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paleoanthropology, genetics and evolution

dogs

  • Dog domestication complexity

    Tue, 2013-06-18 21:25 -- John Hawks

    Ewen Callaway covers the active area of dog domestication research in a new Nature News article ("Dog genetics spur scientific spat") [1].

    In recent months, three international teams have published papers comparing the genomes of dogs and wolves. On some matters — such as the types of genetic changes that make the two differ — the researchers are more or less in agreement. Yet the teams have all arrived at wildly different conclusions about the timing, location and basis for the reinvention of ferocious wolves as placid pooches. “It’s a sexy field,” says Greger Larson, an archaeogeneticist at the University of Durham, UK. He has won a £950,000 (US$1.5-million) grant to study dog domestication starting in October. “You’ve got a lot of big personalities, a lot of money, and people who want to get their Nature paper first.”

    Callaway discusses the divergent genetic results, and gives details about each successive analysis. The newest contender is a preprint by John Novembre and colleagues, which is freely available on the arXiv and discussed in a Haldane's Sieve post, which has developed a good comment stream.

    One reason these results have been fluctuating with the addition of more data is that the population history was complex, and a better representation of wolf and dog genomes adds the ability to reject simple models. As in human populations, there is no necessary reason to think that today's dog populations trace their ancestry predominantly from the earliest archaeological samples of dogs. A wider sample of ancient DNA from archaeological dogs should add much more information about the process and timing of domestication.

    References

    1. Callaway E. Dog genetics spur scientific spat. Nature. 2013;498(7454):282 - 283.
    Tags: 
    dogs
    domestication
    wolves
    ancient DNA

  • Was the first dog from the Altaian Upper Paleolithic?

    Sat, 2013-03-09 22:33 -- John Hawks

    A new paper by Anna Druzhkova and colleagues examines the ancient mtDNA sequence of a putative 33,000-year-old dog from Razboinichya Cave in the Altai region: "Ancient DNA Analysis Affirms the Canid from Altai as a Primitive Dog" [1]. The paper's analysis is a simple application of phylogeography, showing that the mtDNA of the Altai dog fits in a clade with a number of pre-Columbian New World dogs:

    The domestication of dogs from the grey wolf is well accepted [1]. However, the timing, location and number of domestication events is still actively debated [2]–[5]. The archaeological record provides unequivocal dog remains beginning about 14,000 calendar years (cy) ago [6]–[7] requiring a domestication that predates agriculture. Putative dog remains ranging in age from 31,000 to 36,000 cy [2] [8]–[9] have been questioned as potentially representing aborted attempts at domestication, or morphologically unique wolves [4]. A full mitochondrial genome analysis of modern dogs suggests an origin in southern China around 16,000 years ago [10], whereas an extensive nuclear genome-wide SNP analysis supports a Middle East and European origin [11], which is more in accordance with archaeological data. Here we isolated, sequenced and analysed 413 nucleotides of the mitochondrial DNA control region from a putative dog specimen dated as approx. 33,000 cy from the Altai Mountains in central Asia. Only a single specimen - namely the Goyet dog (36,000 cy [2]) predates the Altai dog and hence it is thus far the second oldest known specimen assigned morphologically to the domestic dog [8].

    The evidence of dog domestication has developed piecewise over the last several years. A number of Upper Paleolithic skeletal specimens have morphological dimensions inconsistent with wolves, but comparisons of the genetics of recent dogs has tended to argue against such early domestication.

    In the current paper, the mtDNA similarity of the Razboinichya canid and pre-Columbian American dogs is pretty persuasive evidence that this specimen came from an early population ancestral to the dogs of northeast Asia, which would later enter the New World. This paleontological specimen shows that the mtDNA phylogeny of modern-day dogs does go way back into the Late Pleistocene, which argues against a single recent domestication. Still, the mtDNA is not the strongest possible source of evidence, since present-day dogs can be found across many of the clades that include mtDNA from wild wolf populations.

    Curiously, Druzhkova and colleagues did not include the Goyet canids in their mtDNA comparisons. An analysis of 57-bp of the mtDNA of these dogs was carried out by Germonpré and colleagues [2], showing that the Belgian Upper Paleolithic dogs have a diverse range of mtDNA haplotypes, across several clades of the wolf genealogy. The current paper bases its mtDNA cladogram on 400-bp sequences, so they aren't strictly comparable, but it is nevertheless interesting that the other putative early dogs are not part of this clade including pre-Columbian dogs and the Altai specimen.

