john hawks weblog

paleoanthropology, genetics and evolution

domestication

  • 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

    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

    Synopsis: 
    A paper finds evidence of recent selection on starch digestion in dog domestication.
  • Mailbag: The Eemian: what gives?

    Wed, 2012-10-31 21:12 -- John Hawks

    I wandered into your site after searching for Eemian and human evolution.

    The general consensus is that anatomically modern humans were in Africa 150-200K year ago. During the Eemian interglacial these humans presumably had similar opportunities to migrate and develop agriculture as humans did during the Holocene. Yet apparently they didn't.

    Do have any thoughts on why this is so?

    Of course, a smaller population base at the beginning of the Eemian than at the beginning of the Holocene might account for this but I would think that with favorable climatic conditions a small population at the start would rapidly increase.

    Another reason might be that anatomically modern humans at the beginning of the Eemian lacked something in the neurological wiring to build modern culture.

    Thanks for writing. Indeed, this very question has interested archaeologists for a long time. The multiple independent origins of domestication and agriculture seem to have a demographic explanation. That means that the Eemian, with its environmental profile so similar to the Holocene, might be expected to have given rise to the same events. Surely Eemian west Asia was more similar to Holocene west Asia than the latter was to Holocene Mexico.

    Archaeologists' explanations are basically as you describe, although I could add a few:

    1. Maybe the Eemian wasn't really so similar to the Holocene, despite appearances.
    2. The technology in pre-Eemian times may not have allowed population growth in response to the ameliorating climate to the extent that Upper Paleolithic-era technologies did prior to the Holocene.
    3. The cognitive abilities of Eemian-era humans may not have enabled effective response to changing climate.
    4. The cultural systems of pre-Eemian times may have been more highly based on population regulation/limits to growth, thereby enabling the population to respond without the overgrowth that necessitated sedentism and ultimately domestication of plants.
    5. Demographic intensification in Africa and resulting mass migration DID happen in the Eemian, and we call this the out-of-Africa event.

    I will note that there is now some evidence of intensive collection of cereals in tropical Africa before the Eemian, so this problem may yet become more complex. One of the reasons I follow the Holocene domestication literature so closely is to try to perceive what social dynamics were shared among terminal Pleistocene peoples -- because some critical factors must have been absent pre-Eemian, but we don't know which!

  • Link parade

    Fri, 2012-10-19 22:02 -- John Hawks

    Here are some stories to entertain, amuse, or depress:

    Bryan Gardiner in Wired Science profiles professional glassblowers who are dedicated to making anatomical models: "Heart of Glass: The Art of Medical Models". The products are beautiful and educational in a way computer models cannot match.


    "The detection of interstellar boron sulfide" blog has "A Motivational Correspondance" from a department's astronomy faculty to their graduate students. I can't believe that it's not a parody (although it is presented as serious) because the whole thing would be such a fat target for a lawsuit.

    First, while some students are clearly putting their hearts and souls into their research, and spending the hours at the office or lab that are required, others are not. We have received some questions about how many hours a graduate student is expected to work. There is no easy answer, as what matters is your productivity, particularly in the form of good scientific papers. However, if you informally canvass the faculty (those people for whose jobs you came here to train), most will tell you that they worked 80-100 hours/week in graduate school. No one told us to work those hours, but we enjoyed what we were doing enough to want to do so. We were almost always at the office, including at night and on weekends. Nowadays, with the internet, it is fine to work from home sometimes, but you still miss out on learning from and forming collaborations with other graduate students when everyone does not work in the same place at the same time.


    From Nature News: "Rejection improves eventual impact of manuscripts". Apparently, articles average more citations when they get bumped from one journal and published in a different journal, irrespective of whether they get published in a higher-impact or lower-impact journal. For all those who have been tweeting the link, do note that the study has a fairly obvious bias: papers that get bumped and then never published aren't counted...


    The Archaeobotanist has a detailed critique of the recent rice domestication paper: "A genome map that is not a map of origins (Rice Genetics Watch returns)". Many of the issues that are problematic in identifying "rice origins" are also problems for identifying human migrations:

    The authors have concluded the the closest wild ancestors to cultivated rice are living wild populations in the Pearl River basin. The problem is that rice was domesticated not from living population but from past populations almost certainly from regions where wild rice is no extinct (technically, we would say, extirpated). This study demonstrated that big science and lots of resources do not inevitably produce answers, but that nuanced analysis and critical thinking, and in this case some knowledge of Chinese history, are necessary to direct analyses.

    The post's final paragraph discusses the use of archaeological evidence as a reality check on the genetics. I don't have any commitment on rice domestication, but the arguments presented here must be understood.


    Clay Shirky in Poynter discusses the media's loss of "trust": "Shirky: ‘We are indeed less willing to agree on what constitutes truth’".

    Consider three acts of mainstream media malfeasance unmasked by outsiders: Philip Elmer-DeWitt’s 1995 Time magazine cover story that relied on faked data; CBS News’s 2004 accusations against the President based on forged National Guard memos; and Jonah Lehrer’s 2011 recycling and plagiarism in work he did for the New Yorker and Wired. In all three cases, the ethical lapses were committed by mainstream journalists and unmasked by outsiders working on the Internet, but with very different responses by the institutions that initially published the erroneous material.

    I don't endorse Shirky's conclusions but the essay is thought-provoking.


