Turtle origins

by Greg Mayer

In a paper soon to be published in Current Biology (abstract), Tyler Lyson and colleagues propose a model for the origin of turtles, using the Permian (ca. 260 mya) fossil Eunotosuarus as a transitional form.

GraphicalAbstract-finalThe origin of turtles is a fascinating and important area of study, although one that is perhaps generally underappreciated (Burke 2009). The reason for its importance is that the turtle shell is probably the most novel and highly derived of all skeletal structures in the vertebrates. Nothing in human evolution, for example, compares. What do we have that’s distinctive? A really short tail? It’s been done to death, and just involves some reduction in size and number of bones. Bipedality? Also done many times. A large cranium? Just a few bones getting bigger.

What have turtles done? They’ve moved their shoulder and pelvic girdles inside their rib cages! If you want to appreciate what this means, reach behind your back and touch your shoulder blades, then reach down and touch your hip bones. Now feel your ribcage, front and back. And now imagine getting your shoulder blades and hips inside your rib cage– that’s what turtles have done.

Understanding of the origin of turtles has been hampered by the lack of a good fossil record. For many years the earliest known turtle was Proganochelys from the Late Triassic (ca. 210 mya), which, while primitive in various respects, had a full shell, both top (carapace) and bottom (plastron). The first fossil breakthrough came in 2008, when Li and colleagues described Odontochelys, a Late Triassic turtle a bit older than Proganochelys, but in which the plastron was well formed, but the carapace (top) consisted of only neural bones above the vertebrae, and enlarged ribs.

Lyson and colleagues extend the model of shell origins, incorporating further data on shell ontogeny in modern turtles, and, most significantly adding Eunotosaurus as an early ancestral turtle, which has a proto-carapace of expanded ribs. They also point to Milleretta, another Permian reptile, as a possible very first step in the direction of turtles. (At this point, we pause for Snappy to say hello, so readers don’t forget what the object of our discussion is.)

"Snappy", Chelydra serpentina, Somers, WI

“Snappy”, Chelydra serpentina, Somers, WI

There are two phylogenetic controversies that are involved in this scenario of turtle origin. First, although Eunotosaurus has long been bandied about as a turtle precursor, the consensus has long been that it is not, although Lyson and colleagues (2010) have argued it is. Second, there is great debate about where turtles fit in amongst reptiles in general. Because of the generally primitive nature of their skulls (lacking any openings or fenestrations), turtles have often been linked with one or another of various early reptile groups, and Lyson and colleagues favor this view. There is an almost equally old hypothesis, however, that turtles, despite lacking any skull openings, are nonetheless members of the Diapsida, the great group of two-fenestra reptiles (and their modern feathery descendants) that includes Archosaurs (crocodiles and birds among living taxa, dinosaurs and pterosaurs among the extinct) and Lepidosaurs (tuatara, lizards and snakes among living taxa, mosasaurs among the extinct).

Recent molecular data, including two new genome studies (Wang et al. 2013, Shaffer et al. 2013; see Gilbert and Corfe 2013), have supported earlier molecular studies (including one of my own) in placing turtles among the Diapsida, and indeed, well within the Diapsida, as the sister group of the extant archosaurs.  Although the resolution of these latter debates will have bearing on the full turtle origin story, one thing that I think is now clear is the stepwise origin of the turtle shell, with the various components having been assembled sequentially.

h/t P

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Burke, A.C. 2009. Turtles… …again. Evolution & Development 11:622-624.

Gilbert, S.F. and I. Corfe. 2013. Turtle origins: picking up speed. Developmental Cell 25:326-328.

Kirsch, J.A.W. and G.C. Mayer. 1998. The platypus is not a rodent: DNA hybridization, amniote phylogeny and the palimpsest theory. Philosophical Transactions of the Royal Society B 353:1221-1237. pdf

Li, C, X.-C. Wu, O. Rieppel, L.-T. Wang and L.-J. Zhao. 2008. An ancestral turtle from the Late Triassic of southwestern China. Nature 456:497-501. abstract

Lyson, T.R., G.S. Bever, B.S. Bhullar, W.G. Joyce, and J.A. Gauthier. 2010. Transitional fossils and the origin of turtles. Biology Letters 6:830-833. pdf

Lyson, T.R., G.S. Bever, T. M. Scheyer, A.Y. Hsiang, and J.A. Gauthier. 2013. Evolutionary origin of the turtle shell. Current Biology in press. abstract

Shaffer, H.B. et al. 2013. The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biology in press. pdf

Wang, Z., et al. 2013. The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan. Nature Genetics 45 701-706. pdf

22 Comments

  1. marksolock
    Posted June 2, 2013 at 12:49 pm | Permalink

    Reblogged this on Mark Solock Blog.

  2. MKray
    Posted June 2, 2013 at 1:24 pm | Permalink

    But where do tortoises come into the picture? They are quite distinct from turtles, but share, in general terms (at least to non-biogists) the same striking feature… if not more so.

    • Ryan
      Posted June 2, 2013 at 1:33 pm | Permalink

      They are turtles, and so this hypothesis would hold for them as well.

      • MKray
        Posted June 3, 2013 at 6:41 am | Permalink

        Well, to me, the giant tortoises on Galapagos
        look entirely different to turtles. I was once in a university museum (Oxford?) where they had a large preserved turtle and a large preserved tortoise (each so-labelled)
        side-by-side, which made the difference plain.