    The earlier description of the Razboinichya canid by Ovodov and colleagues [3] suggested that the specimen was part of an early domestication event that was "arrested" by the Last Glacial Maximum.

    We suggest that the pre-LGM Goyet and Razboinichya canids are unlikely to be the ancestors of post-LGM dogs. These canids most probably are both “proto” or incipient dogs that did not persist long enough to found enduring lineages, since no putative dog remains have been found at adjacent sites in western and central Europe and in Siberia occupied during the LGM. The ecological changes caused by progressive cooling almost certainly caused social and settlement pattern changes severe enough to have disrupted the domestication process and prevented the evolution of fully domesticated dogs.

    Such a scenario would reconcile the early skeletal evidence for dogs with the conclusion that recent dogs come from a small mtDNA population.

    But I think it's too soon to conclude that today's dogs don't have deeper Pleistocene roots. As zooarchaeologists have been finding more and more possible evidence of dogs, they may be filling in the record (for example, with apparent dogs from the Gravettian Předmostí site [4] and from the later Upper Paleolithic of Kesslerloch, Switzerland [5]). I wonder whether a good actualistic study of dog deaths and remains in small-scale human societies would give rise to clearer expectations about how many dog skeletal specimens we should expect from Upper Paleolithic contexts.

    References

    1. Druzhkova AS, Thalmann O, Trifonov VA, Leonard JA, Vorobieva NV, Ovodov ND, Graphodatsky AS, Wayne RK. Ancient DNA Analysis Affirms the Canid from Altai as a Primitive Dog Hofreiter M. PLoS ONE [Internet]. 2013;8(3):e57754. Available from: http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0057754
    2. Germonpré M, Sablin MV, Stevens RE, Hedges REM, Hofreiter M, Stiller M, Després VR. Fossil dogs and wolves from Palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes. Journal of Archaeological Science. 2009;36(2):473 - 490.
    3. Ovodov ND, Crockford SJ, Kuzmin YV, Higham TFG, Hodgins GWL, van der Plicht J. A 33,000-year-old incipient dog from the Altai Mountains of Siberia: evidence of the earliest domestication disrupted by the Last Glacial Maximum. PLoS One. 2011;6(7):e22821.
    4. Germonpré M, Lázničková-Galetová M, Sablin MV. Palaeolithic dog skulls at the Gravettian Předmostí site, the Czech Republic. Journal of Archaeological Science. 2012;39(1):184 - 202.
    5. Napierala H, Uerpmann H-P. A ‘new’ Palaeolithic dog from central Europe. International Journal of Osteoarchaeology. 2010;22(2):127 - 137.
    Tags: 
    dogs
    wolves
    domestication
    Upper Paleolithic
    Altai
    Synopsis: 
    The record of early dog domestication grows

  • Selection is for the dogs

    Wed, 2013-01-23 16:17 -- John Hawks

    I was really pleased to see the new paper by Erik Axelsson and colleagues [1] on the pattern of recent selection on domesticated dogs. As we began working on recent selection in humans, we expected that domesticated animals might exhibit similar patterns genome-wide. They are among the organisms most similar to humans in demography and ecological change: Domesticated animals have all undergone rapid shifts in diet, predator ecology and social dynamics after domestication, at the same time that they have experienced rapid increases in population size. That is a recipe for rapid adaptive evolution.

    As in humans, the paper shows that dogs were selected strongly for a new agricultural diet. Just as in humans who descend from early agriculturalists, dogs have extensive duplication of the amylase gene. Humans express amylase in saliva, but as explained in the paper dogs only produce amylase in the pancreas, where it digests starches intestinally. Where this paper gets really exciting is when the authors began to investigate the entire metabolic pathway underlying starch digestion. The amylase gene AMY2B underwent duplications similar to those in humans, and not found in wolves. Two other genes that interact in starch digestion and glucose uptake did not undergo duplication but do show near-fixed haplotypes in dogs that are absent or very rare in wolves, and the paper shows using both biochemistry and phylogenetic comparison with herbivores and omnivores that the dog versions of these genes increase enzymatic activity on starches and glucose uptake.

