A four-legged snake

July 26, 2015 • 3:30 pm

by Greg Mayer

It has long been known that some snakes are two-legged, because many modern species have two legs– externally visible hind limbs– a fact we’ve noticed here at WEIT before.

Hindlimbs ('spurs') of a ball python (Python regius). The spurs are next to the anal scale, which covers the vent of the cloaca. (Front of snake is toward top of photo.)
Hindlimbs (‘spurs’) of a ball python (Python regius). The spurs are next to the anal scale, which covers the vent of the cloaca. (Front of snake is toward top of photo.)

These small external legs, capped by keratinous claws, are supported internally by vestigial femurs and a vestigial pelvis. They are larger in males, and are used during courtship. In the fossil record, snakes with much larger hind limbs have been known since Georg Haas described Pachyrachis in 1979 and Ophiomorphus in 1980 from the early Late Cretaceous (about 95 mya). In these the legs were less rudimentary than in modern snakes, having, in addition to the femur and pelvis, a distinct tibia and fibula, and tarsal bones. That legless tetrapods would have legged ancestors is of course expected, and for the caecilians, a modern group of legless amphibians, a four-legged progenitor was described by Farish Jenkins and colleagues several years ago.

In a new paper paper in Science, David Martill, Helmut Tischlinger, and Nicholas Longrich describe a four-legged snake from the late Early Cretaceous (about 120 mya), of Brazil, giving it the rather aptly descriptive name Tetrapodophis, “four-legged snake”. The fore and hind legs are small, but well developed, with five digits on each. The limbs are suggested to have been used during prey capture. They also interpret it as being fossorial. This is significant, as the two major theories of snake origin are that they came from fossorial (burrowing) ancestors, or that they came from marine ancestors (some of the closest known relatives of snakes are extinct aquatic lizards, and Haas’s specimens come from marine sediments).

T. amplectus appendicular morphology. Fig. 4 from Martill et al. (2015). (A) Forelimb. (B) Manus. (C) Hindlimbs and pelvis. (D) Pes. (E) Pelvis. Abbreviations: fem, femur; fib, fibula; hu, humerus; il, ilium; lym, lymphapophysis; man, manus; mc, metacarpal; mt, metatarsals; ph, phalanges; ra, radius; sr, sacral rib; tib, tibia; ul, ulna; un, ungual.
T. amplectus appendicular morphology. Fig. 4 from Martill et al. (2015).
(A) Forelimb. (B) Manus. (C) Hindlimbs and pelvis. (D) Pes. (E) Pelvis. Abbreviations: fem, femur; fib, fibula; hu, humerus; il, ilium; lym, lymphapophysis; man, manus; mc, metacarpal; mt, metatarsals; ph, phalanges; ra, radius; sr, sacral rib; tib, tibia; ul, ulna; un, ungual.

A long, flexible body, recurved teeth, and intramandibular joint (for opening the mouth wide) all suggest to Martill and colleagues that Tetrapodophis was a constrictor, preying on other vertebrates. This also has significance for what it says about the origin of snakes. Under the fossorial theory, the earliest snakes should have been insectivorous or eating other small prey (as are many supposedly primitive burrowing snakes today). Under the marine theory, the earliest snakes should have been predators of prey “bigger than their heads“, having large, extensible mouths, and associated adaptations of the skeleton and musculature– such snakes are called macrostomatan (literally, ‘large mouthed’). Haas’s two-legged marine snakes are macrostomatan. Martill and colleagues have found what they consider to be a very early macrostomatan, yet fossorial, snake– a cross between the two theories.

Tetrapodophis constricting and eating a small mammal, reconstruction by Julius Cstonyi.
Tetrapodophis constricting and eating a small mammal, reconstruction by Julius Cstonyi.

Almost immediately upon its publication, the paper became enmeshed in a series of overlapping controversies, which, while nothing compared to the brouhaha over the insults traded between Nicki Minaj and Taylor Swift, has created quite a stir in the small world of science social media. There are at least three areas in which questions have been raised, so let’s take them one at a time.

