Prehistoric DNA reveals the story of a Pleistocene survivor, the muskox


A muskox (Ovibos moschatus), photographed in Alaska. From Flickr user drurydrama.

Of all the mass extinctions that have occurred during earth's history, among the most hotly debated is the one which wiped out mammoths, saber-toothed cats, giant ground sloths, and the other peculiar members of the Pleistocene megafauna around 12,000 years ago. It was not the most severe mass extinction, not by a long shot, but unlike the end-Cretaceous catastrophe 65 million years ago there is no single "smoking gun" that can account for the pattern of extinction. Instead the Pleistocene mass extinction remains a very mysterious event, but by looking at the natural history of one of the event's survivors scientists have been able to get a better idea about how one of the suspected extinction triggers affected prehistoric mammals.

Today's populations of muskox (Ovibos moschatus) are remnants of the Pleistocene herds which were once spread all around the Arctic Circle. The shaggy bovids are survivors of the events which wiped out so many other large mammals, but this does not mean that they were immune to ecological changes that may have played a pivotal role in the extinction. As illustrated by a new paper in the journal PNAS, the changing climate had a major influence on muskox populations, and by looking at what happened to them it may be possible to understand the fate of some of their extinct contemporaries.

Naturally much of what we know about Pleistocene mammals has been derived from fossils, but the bones do not just record the anatomy of the long-dead animals. Many of the Pleistocene fossils are recent enough that at least a few snippets of DNA can be obtained from them, and experts on the Pleistocene have been increasingly bringing together the more traditional aspects of paleontology with genetics to better understand the life of the past. In the case of the muskox, the international team of researchers behind the new PNAS study looked at 682 base pairs of mitochondrial DNA obtained from 149 prehistoric muskox specimens from North America and Eurasia dated between about 57,000 years ago to the present.


A diagram of fluctuations in muskox diversity (colored waves) over time (from right to left). Each color represents a different population: blue, Greenland; red, Northeast Siberia; orange, Taimyr; green, Urals; light blue, Canada. From Campos et al. 2010.

As might be expected given the status of current muskox populations, genetic diversity among living muskox is lower than in their Pleistocene counterparts. This is not the effect of a unidirectional, gradual dwindling trend, however. Between about 60,000 and 47,000 years ago there was an increasing trend in muskox genetic diversity, but that diversity began to decline before sharply increasing again around 20,000 years ago. After that genetic diversity began to fall once more before again rising in recent times (representing the expansion of muskox to Greenland). Roughly speaking, these increases and declines in diversity track changes in muskox populations over the past 60,000 years, but what could have caused these fluctuations?

Numerous hypotheses have been forwarded to explain the Pleistocene mass extinction, but for the past forty years or so the top contenders have been human hunting or climate change. Different authorities prefer different scenarios, but until now it has been difficult to determine how these ecological changes affected populations of large mammals. In the case of the muskox, the fluctuations in their genetic diversity do not appear to be tied to the arrival of human hunters in their habitats but to changes in climate.

As the authors of the new study point out, muskox live in cold, dry habitats in which the snow is just shallow enough for them get to the forage underneath it. These habitats can be greatly affected by shifts in climate, however, and naturalists have observed some populations decline by as much as 76% in a single year due to such changes. While the scientists behind the new study acknowledge that the muskox population dynamics and global climate models cannot yet be brought together to rigorously test the idea, from what is presently known it appears that the peaks in muskox genetic diversity match up with periods of global cooling. When things were cold and dry muskox genetic diversity went up, and when things got warmer (during interglacials such as the one we're in) their genetic diversity went down. There is no indication that the activities of humans were responsible for these trends. As the authors conclude, "although humans may have played a significant role in the history of other large Beringian mammalian herbivores, to our knowledge this example is unique in showing there is no evidence that humans drove musk ox demographic fluctuations over the last 60,000 years."