    In conclusion, we have presented evidence that dog domestication was accompanied by selection at three genes with key roles in starch digestion: AMY2B, MGAM and SGLT1. Our results show that adaptations that allowed the early ancestors of modern dogs to thrive on a diet rich in starch, relative to the carnivorous diet of wolves, constituted a crucial step in early dog domestication. This may suggest that a change of ecological niche could have been the driving force behind the domestication process, and that scavenging in waste dumps near the increasingly common human settlements during the dawn of the agricultural revolution may have constituted this new niche6. In light of previous results describing the timing and location of dog domestication, our findings may suggest that the development of agriculture catalysed the domestication of dogs.

    So for those of you wondering why we feed dogs kibble instead of raw beef, here's the reason.

    After finding candidate regions for selection across the genome, the authors ran a gene ontology analysis to see whether functional gene loci in these regions fall into any consistent categories. Along with the metabolic and digestive genes, they found

    The most conspicuous cluster (11 terms) relates to the term ‘nervous system development’. The eight genes belonging to this category (Supplementary Tables 7 and 8) include MBP, VWC2, SMO, TLX3, CYFIP1 and SH3GL2, of which several affect developmental signalling and synaptic strength and plasticity. We surveyed published literature and identified 11 additional CDR genes with central nervous system function (Supplementary Table 9), adding to a total of 19 CDRs that contain brain genes. These findings support the hypothesis that selection for altered behaviour was important during dog domestication and that mutations affecting developmental genes may underlie these changes7.

    That is a similar story to humans. We don't know what such genes might do, and unraveling what difference these genes may have made to behavior will take a lot of additional understanding of developmental biology. Much easier to work out what is going on when you can examine the biochemistry in vitro as with starch enzymes.

    The paper also makes clear why finding evidence of selection can be a difficult empirical problem at the moment:

    Uniquely placed sequence reads from pooled DNA representing 12 wolves of worldwide distribution and 60 dogs from 14 diverse breeds (Supplementary Table 1) covered 91.6% and 94.6%, respectively, of the 2,385 megabases (Mb) of autosomal sequence in the CanFam 2.0 genome assembly11. The aligned coverage depth was 29.8× for all dog pools combined and 6.2× for the single wolf pool (Supplementary Table 1 and Supplementary Fig. 1). We identified 3,786,655 putative single nucleotide polymorphisms (SNPs) in the combined dog and wolf data, 1,770,909 (46.8%) of which were only segregating in the dog pools, whereas 140,818 (3.7%) were private to wolves (Supplementary Table 2). Similarly we detected 506,148 short indels and 26,619 copy-number variations (CNVs) (Supplementary Files 1 and 2). We were able to experimentally validate 113 out of 114 tested SNPs (Supplementary Table 3 and Supplementary Discussion, section 1).

    If that sounds confusing, that's because it is confusing. Right now whole-genome sequencing is not yet routine, and whole-exome sequencing is not routine for creatures other than people. So maximizing the available data means working with partial genomes at varying levels of coverage, often accumulated for other purposes by other research groups using different sequencing platforms. Verifying sequence differences is not trivial. Generating a sample of gene sequences from many individuals is challenging, particularly as different individuals may be covered or not for different parts of their genomes.

    Studying selection requires a fairly large sample of genomes. This paper establishes evidence of selection on a few things in which domesticated dogs are mostly the same, and all are different from wolves. In other words, these are "complete sweeps" or "near-complete sweeps", in which a new genetic variant has become mostly fixed within the domesticated dog sample. A larger sample of dogs would be able to test selection with a broader range of strength and initial date, including "partial sweeps" and selection on standing variation that may have already existed in ancestral wolves before being subject to selection in domesticated dogs. So this paper opens a new area of inquiry on the causes of domestication without ruling out that we will discover much, much more about the history of selection in dogs.

    One really cool possibility is that we will uncover convergent or parallel patterns of selection in dogs with different geographic origins. Already we know that body size and pigmentation have been subject to selection in different dog breeds, and that single genes transferred across breeds have been important parts of that process. There are a few cases in humans where the extensive geographic dispersal of a single adaptive variant can explain the present distribution of a trait. But in many more cases, different human groups have attained traits by parallel selection on different genetic variants. Because humans control the breeding of dogs and traded dogs across long distances in historic times, we may find that dogs are much less affected by parallelism and much more by long-distance gene flow than humans. But we won't know until we put that hypothesis to the test.