Where (and thus when) is the type specimen of Tetrapodophis from? It turns out that the authors of the paper don’t actually know the provenance of the specimen. They have made an inference about it (and they may very well be right), but the fact that they do not even mention the assumed nature of the specimen’s provenance in the paper is shocking. A specimen’s provenance is absolutely crucial information in systematic biology; it is especially so for fossil specimens, because in most instances it is only by examining the geological context of the discovery (the associated fossils within the bed, and the nature of the over- and underlying beds) that we can date the fossil. In this case, we are not really sure where the specimen came from, and thus we cannot be certain of when the specimen died and was entombed in sediment.

I read the paper, and did not realize the provenance was uncertain. The uncertainty, and the argument for why the authors felt they could identify the provenance, are buried in an online supplement. To some it may seem like I’ve been a bit “hey you damned kids, get off of my lawn” about it”, but I’ve long complained of the growing practice of journals, especially Science, of burying key details of papers in ephemeral online sources, and in this case such warnings have come home to roost. Where (and thus when) it’s from is just about the most basic thing you can say about a fossil, and to hide the fact that in this case it’s unknown in an online supplement is unconscionable.

In the online material, Martill and colleagues state that “no notes as to its [the specimen’s] acquisition or provenance are available.” However, in an interview with the BBC, Martill says that he first saw the specimen at the Museum Solnhofen in an “exhibition of Brazilian fossils”, so some notes on provenance seem to have been available to the Museum. Another source states that the exhibit was of fossils specifically from the “Crato Formation”.

Is the fossil, as the authors claim, from the Nova Olinda member of the Crato Formation of Ceara, Brazil? It might well be. Martill is an expert on the formation. Certain fossil localities do have a distinctive lithology and preservation– I can (usually) recognize Green River Formation fossils myself. But to not mention this up front, and provide the justification for the assignment to provenance in the paper, is beyond the pale.

Is Tetrapodophis even a snake? In a news posting on Science‘s website, Michael Caldwell alleges that the specimen is not a snake; in fact, he says, it’s not even a reptile. Rather, the article says, Caldwell thinks it might be a surviving member of a “group of extinct amphibians that died out during mass extinctions about 251 million years ago, long before Tetrapodophis appeared on the scene.” (I’m not sure what amphibians he’s thinking of– perhaps microsaurs or lysorophids?) This would be astonishing– that a group survives 150 million years without a fossil record and then reappears (which does, though, have a partial precedent in the coelacanth), and that the authors and reviewers of a paper in Science could be so wildly off in the identification of the subject of the paper. This of course is not impossible, but it would be surprising. I have only seen the published figures, but Martill and colleagues do discuss and defend the characters by which they assign the specimen to the snakes. Caldwell has published on early snakes and should know their morphology, but he has not seen the specimen either, so it’s hard to give full credence to his views. We’ll have to wait till others get to look at the specimen more closely, or perhaps for a monographic treatment by Martill and colleagues. This is the scientifically most important controversy (although the first controversy is right up there, because much of its significance as a four-legged snake depends on its supposed time of occurrence).

Should fossil collecting and/or exporting require a permit or license? Since the specimen has no collecting data accompanying it, it is unclear if the specimen was collected legally. Fossil collecting in Brazil has required a license since 1942 (or perhaps 1988– recent sources diverge on the date). This is of course not a scientific question, but a question of public policy that has implications for science. To a great extent, the controversy is an old one in paleontology– does  amateur and commercial collecting enhance or retard the growth of scientific knowledge?  There are strong opinions on both sides. In the United States, this argument flared up over Tyrannosaurus Sue, which was discovered and collected by commercial collectors, but eventually seized from them without recompense (one even went to jail). The downside of such regulation is that many specimens will never come to light, or, if found, will be tossed aside and left to degrade, as their possession would be illegal. A commercial black market may develop, in which the best fossils may be found, but then disappear, unstudied, into private collections. The upside is that specimens will have known provenance, and be of maximal scientific value. Martill has long argued (also here) that in Brazil the permitting system has become so corrupt that scientists are driven out of the field, and that, through bribery, commercial trade flourishes, while many fossils are left to erode and break, as no one may legally save them. He also says it was not always so– for years he worked successfully under Brazil’s regulations. His view:

