refute it mattered little to those who took this narrative as received wisdom.  For example, the ‘tame’ foxes were larger than the randomly bred controls rather than smaller, as predicted; they did not bark (the aggressive foxes did); and they did not come into estrus twice a year, as expected.  That not all dogs had piebald coats, curled tales and floppy ears mattered little to fans of the farm fox.  That the same could be said of the farm foxes mattered even less.

More significant, Belyaev and his followers recognized that the farm fox experiment involved rigorous, intensive selection by humans of which foxes would breed, whereas those who saw emergent dogs in the foxes insisted that there was no human involvement in their initial evolution.   Since there simply is no way around that fact of intensive human selection in the farm fox experiment, proponents of self-domestication ignore it and instead fall back on the equally spurious argument that wild wolves were always the enemy of humans and had to change their nature to become human’s best friend.

The alternative to that theory–that that dogs resulted from a dynamic process of mutual discovery and assistance involving two species who were similar in so many ways that it would have been more shocking had they not gotten together—was not as simple and contrarian. There is pleasure to be had in striking a blow against human exceptionalism by arguing that humans had no responsibility for creation of their best friend, but there are better ways to make that case than by promoting an alternative myth.

It has become clear as well that dogs emerged in the camps of Paleolithic hunters and gatherers, not the villages of proto farmers, and it is unlikely that those bands generated enough waste to support a population of incipient dogs.  Other problems with using the foxes as a cutout for dog domestication were readily apparent to anyone who looked.  But few of its believers bothered to look.  Unable to produce solid evidence, most proponents of dump diving have simply fallen back on restating their theory as fact.  (Anyone interested in more details can check my earlier blogs on the subject.)

Now compliments of Nature Ecology and Evolution comes a report on the fully sequenced red fox genome and the use of ten sequenced genomes from each of the three farm fox groups—“tame,” aggressive,” and “normal”—to look for genomic regions associated with tame and aggressive behaviors.  The scientists involved in this project hoped those gene-holding regions would lead them to the genes involved in domestication of the fox and by extension dogs and even people.  But this time, although the grandiose claim of recreating the process of domestication from wolves to modern dogs remains in place, it is qualified by talk of the difficulties arising in part from the differences between foxes and dogs. Those include the number and types of chromosomes that make it difficult to align the two genomes for comparative purposes, writes lead author Anna V. Kukekova of the University of Illinois, Urbana-Champaign.   They are different behaviorally as well, she writes: “Unlike modern dogs, which have been selected for a wide variety of traits, these fox strains were selected solely for [a single] behaviour ….”

This study was widely reported, especially regarding its identification of a variation in SorCS1, a gene associated with protein trafficking and sorting, synapse plasticity, memory, and learning, in tame foxes and two aggressive foxes. They also searched for genes  thought to play a role in domestication of cats, rabbits, and dogs that are associated in humans with conditions like bipolar disorder and schizophrenia.   Yet the study also produced a cautionary note with regard to the association of human mental and developmental disorders with dog domestication.  In this case, the researchers looked for the variations in the genes associated with Williams syndrome— a developmental disorder in humans characterized in some cases by hypersociability.   Last year Bridgett vonHoldt, a canine  geneticist at Princeton, found the genetic variant believed involved Williams syndrome in dogs and posited that it potentially played a role in dog domestication. (See blog from last year.)

Kukekova and her colleagues found the variant genes in the aggressive foxes, not the tame ones, as expected.   In a press release from the University of Illinois at Urbana, Champaign, Kukekova expressed surprise at the findings and said they indicate how complex the genetics of behavior—and domestication—can be.

Generally ignored in this discussion as in other papers on the farm fox experiment, is a looseness of language. Not considered, for example, is the possibility that the aggressive foxes have an exaggerated fear response, so that they attack because they are unable to escape their cages and flee the approaching threat, whereas reduced fear response might be at work in the “tame” foxes.  Without precise definitions, observers are left to speculate.  In their new book, The First Domestication, Raymond Pierotti and Brandy Fogg, observe that “the Russian study involved intense selection on a presumed single trait—sociability or ‘tameness’—which actually turned out to be a complex of traits involving life history, physiology, anatomy, and behavior.”  At a more fundamental level, sociable is not a synonym for tame. 

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