By itself this finding does little to resolve the ongoing (and sometimes acrimonious) debate over whether climate change or the depredations of humans were more important in driving Pleistocene mammals to extinction, but it does raise several interesting points. The most obvious is that we now know that not all large Pleistocene mammals were significantly affected by human hunting during the past 60,000 years, and, perhaps more importantly, by looking at preserved DNA from multiple populations scientists have found a way to document fluctuations in genetic diversity during prehistory. If this approach can be married to studies of paleoclimate and archaeology then we can better understand how populations of large mammals were affected by different ecological events. Combined with other new techniques, such as the ability to retrieve preserved DNA directly from soil, paleontologists will be more able to put hypotheses about what caused the Pleistocene mass extinction to the test.

Campos, P., Willerslev, E., Sher, A., Orlando, L., Axelsson, E., Tikhonov, A., Aaris-Sorensen, K., Greenwood, A., Kahlke, R., Kosintsev, P., Krakhmalnaya, T., Kuznetsova, T., Lemey, P., MacPhee, R., Norris, C., Shepherd, K., Suchard, M., Zazula, G., Shapiro, B., & Gilbert, M. (2010). Ancient DNA analyses exclude humans as the driving force behind late Pleistocene musk ox (Ovibos moschatus) population dynamics Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.0907189107

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"When things were cold and dry muskox genetic diversity went up, and when things got warmer (during interglacials such as the one we're in) their genetic diversity went down."

Because human predation pressure in the far North was greater during orbitally forced interstadials. Look at when musk oxen populations declined & extinction ensued in the Palearctic: about the time when invention of the eyed needle allowed human penetration of the "Cold Wall." Musk oxen persisted in Greenland because that land mass was invaded & occupied by specialist marine mammal hunting cultures. Anthropogenic Mass Extinction has been ongoing for millenia.

By darwinsdog (not verified) on 10 Mar 2010 #permalink

The most obvious is that we now know that not all large Pleistocene mammals were significantly affected by human hunting during the past 6,000 years.

Yeah that sucks. I wish they would have left a few velociraptors and T Rex around to hunt down. I would love to hunt T Rex with a 50 BMG, but I bet he wasn;t as tasty as the musk ox that was killed off in the las SIX THOUSAND YEARS just like the dinosaurs. it sucks that humans hunted them for sport and called them dragons.

By Head Hunter (not verified) on 10 Mar 2010 #permalink

I'm not sure how the conclusion follows that since diversity is linked to climate fluctuations, diversity isn't linked to human predation.

It should seem fairly obvious that when diversity and/or population size goes down due to climate change, a population will be much more sensitive to human predation. It's not either/or between predation and climate change, but how they work together to push a population hand-in-hand.

I can't imagine that human predation would be effective without the effects of climate change -- or visa versa. Megafauna went through climate cycles without massive extinctions before human predation became significant; and human predation appears to possibly cause extinction only during periods of massive climate change until the last two thousand years.

@Head Hunter - That is the most bizarre thing I have ever heard. Surely you jest? We are in agreement that dinosaur hunting would indeed be good sport, but suggesting that it actually happened is madness!

By ScienceAndHonor (not verified) on 10 Mar 2010 #permalink

darwin's pup- you seized on the exact phrases I did. puh-leeze.

I fear to read articles like this, because with few exceptions they mostly illustrate the complete inability of the authors to think. Oh, sorry- was that rude? Um; "illustrate an appalling lack of appropriate cross-disciplinary imagination". Ah, much better.

It happens constantly when paleontologists extrapolate. None of them, apparently, ever took a course in anthropology, or ecology. It correlates with climate, therefore not with human activity? My god- and this was peer reviewed? You know what that says about their peers?

My all-time fave has been the long, long discussions and fantasies about how hominids obviously had to evolve long legs, before their populations could migrate out of Africa. That one was, and still is, repeated constantly- and was dogma for decades at the Nat'l Geo, until they could publish the article about "AMAZING!" short legged hominid so far out of place.