‘Protecting fossils’ criminalises palaeontologists. Laws banning fossil collecting and private fossil collections deter amateur palaeontologists, drive them underground and stifle curiosity. Fossils left in the ground weather away and are lost. Banning commercial collecting loses tax revenue.

A group of Brazilian paleontologists led by Max Langer, in a strong riposte to one of Martill’s pieces, wrote

Instead, the Brazilian perspective is that taking fossils out of the country is depleting its scientific resources. Brazil has a growing, but still minor scientific community. For palaeontology, keeping the fossils in the country is a way of promoting scientific opportunities. International partnerships are most welcome, but simply allowing fossils to leave Brazil to be studied by foreign scientists mostly helps science in the other countries.

On the issue of regulation, my own view is an in-between one. An analogy can be made (one which Martill disputes) with wildlife conservation. Many species and natural areas require protection. It is often scientists who are at the forefront of advocating for such protections, even though it will add to the difficulty of doing scientific work on the protected species and habitats.  It is true that sometimes such regulations can be over-zealously enforced against scientists (in part because they are so visible and have no economic clout), while ignoring the truly endangering factors. But when scientifically informed and sensibly applied, these protections are welcomed by scientists. And, indeed, Martill describes a formerly good relationship with the Brazilian authorities. I do not know enough about the situation in Brazil to have an informed opinion on whether Brazilian policy and practice on this matter has achieved the right balance to encourage discovery and scientific research, while maintaining proper stewardship of their resources.

Another analogy with wildlife conservation issues is what to do with illegally collected specimens. It is standard for wildlife enforcement agencies to donate such materials to museums or educational institutions (although their value as scientific specimens is lowered by the frequent lack of provenance). More controversial is what to do with seized specimens of commercial, but no scientific, value. For example, some advocate the destruction of seized elephant ivory, while others argue that that only drives up prices, leading to more poaching. In the case of fossils, what scientific value there is in them can be extracted by describing them (again subject to the constraints of knowledge of provenance) and placing them in museums (not, by any means, destroying them!).

Regarding the issue of whether fossils should be exported, I am sympathetic to the need to develop scientific institutions throughout the world, and thus to build local collections and relationships between foreign and local institutions and researchers. This must be tempered by recognition that not all places are in a position to care for important collections or engage in collaboration. In this regard, I would note that Brazil has at least one distinguished student of early snake evolution, Hussam Zaher, and at least some excellent museums, although I do not know enough about the situation with the Crato fossils to have an informed opinion on that specific case. I would point to the recent return of Tiktaalik to the Canadian Museum of Nature after 11 years of study in the U.S., and Costa Rica’s policy of a division of collected specimens among foreign and Costa Rican institutions as policies that seem to be working.

The Brazilian journalist Herton Escobar has conducted an email interview with Martill. In it, Martill’s frustration with being denied further access to his field sites in Brazil is evident. He asserts (correctly, in my opinion) that the scientific value of the fossil is not affected by the legality of its collection (to which, I should add, there is no suggestion that Martill or his colleagues were involved in its collection– he first saw it in Museum Solnhofen during a class field trip); its value is affected by the lack of certain provenance. In response to a question as to whether he had sought a Brazilian collaborator, Martill said he did not. Not seeking a Brazilian collaborator is fair enough– he worked with colleagues in England and Solnhofen, close to him and the fossil, and he had at best difficult personal relationships with Brazilian workers at the time. But Martill also goes off on an odd rant about ethnic and sexual diversity in research groups– not at all what Escobar was asking about.