    References

    1. Axelsson E, Ratnakumar A, Arendt M-L, Maqbool K, Webster MT, Perloski M, Liberg O, Arnemo JM, Hedhammar Å, Lindblad-Toh K. The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature. 2013.
    Tags: 
    dogs
    recent selection
    domestication
    positive selection
    diet
    non-primate
    Synopsis: 
    A paper finds evidence of recent selection on starch digestion in dog domestication.

  • Warp and woof

    Thu, 2012-05-24 23:44 -- John Hawks

    James Gorman stirs the pot on dog domestication, by comparing the new review article by Greger Larson and colleagues [1] with Pat Shipman's American Scientist piece [2] ("What-If and What-Is: The Role of Speculation in Science"). This is a complex story, and Gorman lines the two papers in opposition to each other -- the data-focused paper by Larson and colleagues, which ultimately has an ambiguous conclusion, opposed to the speculative paper by Shipman, with relatively little empirical data and a strong prediction.

    I won't go into the whole argument, which you can read at the link, but it boils down to whether the archaeological evidence shows early dogs or not.

    If dogs were watching us too, that would have added survival value to having a partly white eye and thus played a role in our evolution. Fair enough, but the dogs had to be there at that time when humans and Neanderthals overlapped. I asked Dr. Larson about Dr. Shipman’s essay, and I confess I expected he might object to its speculative nature. Not so. “I love speculation,” he wrote back, “I do it all the time.” And, he said of Dr. Shipman’s essay, “it’s a lovely chain of reasoning.”

    But, he said, “it begins from the premise that the late Pleistocene canid remains are dogs. And they are not.”

    I rather like the new Larson paper, but there are some weak points. Dog domestication was a complex process and ultimately we will need a lot more genetic data from zoo archaeology to sort it out.

    References

    1. Larson G, Karlsson EK, Perri A, Webster MT, Ho SYW, Peters J, Stahl PW, Piper PJ, Lingaas F, Fredholm M, et al. Rethinking dog domestication by integrating genetics, archeology, and biogeography. Proceedings of the National Academy of Sciences of the United States of America. 2012.
    2. Shipman P. Do the Eyes Have It?. American Scientist. 2012;100(3):198.
    Tags: 
    dogs
    domestication
    zooarchaeology

  • Mailbag: Dogs in Chauvet

    Sat, 2011-06-25 11:25 -- John Hawks
    Love your blog, which I stumbled across while googling for more detail on the wolf tracks in Chauvet Cave. Have been fascinated by this stuff since 1st grade, did fieldwork in high school & college, and now wish I hadn't let the dryness of academia drive me away from anthro back in Ann Arbor (not Wolpoff's fault). I still read around though; loved your take on the Clovis Comet Crap (what suckers the media are), though obviously impact events play a major evolutionary role.

    So anyhow, back to my question. Recently saw Herzog's documentary on the art in Chauvet. Having dabbled in caving during a Peace Corps Guatemala stint, I find it extremely unlikely that a wolf is going to be walking around deep in a pitch black cave by himself. To me this is potentially strong evidence if not downright proof of domestication, but I'm looking for more specifics on track layout (esp. in relation to those human child tracks) and actual location/depth within the cave (to ascertain feasibility of wild vs domesticated access). Do you have anything more on this, or could you point me towards same? Much obliged, tlc

    Thanks for the kind words!

    Pat Shipman has written about this topic quite a lot lately, she has a book out on the history of human-animal interactions. Last year she wrote about Aurignacian-era dog domestication evidence (I linked here):

    http://johnhawks.net/weblog/reviews/archaeology/upper/europe/dog-domesti...

    And I cited some of the original research here:

    http://johnhawks.net/node/1686

    The main impediment to accepting a very early domestication is the genetics; as modern dog breeds don't seem to have such a distant ancestor. But that may be due to recent gene flow among breeds and subsequent selection after domestication. At the very least, domestication was clearly early enough that dogs accompanied people to the Americas before 12,000 years ago.