Yup, them frogs, fungi, and trees- all had to have long legs too. (hint; "migrate" over evolutionary time, is not the same as that fascinating Discovery program about wildebeest and crocodiles.)


According to numerous accounts handed down from generation to generation, people have killed dinosaurs before. Ever hear of marco Polo? he saw a triceratops when he visited China. The Chinese were using them to pull wagons. What of all the stories of people slaying a "dragon" that looked exatly like a dinosaur? What about the cave drawings of brachiosaurus? What about rock depictions with dino sketches on them? Yep, it happened less than 10,000 years ago. Between the beginning of time and now.

By Head Hunter (not verified) on 10 Mar 2010 #permalink

Hm, two strikes against this paper right from the start:

1) as has been poointed out, the authors look at a correlation and assume direct causation. Without any furhter evidence. OOPS!

2) the journal. Lately, PNAS has been full of cow droppings. Greenpa put it right: "And this was peer reviewed?". Well, maybe the editors are the problem, and passed the paper despite reviewers screaming bloody murder, or selected unsuitable reviewers in the first place. So do not be too rash to blame the 'peers'. In any case, the problem is not limited to this article, but it is a recurring problem with the journal. Remind me never to publish there.

In all: a pity! A great study, great idea, great data collection, and then the (preconceived notion-driven?) over-hasty conclusion.

By Heinrich Mallison (not verified) on 10 Mar 2010 #permalink

Ignore the trolls, focus on the fascinating subject.

Since diversity has been reduced, one wonders if a breeding program could re-insert the "fossil" DNA, thus adding to diversity and improving the chances of long-term species survival of the muskox. I would refer you to the progress Max Planck institute has made (Svante Pääbo et al) in developing technologies to extract fossil DNA of pleistocene fossils without contamination, but I forgot the link.

By Birger Johansson (not verified) on 10 Mar 2010 #permalink

"According to numerous accounts handed down from generation to generation, people have killed dinosaurs before. Ever hear of marco Polo? he saw a triceratops when he visited China. The Chinese were using them to pull wagons."

Yeah, I hear that old Marco took some pictures of it with his digital camera, but those evil Darwinists had them locked away in a secret vault somewhere to prevent the world from knowing the truth. They're concealed along with Henry VIII's favourite recipe for trilobite thermidor and Columbus' account of how his ships were attacked by a flock of Pteranodons in mid-Atlantic.

Head Hunter: you should change your name to "Brain Hunter". You're in serious need of one.

I respectfully disagree not with the data but with the conclusions. There is a smoking gun we humans caused mass extinctions of magafauna where ever modern humans went. In a very rapid time frame megafauna disapeared from Australia and the Americas exactly when we got there. I can just as easily conclude from the data that the musk oxen was saved from extinction because it was able to reteat to two locations, Greenland and areas in northern Canada where it was able to survive in an envirement so harsh that only minimal human population ever lived there.
I'm getting really tired of the "it's complex" argument to deny our incredibly murderous history as a species. It smacks of politically correct thinking influencing good science.

By Dave Chamberlin (not verified) on 11 Mar 2010 #permalink

Thanks for the comments everyone, though I am a bit puzzled by some of the reactions. The authors used new data to track the shifts in muskox populations over time, and they forwarded a hypothesis to explain the fluctuations based upon shifts that have been observed in living populations. They recognize this as a hypothesis that requires further testing, so I can hardly regard this as a failure of peer review as some have hinted here. (Are scientists not allowed to hypothesize? Should we only report data and leave it at that?) Nor do I consider it a "strike" against the paper that it was published in PNAS. PNAS has published a few bad papers, but it has also published some good ones, and the merits of the research has to stand for itself. It is not as if it is a journal like Medical Hypotheses which is simply a dumping ground for crazy stuff. Furthermore, I do not see the problem with recognizing the correlation between population size and climate shifts; sometimes correlations are evidence of causation, and I have no doubt that the question of what spurred the shifts in muskox populations will continue to be investigated.