Haas, G. 1979. On a new snakelike reptile from the Lower Cenomanian of Ein Jabrud, near Jerusalem. Bulletin du Museum national d’Histoire naturelle 4: 51–64.

Haas, G. 1980. Remarks on a new ophiomorph reptile from the lower Cenomanian of Ein Jabrud, Israel. pp. 177–192. In Jacobs, L.L.,
ed., Aspects of Vertebrate History. Museum of Northern Arizona Press, Flagstaff, Arizona.

Martill, D.M., H. Tischlinger, and N.R. Longrich. 2015. A four-legged snake form the Early Cretaceous of Gondwana. Science 349:416-419.

h/t Matthew

36 thoughts on “A four-legged snake

  1. There’s another serious problem with the report on this spectacular fossil (it’s got gut contents!), namely that in the title, abstract, and first four paragraphs it’s written of as a “snake,” whereas it’s no more a snake than Dimetrodon is a mammal. Only into paragraph 5 of the text is Tetrapodophis accurately said to be a stem-snake, an important distinction likely lost on many biologists, let alone the media and lay readers of Science. After all, wouldn’t we expect to encounter snakes with four legs on branches off earlier on the stem to crown-group snakes?

    1. I am not up on the details of what makes a snake, but if this fossil has characters that are unique to snakes then it could be called a snake.

    2. I have often thought that a four-legged stem-snake should not be called a ‘snake’, but I never expected to live to see one. Now it’s out there, it actually seems a lot snakier than I would have expected. Huh.

  2. I’ve long complained of the growing practice of journals, especially Science, of burying key details of papers in ephemeral online sources, …

    Just a quibble, I agree with most of what you say on this, but are the online supplements really ephemeral? In these days with entire journals going online-only, I’d have presumed that online resources are intended as permanent.

    1. I’d have presumed that online resources are intended as permanent.

      That’s what I’d expected too. But … well, I’ve got ink-on-paper going back to the 1930s and I’ve handled reports from the early 18th century. It’ll be several centuries before we know if online archives can actually achieve that level of reliability.
      There are several Latin and/ or Greek scholars in the Usual Suspects, who can take the analogy back another millennium or so.
      And I haven’t even started on the geologist’s or archaeologist’s view of “permanent”.

      1. It’ll be several centuries before we know if online archives can actually achieve that level of reliability.

        We already know that digital information can be copied indefinitely without loss of fidelity. So assuming redundant distribution of digital archives around the world, it’s hard to imagine a scenario short of global collapse of civilization that would render them less permanent than perishable analog media.

        1. So assuming redundant distribution of digital archives around the world

          That is not in the interest of publishers, who would like to rent you the right to read a document, but not be able to remember it.

          1. Agreed, but supplements are (generally) free.

            Maybe I am speculating too much, but I connected this with a recent article on how our virtual persona (internet presence) will, if we let it, rapidly know more about ourselves than we do. (Re health issues, minimizing energy expenditure, et cetera.)

            So large supplements are unwieldy today. But perhaps in a few years an expert ‘reader’ can help us dig out misplaced vital data such as what Greg points out.

    2. I think the more important ethical concern is that scientist readers take it somewhat for granted that if there is a huge caveat to your work, you will mention it up front in the main body of the paper. If (making up an example) there’s a 10-page paper and 100 pages of supplementary material, I think a reasonable argument can be made that it is poor and unethical science to put some major caveat to your findings on page 72 of the supplementary material. It should show up in the 10-page report. It is irrelevant whether the supplementary material is preserved or not; the point is, very few scientists will read that much, even people in that field. Scientists simply don’t have the time to read a hundred or hundreds of pages on each individual discovery.

    3. I’ve already run into papers with missing online supplements. I tend not to think that this is an inherent problem with digital media but rather a problem with splitting a paper into multiple parts that are distributed independently, some of which are clearly considered to be non-essential.