    Tags: 
    wolves
    domestication
    dogs

  • Wolves in coyotes' clothing

    Thu, 2011-05-19 02:58 -- John Hawks

    Razib's post on the genetics of canids ("A map of charismatic canid genomic variation") does a nice summary of a recent paper in Genome Research, by vonHoldt and colleagues [1]. I just want to quickly point out that humans are not the only species for whom we are developing a complicated and relatively well-resolved scenario of population history. Still, the methods used in present-day studies of population structure are really "first-cut" kinds of approaches. The data have reached the point where simple models no longer fit, and that's a good thing.

    Also, there's this:

    Another interesting implication of the possibility of long term hybridization is that some of the distinctive alleles of extinct American wolf populations may now only be found in coyotes, since this species was much better at surviving human encroachment. And if wolves went extinct tomorrow, we could reconstruct them from what we find within coyotes I’d think.

    That gives me the chance to pull out my favorite quote from the famous evolutionary plant biologist G. Ledyard Stebbins [2]:

    We inevitably reach the conclusion, therefore, that introgressive genotypes not only persist indefinitely, but that also, like polyploids, they can migrate far beyond the areas in which they originated, and can actually survive after the non-introgressed parental species has become extinct.

    Theories that predict unknown facts before they can be observed are like uncut diamonds.

    References

    1. vonHoldt BM, Pollinger JP, Earl DA, Knowles JC, Boyko AR, Parker H, Geffen E, Pilot M, Jedrzejewski W, Jedrzejewska B, et al. A genome-wide perspective on the evolutionary history of enigmatic wolf-like canids. Genome Research [Internet]. 2011. Available from: http://dx.doi.org/10.1101/gr.116301.110
    2. Stebbins LG. The Role of Hybridization in Evolution. Proceedings of the American Philosophical Society. 1959;103:231–251.
    Tags: 
    population structure
    dogs
    non-primate
    wolves
    genomics

  • Mailbag: Coyote attacks

    Wed, 2010-06-02 14:12 -- John Hawks

    Sorry to interrupt the 'all Anthropoid all the time' theme going on lately but I want to get back to a subject we've discussed before (well kind of).

    Coyotes have a record in recent years of attacking and even killing people. Why do we see so few reports of wolves attacking and killing people? Seemingly it would be much easier for them. The 'yotes that killed the girl in Canada went after a full sized adult.

    Perhaps a pack of wolves would leave less evidence?

    I think first you have to correct for the fact that coyotes are around people a lot more. People who have gone places where they are likely to encounter wolves tend to be better prepared outdoorsmen, able to deal with bears.

    But maybe in addition to that, there's a pack hunting advantage. Coyotes hunt independently or in small groups and are apt to be both hungrier and more limited in range due to conflicts with neighbors. Wolves get their risk spread among more group members and maintain larger home ranges.

    I think leopards are also more dangerous to people than lions, may be the same reason.

    Tags: 
    animal attacks
    dogs
    wolves

  • The Aurignacian dogs

    Fri, 2010-05-14 14:37 -- John Hawks

    I didn't see this article when it came out but I ran across it this week: Pat Shipman writes about possible evidence for early dog domestication ("The Woof at the Door").

    Some of the earliest known art objects from Europe include the remarkable cave paintings of Chauvet Cave in France, the oldest of which were made 32,900 ± 490 years ago. None of the hundreds of glorious Chauvet paintings show wolves. However, the cave preserves something even more haunting: the footprints of a human child about four-and-a-half feet tall, as well as many footprints of large canids and bears.

    Michel-Alain Garcia of the Centre National de la Recherche Scientifique in Nanterre noticed in 1999 that one track of canid prints appears to accompany the child’s prints. These canid prints, unlike the others, have a shortened middle digit on the front paw: a characteristic of dogs. Garcia suggested that the child and dog might have explored the cave together. Charcoal from a torch the child carried is 26,000 years old.

    It's a nice article throughout, describing why some are convinced that dog domestication was Aurignacian or earlier in time. It would be interesting to see an update to the story in light of the recent description of dog and wolf genetics, that argued for a more recent domestication in the Near East. Personally I don't see a contradiction here, if we suppose that the population of dogs may have grown enormously with pastoralism in the Near East, drawing substantially upon local wolf populations. It's shaping up to be a complicated problem.

    Tags: 
    art
    Aurignacian
    dogs
    Upper Paleolithic
    domestication

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