    Time magazine's "Moneyland" site has an article by Dan Kadlec: "Why College May Be Totally Free Within 10 Years". The more interesting exchange occurs near the end, where he quotes former Harvard president Lawrence Summers:

    There is a reason that people pay a lot of money to go to an event like the Super Bowl when it is free on TV, Summers offers. They get more out of it by being present. Something similar is true of an on-campus education, where you may attend extra-curricular events and engage more fully with faculty and other students.

    "Unbundling" college -- in the sense of unbundling a cable TV package -- is an interesting analogy raised in the article. I have heard a high-level college administrator make the same argument, that our students enjoy their campus experience and don't want to finish college sooner. I couldn't help but respond to this argument on the spot: If we allow students to spend less time on campus, we can open the educational experience to more students, including many who can't afford to spend four years marking time.


    John T. Tierney in The Atlantic: "AP Classes Are a Scam".

    The traditional monetary argument for AP courses -- that they can enable an ambitious and hardworking student to avoid a semester or even a year of college tuition through the early accumulation of credits -- often no longer holds. Increasingly, students don't receive college credit for high scores on AP courses; they simply are allowed to opt out of the introductory sequence in a major. And more and more students say that's a bad idea, and that they're better off taking their department's courses.

    I have some experience working with the new AP biology guidelines, which were formulated following the "Vision and Change" document from the National Academies, and is guiding biology education reform at both secondary and undergraduate levels. So I don't agree with Tierney's criticisms about the "stultification" of the curriculum. But it is clear that AP courses are not treated with any consistency by universities, and results in other disciplines vary widely.

  • 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.
  • Rapid adaptation to captivity in salmon

    Wed, 2011-12-21 13:15 -- John Hawks

    I just want to note this study by Mark Christie and colleagues [1] because it is such a clear demonstration of powerful selection working on standing variants in association with domestication. Rachel Newer has a good description of the study in the New York Times Green blog. Here's the study's abstract:

    We used a multigenerational pedigree analysis to demonstrate that domestication selection can explain the precipitous decline in fitness observed in hatchery steelhead released into the Hood River in Oregon. After returning from the ocean, wild-born and first-generation hatchery fish were used as broodstock in the hatchery, and their offspring were released into the wild as smolts. First-generation hatchery fish had nearly double the lifetime reproductive success (measured as the number of returning adult offspring) when spawned in captivity compared with wild fish spawned under identical conditions, which is a clear demonstration of adaptation to captivity. We also documented a tradeoff among the wild-born broodstock: Those with the greatest fitness in a captive environment produced offspring that performed the worst in the wild. Specifically, captive-born individuals with five (the median) or more returning siblings (i.e., offspring of successful broodstock) averaged 0.62 returning offspring in the wild, whereas captive-born individuals with less than five siblings averaged 2.05 returning offspring in the wild. These results demonstrate that a single generation in captivity can result in a substantial response to selection on traits that are beneficial in captivity but severely maladaptive in the wild.

    We have few cases of new or recent domestication, so this kind of experiment is hard to do in other contexts. Also, in this case the selection is "natural-looking", imposed by the captive environment in some way, instead of directly applied by culling undesirable individuals. In most cases of mammal domestication, the wild relatives are either now vanishingly rare, or have been potentially influenced by introgression from the domesticated population. But I think it's reasonable to hypothesize that the additive variation in behavioral traits in wild populations is large enough to have allowed early mammalian domesticates like dogs and horses to adapt to captivity almost as fast as the salmon. Notice that the key element here is high reproduction in captivity, and in the salmon that trait covaries negatively with success in the wild.

    Domestication may not have been a "hump" that humans brought wild animal populations over; it may have been a valley that trapped once-wild animals into dependence on humans.


    References

    1. Christie MR, Marine ML, French RA, Blouin MS. Genetic adaptation to captivity can occur in a single generation. Proceedings of the National Academy of Sciences of the United States of America. 2011.
  • Potato sack race

    Fri, 2011-10-28 14:30 -- John Hawks

    Smithsonian magazine has a very nice article by Charles C. Mann, "How the Potato Changed the World", focusing on the effects of the Columbian exchange on Europe.

    “For the first time in the history of western Europe, a definitive solution had been found to the food problem,” the Belgian historian Christian Vandenbroeke concluded in the 1970s. By the end of the 18th century, potatoes had become in much of Europe what they were in the Andes—a staple. Roughly 40 percent of the Irish ate no solid food other than potatoes; the figure was between 10 percent and 30 percent in the Netherlands, Belgium, Prussia and perhaps Poland. Routine famine almost disappeared in potato country, a 2,000-mile band that stretched from Ireland in the west to Russia’s Ural Mountains in the east. At long last, the continent could produce its own dinner.

    When I toured through the Altai this summer, I was impressed at the healthy potato patch outside nearly every house. How unlikely it seems that this American crop should have become a central part of people's lives in some of the most remote parts of Central Asia.

  • 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.

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Neandertals

For years, I've worked on their bones. Now I'm working on their genes. Read more about the science studying these ancient people.

Denisova

From a finger bone of an ancient human came the record of a completely unexpected population. My lab is working on the science of the Denisova genome.

Acceleration

The advent of agriculture caused natural selection to speed up greatly in humans. We're uncovering some of the ways that populations have rapidly changed during the last 10,000 years.

Malapa

Just outside Johannesburg, the Malapa site is producing some of the most exciting finds in human evolution. This site is the headquarters of the Malapa Soft Tissue Project.