      If the supplemental material really is ancillary and non-essential, this might not be a problem; if it is essential information without which the article cannot be understood, on the other hand, separating it out from the article and placing it in a format that is -viewed- as ancillary and non-essential is a problem no matter the format. In that case, it needs to just be included in the article. The gist is, we shouldn’t have academic articles that are published and distributed in an incomplete form.

      1. When there’s a change of publisher, printed articles are usually archived at the new site (sometimes as well as the old one), but supplements are frequently tossed. Self-archiving by authors and their institutions is essential.

  3. From what I’ve read of the controversy, Martill has shot himself in the foot with a large item of field artillery, as far as the prospect of continuing field work in Brazil goes. I wouldn’t be surprised, given some of the comments attributed to him, if he’s queered the pitch for any other British academics or students who want to work on the Crato materials (or any other materials from Brazil). Politics doesn’t make your tongue taste any nicer when you have a long chew on it, but it’s often a political necessity.
    I’ve had days of additional work courtesy of other countries (not Brazil’s) policies on export of specimens, and I’ve had the hours of being shouted at by groups of irate customs personnel when I’ve been hand-carrying samples out of the country (through ignorance of the permit requirements, not through unwillingness to adhere to them ; I had abundant relevant and accurate paperwork, just not the correct paperwork. So I can appreciate where frustration with such restrictions comes from. OTOH, part of professionalism is sucking it up in situations like that, to avoid making life harder for the next person in that situation (who might actually be yourself). Their country ; their rules.
    From the other point of view, if your nascent Department of X-ology can’t get involved in current research within it’s borders, how the hell are you going to build breadth and depth of experience in your senior staff, technicians and students? In a very real sense, you learn by doing.
    The absence of a good provenance for the specimen is a big, big hole in the project. They might be able to fill, or reduce, the hole by micropalaeontology, but very literally you would expect the people with the best experience on the micropalaeo of the Crato formation to be working at/for Brazilian institutions. For exactly the same reason, if I want an opinion on the dating of Russian rocks, I’d probably be looking at finding collaborators in Moscow, and for Tanzanian rocks I’d go to Dodoma.
    A fossil removed from it’s context is a seriously depleted specimen.
    (From the description given, Martill et al are simply making the best of a bad job here, however the specimen got detached from it’s context. But given the public furore, they’ve got an uphill struggle to get cooperation from the Brazilians now.)

    1. Good comment. “Their country; their rules.” Or as they say around here (Brazil), you don’t discuss the law, you obey it.

  4. From Martill response on why he didn’t invite a Brazilian research:

    “I mean, do you want me also to have a black person on the team for ethnicity reasons, and a cripple and a woman, and maybe a homosexual too just for a bit of all round balance?”

    That’s the sign of an asshole right there.

    1. Yeah, not hard to understand why he’s had trouble with the Brazilian authorities. Personal charm doesn’t seem to be a strong point.

  5. Thanks for this article, Greg. I didn’t realize the provenance was unknown and that is such a shame.

  6. Great article, Greg! I don’t have the correct background to weigh in on the merits of the paper or it’s findings, but I think this is an excellent summary of some of the details of how science (or any knowledge art) works. I especially liked how you showed the peer review process isn’t over just because the paper is published, questions over how the publication methods can effect the peer review process, and research ethics all in one short post.

  7. Thank you for this very detailed description of the scientific and the very messy situation surrounding this fossil. I was not aware of most of the latter details.
    I agree fully that one needs to be sensitive to the pride and rightful feelings of ownership when it comes to collecting fossils and other antiquities. To my knowledge the relationship that Donald Johanson (the discoverer of Lucy) has developed with the Ethiopian government is a model of how this sort of thing should develop. Both the scientists and the government should make good choices in developing these relationships.