If anything, this thread seems to show the opposite problem in assuming that humans must have been involved in the fluctuations despite a lack of direct evidence. The samples from Greenland and Canada, for example, show the start of a declining trend before the arrival of humans in enough numbers to cause such a decline. Additionally, we know that members of the Independence I culture in Greenland hunted many muskox in Greenland between 2,400 and 1,000 years ago, yet there is no dent in the increasing trend of genetic diversity during that time. Perhaps, in the case of muskox, humans have not affected genetic diversity (and hence population size) as much as might have otherwise been expected. As the authors of the paper note changes in climate seem to be a better fit for the increasing and decreasing trends in genetic diversity, and I think that is a fine hypothesis (which, of course, requires further testing).

And to riff off of Dave's comment, I am getting tired of the "humans must have done it, end of story" argument. Mass extinctions are complex events, and the more we find out about the natural history of Pleistocene mammals the less the "humans show up, megafauna goes extinct" model works. From what I have seen in the literature there seems to be a growing consensus that we need to better understand the natural history of each species of large Pleistocene mammal if we are to comprehend how they were affected by both humans and climate change. We cannot assume that there was just one cause that explains everything for every species. Indeed, in some places, like Eurasia, climate appears to be a more important driver of extinction than human presence, while in North America more people prefer the "overkill" model. Despite this, however, there is still a lot we don't know about what actually happened, and I am not particularly inclined to entirely get behind humans or climate change as the sole extinction triggers. If anything, I think these pressures were felt differently by a variety of species; I am dubious that there was any neat, single cause that can explain everything. This has nothing to do with "politically correct thinking", as David asserts, and if anything I think the overkill hypothesis has been given undue prominence during a time when there is still much we don't know. I have no doubt that both humans and climate change were significant factors during the mass extinction, but the question is just how important each was in accounting for the disappearance of particular species and the survival of others.

I come for the great science posts, but from now on I'm going to be sure to read the comments for the surreal-ness.

Laelaps- "The samples from Greenland and Canada, for example, show the start of a declining trend before the arrival of humans in enough numbers to cause such a decline."

WHOA. Hold it. Stop.

I'm sorry, but your assumption that large numbers of humans are necessary for massive interference in animal populations is not at all warranted, nor supported by clearly known history.

This is where the simple-minded extrapolation, with just plain no knowledge about the subject, is indeed highly harmful.

Assuming almost everybody here is a practicing scientist- is there anyone here who has NOT had the experience of beginning to investigate a new area- and discovering that in fact, 80% or so of the extant literature is absolute garbage? Long since discarded by the competent workers in the field- but still there, and requiring you to work through it?

Publishing crap is a huge problem.

In regard to animal populations- when humans invade a region which previously had no human predation, it is very easy, indeed common, for them to disrupt animal populations- in many many ways besides simple hunting for meat. By far the most common is interference with reproduction. It's exceedingly easy to imagine- as an ethologist- a situation where a small group of hunters discover a human-naive population of large herbivores, and find that not only the easiest way to kill them, but almost the only way, given their primary weapon of an atlatl, is to attack herds gathered for mating. Or to specifically attack infants and juveniles, which adults are unable to protect against group hunting.

Now- do that for about 10 years- and it could easily cause a drastic drop in the local population- then making that population far more susceptible to impacts from things like dire wolves and sabertoothed cats. - etc, etc. Positive feedback.

Any naive population has to be considered metastable, when a new factor is introduced- the entire system is forced to move toward a new balance; and it is very easy for that to include extinctions.

How is it possible for us to ignore and forget the Passenger Pigeon story- where flocks of many thousand birds still flew- years after they were unable to reproduce?

The well known histories of the European invasion of the Americas, the Polynesian invasions of the Pacific islands (and Madagascar), and the Aboriginal invasion of Australia are absolutely uniform.

That, at least, requires that the possibility of human causality be examined extremely carefully, in light of any new data.