        • Posted June 3, 2013 at 1:04 pm | Permalink

          Is this just a case of the American usage in which “turtle” is a broader term that includes what Brits would call ”tortoises”?

          /@

  3. ladyatheist
    Posted June 2, 2013 at 1:49 pm | Permalink

    *sigh* Now there are two additional gaps in the fossil record for God to jump into

  4. Logicophilosophicus
    Posted June 2, 2013 at 2:02 pm | Permalink

    “turtle precursor”?

    You can’t fool me – it’s turtles all the way.

    • Diana MacPherson
      Posted June 2, 2013 at 3:04 pm | Permalink

      Ha ha! Nice one.

    • pacopicopiedra
      Posted June 2, 2013 at 9:10 pm | Permalink

      Winner.

  5. Kevin Alexander
    Posted June 2, 2013 at 2:19 pm | Permalink

    When Odontochelys was first described there was some wonder about why the plastron evolved. We usually think of the turtle shell as protection, and it is but why would it appear on the bottom first? Usually threats come from above.
    I suggested that maybe the shell evolved for locomotion first.
    Google Plastron Toboggan and read the comments at Panda’s Thumb.

    • Marcoli
      Posted June 2, 2013 at 8:45 pm | Permalink

      Ballast to stay under water? Just a guess, but if the dense shell helps it to stay submerged that alone would be useful.

      • Kevin Alexander
        Posted June 3, 2013 at 6:14 am | Permalink

        Ballast, yes. I mentioned that in the comments at Panda’s Thumb but with reference to the dense bones. A dense body not only will help produce neutral buoyancy but will also make a good anchor for an animal that hunts with a long neck and snapping jaws.
        I tried to get my granddaughter to do a science fair project on the aid to locomotion part. Some ground is just too soft to walk on.
        Make two bean bag Odontochelys one with a plastron and one without and drag them across very soft wet ground. Add things like sticks and other obstructions then measure which takes the least amount of force to do that.

  6. pacopicopiedra
    Posted June 2, 2013 at 6:14 pm | Permalink

    I think your shoulder/rib inside the ribcage paragraph is a bit misleading. First of all their shoulder anatomy is different than ours. It’s not like they have a big broad scapula like ours which somehow got moved underneath their ribs. Also, to get your hips “inside” the ribcage would only take a contraction of the lumbar spine (which they don’t seem to have). Move the pelvis superiorly, and your hips are in your ribcage. For the shoulders, it seems like they just have a really hypertrophied first rib, so it juts up superiorly over the shoulder region (which does not have a big, broad scapula).

    Thanks for the post. I think it’s fascinating; but I think there are other aspects of turtle anatomy and evolution that are far more impressive than the hips’ and shoulders’ relation to the ribs.

    • pacopicopiedra
      Posted June 2, 2013 at 6:15 pm | Permalink

      Sorry, shoulder/rib should be shoulder/hip.

  7. John Harshman
    Posted June 2, 2013 at 6:43 pm | Permalink

    If you ask me (didn’t you ask me?) the molecular data have by now become completely conclusive: turtles are the living sister group of Archosauria. So either Eunotosaurus has been seriously misplaced in previous phylogenies or it has nothing to do with turtle evolution.

    Now of course you can use anything as a hypothetical intermediate stage, in the same way Darwin used bears as hypothetical intermediates between land animals and whales. Proof of concept only, and not intended as an actual hypothesis of relationships. (Despite what many have claimed, Darwin never intended to advance the notion that bears were ancestral to whales.)

    • Marcoli
      Posted June 2, 2013 at 9:02 pm | Permalink

      It is surprising to me that the early fossil record on this lineage is very spotty. Semi-aquatic vertebrate. Lives near river banks. Kind of slow. Hello?

      • John Harshman
        Posted June 3, 2013 at 7:30 am | Permalink

        Hello. The early record of pretty much all vertebrate groups is spotty. You want a good fossil record, you need to deal with shelled marine invertebrates. Brachiopods, say.

  8. Marcoli
    Posted June 2, 2013 at 8:55 pm | Permalink

    This is awesome. What puzzles me is how slow textbooks are in reassigning turtles from anapsids to diapsids. Even the most recent edition of my evolution text still places them in the anapsida as if it was not even controversial.
    So now the thought for me is: what other extinct ‘anapsid’ reptiles are really diapsids or synapsids? Besides the precursors for turtles that is.

    • John Scanlon, FCD
      Posted June 3, 2013 at 12:48 am | Permalink

      Wouldn’t it be funny if all the Parareptilia turned out to be inside Eureptilia?

  9. heleen
    Posted June 3, 2013 at 1:09 am | Permalink

    Even if Lyson et al are correct about Eunotosaurus, they are almost certainly incorrect in pointing to Milleretta as the earlies identifiable member of a turtle line, despite their large phylogeny in Suppl Info.

    I don’t know how much of the phylogeny depends upon skull characteristics. The turtle skull is anapsid but not primitive, but the anapsid skull might predetermine the phylogenetic analysis.

    • Marcoli
      Posted June 3, 2013 at 4:28 am | Permalink

      I was perusing some material online about turtle evolution. What is it about Milleretta that does not put it in line (even at an early step)?

      • heleen
        Posted June 3, 2013 at 6:05 am | Permalink

        Primitively anapsid.
        And far too early.
        At least if the archosaur sistergroup status of turtles is accepted, and the cited paper of Wang in Nature Genetics leaves little doubt.


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