  8. Undoubltedly Martill has short fuses and should turn his tongue seven times in his mouth before speaking. And he is or was probably in some trouble with Brazilian authorities – but having experienced several custom, veterinary and/or nature protection administrations in my shrew hunting I can understand that. And for relegating important stuff of a paper in the “supplementary material”, it is unfortunately a rather generalized tendency of top scientific journals. What they want is an appealing title and an article short enough to be read while commuting. Thus I would not throw too heavy stones on the authors.
    But back to science. I’m not an expert of this field and I have some questions.
    1) Considering the vertebrae morphology, Caldwell denies that Tetrapodophis is even a Squamate. In this case, the level of convergence would be absolutely fantastic. Do we have another example of convergence going down to so many morphological and even behavioral (cf the ingested prey) details ?
    2) Aquatic vs fossorial origin: does not the similar evolution in other groups (Anguidae, Scincidae) very strongly speaks in favor of the fossorial origin ? Why should snakes have a different one ?
    Amusing: some christians are very happy with Tetrapodophis: its legs are the proof, you know, that the Genesis is an exact account of what occured.

  9. I somehow thought the find would settle the snake origin controversy, not fan it.

    The data on the ‘big mouth’ potential “marriage” of theories was interesting too.

    it is unclear if the specimen was collected legally.

    Well then. No evidence either way means not a problem of legality (in most jurisdictions).

    On the larger issue, perhaps fossils should be made “open source” instead of being under “stewardship”? I think John Hawks proposes that over on his paleontology blog. In most cases of open databases, the responsible scientists get a year (or 11), whatever they need to secure return on investment before publishing the data.

    For example, some advocate the destruction of seized elephant ivory, while others argue that that only drives up prices, leading to more poaching.

    I thought it was a moral issue. The killing and/or torturing is hurtful; burn it with fire!

    But Martill also goes off on an odd rant about ethnic and sexual diversity in research groups– not at all what Escobar was asking about.

    Speaking of a null hypotheses of freeing rather than convicting, Martill is responding to Escobar under the assumption that it is a nationalistic issue. “For me nationality (or sexuality) is not an issue.” I don’t think it was an erroneous assumption. (But he responded as a bigot on groups. Speaking of ‘big mouths’.)

  10. One of the more interesting aspects of this “stem-snake” is that the distal phalanges are longer than the proximals, giving the impression of a “reverse situation” to that found in modern vertebrates.

    As usual, Greg, good coverage. I’m sure this discovery will generate some interesting discussions at the SSAR meetings this week.

  11. Regarding the permitting question, isn’t there an easy way to split the baby? Martill is concerned about what the criminalization of private efforts will do. Brazil is worried about abusive exportation. So, make it legal to privately collect and sell fossils within Brazil but not to outside sources.

    1. Anytime that a monetary value is placed on a fossil it fuels the underground fossil market, which has been estimated to go over $2 BILLION dollars a year. It should be legal to collect privately, but private collections need to be monitored by paleontologists who have the where-with-all to say that something is scientifically significant and belongs in a museum collection. Hobby collectors make some (perhaps most) of the most significant contributions to Paleontology, so their efforts should not be reduced. What the scientific community needs to do is to make the hobby collector community aware of the significance of their finds to all of us, and to inculcate a “donor mentality” in them. This will NOT happen when monetary values are placed on the fossils their finds!

      1. A monetary value is going to be placed on them regardless of whether collecting them is legal or not. In fact, like prohibition, the monetary value probably goes up (not down) when you make private collection illegal.

  12. Excellent article! This would’ve been a really good candidate for discussion in our journal club; sadly, we had our last meeting of the summer already. I too find Caldwell’s contention implausible, though not impossible.

    As for the controversy surrounding how the fossil was obtained, I have no strong opinion, not because I don’t consider the issue serious but because I’m torn.

  13. As much as I am in favour of amateur scientists, I wonder what can be done. Could there be a way to have certain sorts of fossils be collectable (without a permit) but others not?

  14. Doncha know god that did it? Genesis 3:14 And the Lord God said unto the serpent, Because thou hast done this, thou art cursed above all cattle, and above every beast of the field; upon thy belly shalt thou go, and dust shalt thou eat all the days of thy life:


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