And it simply was not, in the current paper- as multiple commenters here pointed out.

Brian, just look at the illustration above. In every geographic location decline in diversity begins at just about the time of human invasion of those various locations, and the more abruptly humans arrived on the scene the more precipitantly diversity declines. Now, it may be true that these invasions correlate with times of warmer and wetter climate, but climate served only to facilitate human invasion and in itself had little or no impact on musk oxen population or genetic diversity. The evidence speaks for itself and it's a glaring deficiency of analysis that the authors so egregiously misinterpret their own evidence.

By darwinsdog (not verified) on 11 Mar 2010 #permalink

Thank you for your quick and detailed reponse. Of course there is complexity in the extinction of any animal. I can take your comments out of context to prove my point and you can then take mine and all we will prove is we both have egos. In science there is the old but not yet worn out cliche that extraordinary claims requires extraordinary evidence. Well there happens to be extraordinary evidence that we did cause mass extinctions of megafauna. It has been roughly estimated that a species has an existance of five to ten million years, of course there are exceptions. In Australia within 1200 years every single plant eating animal wieghing more than 200 pounds went extinct, all 55 of them. When did this happen? Right when we got there. It has been estimated that 73% of all large and tasty critters made a quick exit from the Americas right about the time modern man hit the scene. Nit pick and quibble all you like, maybe you can get the odds down to one in a trillion that this was a random event, if you try hard enough. Anyway fantastic chart on the genetic diversity of the musk oxen. I was raised in a family where we enjoyed disagreeing, we never took it personally, I hope you take this the same way.

By dave chamberlin (not verified) on 11 Mar 2010 #permalink

It does seem somewhat odd to make extinction assumptions about a relatively smaller member of the local megafauna. Clearly, buffalo did not get wiped out; we just wiped out everything larger that might have competed with them. When larger competitors and their predators went extinct, presumably more marginal niches for the muskox would open up.

I'm also surprised that they're correlating expansion through colonizing a large new habitat with improved habitat by environmental effects. The two seem quite separate, and without Greenland, it looks like a nice, steady free-fall in each region from needles or humans (whichever happens last) to the present.

Of course, the climate argument is the one that can be made with the simplest and most accessible data. At this point, they may principally be presenting their genetic findings, rather than establishing causes. I wouldn't be too surprised to see further work from the group correlating it with other categories of events instead.

Chris, in all probability humans did drive several species of the genus [i]Bison[/i] extinct. The story is that the hyper-abundance of the one remaining species (in North America) is attributable to reduced grazing competition by congeners and other recently extinct ungulates.

I agree with you that without the Greenland refugium, musk oxen would have been hunted to complete extinction.

By darwinsdog (not verified) on 11 Mar 2010 #permalink

Hard times in interglacial periods is probably the same hazard for Musk Ox as for Caribou. Warmer climes means deeper snow cover, freezing rain icing over food. Calving in wet weather etc. No men required

I was under the impression that the latest studies show musk oxen are more related to sheep (ovis) than cattle (bos). One of the issues with "humans killed them" I have is why megafauna survived in Africa, and to a lesser extent, in India. Africa is our first home, India looks to have been a very close competitor for "how humans got out of Africa". I don't buy the "these somehow adapted to human predation" arguement -- there were significantly more humans in Africa to do the hunting during the initial expansions. Certainly humans have done their share of extermination, but I doubt humans are the only cause. Why do lions die out in America where they survive in many locations outside their current areas until Roman times? I believe that some of the current archeological/antropological studies indicate that Amerindians actually managed bison herds prior to the 1500s by using fire to create better grazing zones.
vr, Peggy Richter

By Peggy Richter (not verified) on 12 Mar 2010 #permalink

Peggy, the rise of humans in Africa was accompanied by an extinction pulse - several species of hyaenid, for instance, were driven extinct presumably by scavenging competition with hominids - but Anthropgenic Mass Extinction (AME) was more drawn out and less inclusive in Africa because the African fauna had the chance to coevolve with hominid & human predation pressure. In places where a naive fauna was impacted by the sudden advent of humans, the mass extinction event was much more abrupt and inclusive. This is seen in Australia & the Americas, as stated above. It was especially seen on oceanic islands & archipelagos. The North American lion is a good example of a widespread, successful species driven extinct in short order following the advent of humans in the Americas, as humans wiped out the lion's prey. AME began in Africa and accelerated as humans expanded their range thruout the world. Today, AME has jacked the extinction rate up several orders of magnitude over the background extinction rate. You may be correct to state that humans aren't the only current cause of extinction but our species is so overwhelmingly the agent of megadeath on Earth that other causes are negligible in comparison.

By darwinsdog (not verified) on 12 Mar 2010 #permalink

Darwinsdog : "The North American lion is a good example of a widespread, successful species driven extinct in short order following the advent of humans in the Americas, as humans wiped out the lion's prey. "

I expect that's largely true- I would like to see a little more weight given however to "ceremonial" hunting by humans; something we know many peoples do, and not just hunter/gatherers.

We like to kill rare animals specifically because they are rare- and not just wacko moderns. There are abundant first person narratives about European hunters with native guides coming upon a rare creature; and the natives wanting immediately to kill it- because it's rare, and would enhance their status.

In primal situations, its a matter of great status (i.e. reproductive success) to kill large predators; with the Masai not long ago, it was necessary for boys to kill a male lion single handedly to become a functional adult.

I think that pattern could go a long way to explaining why humans are so good at eradicating species. Knock the populations down via food hunting- finish the job with ceremonial- get that last mammoth now, Sonny- you'll never have another chance.

greenpa- untestable, of course- but it sure rings true.

By ranklebiter (not verified) on 12 Mar 2010 #permalink

Qiviut, wool of the musk ox. And it ain't cheap.

By mikey.duhhh (not verified) on 12 Mar 2010 #permalink

Nor do I consider it a "strike" against the paper that it was published in PNAS. PNAS has published a few bad papers, but it has also published some good ones, and the merits of the research has to stand for itself. It is not as if it is a journal like Medical Hypotheses which is simply a dumping ground for crazy stuff.

Brian, let me explain why I see PNAS as a strike against the paper. THis solely refers to my reaction to it, not necessarily the validity of the content. My 'strike' I mean: There are way to many papers for me to read, and this is from a field that is far enough outside my own field for me to read each and every paper. So I have to pick and choose which papers to skim, which to 'read' (i.e. read the abstract, glance at methods, read conclusions and discussion), and which to study (= read completely, re-read partly if necessary, check sources, research further). This paper, by its topic, would usually make the 'read' category. However, skimming the conclusions combined with PNAS dumped it into the 'ignore' category.

The reason is fairly simple: speculation is valid, proposing new, so far insufficiently tested hypotheses is valid. But the reviews and editorial process should catch arm-waving, blantant omission of important facts, or omission of obvious, self-suggesting 'conventional' explanations, especially when the topic is 'loaded'. PNAS has a recent history of repeatedly failing in this respect. Maybe it is the reviewers, maybe it is the editors, most likely both. Thus, off to the dumpster for now. This paper could have been awesome, but it comes up short.

By Heinrich Mallison (not verified) on 14 Mar 2010 #permalink

Are musk ox good to eat? Do they have any use to humans other than their pelt for clothing? A point that I never see raised in the overkill hypothesis is whether the prey animals are tasty? Only desperate humans hunt animals that taste bad. There are exceptions to this in market driven modern times (bison killed for their hides in the US) but otherwise people only kill to eat. If musk oxen taste bad, or at least don't taste good, then humans would not hunt them and they would escape extinction by hunting, and in fact would likely flourish in the absence of competing animals in a similar niche.

By Caw Miller (not verified) on 02 Dec 2010 #permalink