Pharyngula

How the turtle got its shell

In my post bashing that silly article claiming to have figured out how endoskeletons evolved from exoskeletons, there was a good question buried in the comments, and I thought I’d answer it.

Are there any models pulled out of arses which explain the turtle’s unique skeleton?

Yes! I mean, no, not pulled out of arses, but there is a lot of really good and persuasive research that uses evidence to show how the turtle skeleton evolved.

First, I can see how this question popped up in a discussion of the evolution of endo/exoskeletons: the turtle shell is an excellent example of an exoskeleton that evolved in a vertebrate lineage at some time in the Triassic, so it’s definitely relevant. Also, turtle skeletons are a bit weird. The shell is made up of the animal’s ribs fused to plates of dermal bone — that is, sheets of bone formed directly by the ossification of the dermis of the skin (an exoskeleton!) rather than by ossification of cartilaginous centers deeper in the body (endoskeletons). The ribs and vertebrae are ‘endoskeletal’, formed by chondrogenesis and ossification, while the scutes or plates of the shell are dermal bone, so this structure also represents the fusion of two kinds of bone. The confusing bit is the scapula, or shoulder blade; yours, as you can tell, is outside the rib cage, but in turtles, the scapula is located inside the ribs of the shell. So somehow the ribs and scapulae in turtles have flipped their relative positions, which sounds like a radical transformation, and it’s not at all clear how you could do that gradually in evolution.

Here is a comparative diagram of cross sections of a turtle and a chicken to illustrate the difference. The ribs (r) are in light green while the scapula (sc) is in dark red. Notice how the shell makes a kind of shield over the whole turtle, with the scapula and whole shoulder girdle underneath and the forelimbs attached to it? While in the chick the ribs are the deepest bones, with the scapulae on the outside? How did that that happen?


Comparison of deep (as, serratus anterior; lsr, levator scapulae and rhomboid complex) and superficial (ld, latissimus dorsi; p, pectoralis) muscles connecting the trunk and shoulder girdle/forelimb.

The answer, as you might guess, comes from looking at how it gets that way in the development of modern turtles, because as you all know by now, developmental biology rules.

The early turtle embryo looks like a generic tetrapod embryo. The first sign of a significant morphological difference is the appearance of a thickened ridge of skin between the limbs, which eventually expands to form a ring marking the margins of the shell. This structure is called the carapace ridge (CR), and you can see it in the cross sections of embryos at two different ages below.


Carapace ridge and rib entry into the CR of Trachemys scripta. Mallory’s triple stain of embryos sectioned serially on (A) day 23 and (B) day 29 of incubation. The CR has formed by day 23, but rib entry (arrow in (B)) is not seen until a few days later. The sections are taken through extended limb buds (L) that can be seen for comparison.

Note that it appears as the limbs are forming (in A), but before all the bony bits have ossified — no ribs, no scapula yet. The ribs begin to grow outward from the vertebrae, and in most vertebrates they would begin to arc downwards, to wrap around the body cavity, but in turtles something different happens: they are captured by the CR and grow out to the sides. Not down, but laterally, broadening the turtle’s body. As you can see in B above, this is happening as the bones ossify, and before the shoulder girdle has fully formed.

What this means is that as the ribs grow out towards the scapula, and as the scapula extends upwards towards the ribs, where in other animals the scapula would slide upwards over the ribs, in the turtle the ribs are instead pulled up and out over the scapula.


Schematic transverse views to compare the topography of ribs, body wall (lbw), and forelimb bud (lb) with shoulder girdle between the embryos of turtles (I) and generalized amniotes (J). Generally, the amniote ribs grow ventrally into the lateral body wall, whereas in the turtle, they are arrested in the axial part (ax), growing toward the CR.

The relationship of ribs and scapula are flipped around, but notice that appropriate connections are all retained; “as”, in yellow, is the serratus anterior muscle, which attaches from the top of the scapula to the ribs in general tetrapods, and also still connects the top of the scapula to the ribs in the turtle. It’s a perfectly natural retention of other attributes of the system while one other relationship is changed.

Embryologically, this all makes sense — it’s a relatively simple shift due to a change in one tissue. But does it make sense phylogenetically? Yes — meet Odontochelys, a Triassic proto-turtle.

It’s a transitional form! It doesn’t have the full turtle shell, but what it does have is the broadened body plan, a flattened back with a shield-like pattern of ribs and dermal bone between the limbs, and a plastron, or ventral shell (it also has teeth, hence the name). It doesn’t have it’s scapula tucked beneath the shell; instead, the ribs/shell is pulled back. In the modern turtles, those ribs have been pulled further laterally and forward to lie over the scapula. These details are all shown in this diagram.


Evolution of the turtle body plan. (Top) A hypothetical sequence of changes in musculoskeletal connectivities. The scapula is red, AS muscle orange, latissimus dorsi blue, and pectoralis green. In Odontochelys, the AS would have connected the scapula and distal tips of anterior ribs antero-posteriorly. The pectoralis would have connected the humerus and the plastron (pl). (Bottom) A phylogenetic consideration. In Odontochelys, the CR (red broken line) may have developed only temporarily and incompletely in the embryo. In the modern turtle, the CR (red solid line) forms a complete circle, inducing the fan-shaped growth of the ribs. dc, dermal carapace.

See? Not as hard a problem as you might have thought, and all the scars of evolution remain marked in the turtle embryo and in the fossil record.

Oh, also, I just have to leave you with this really beautiful drawing of a turtle embryo from the Gilbert paper.


Gilbert SF, Loredo GA, Brukman A, Burke AC (2001) Morphogenesis of the turtle shell: the development of a novel structure in tetrapod evolution.. Evol Dev 3(2):47-58.

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

Nagashima H, Sugahara F, Takechi M, Ericsson R, Kawashima-Ohya Y, Narita Y, Kuratani S (2009) Evolution of the turtle body plan by the folding and creation of new muscle connections. Science 325(5937):193-6.

Comments

  1. #1 TychaBrahe
    August 30, 2012

    Whenever I see things like this, I marvel at the simplicity and elegance through which nature, seeking the least energy-expensive solution to changes in the availability of environmental niches. And I think how annoying and unsatisfying and crude are explanations like, “God just did it.”

  2. #2 David Marjanović
    Museum für Naturkunde, Berlin
    August 30, 2012

    In the second-to-last figure (“Evolution of the turtle body plan”), the shoulders of Bob the Basal Amniote are too mammal- or birdlike. They’re mounted too high up and too far back; as you can see, the upper arm threatens to clash with the ribcage every time it moves. The shoulder blades should overlap the ribs much less and look more like in Odontochelys, just not quite as vertical.

    This is clear from well-preserved fossils of early amniotes as well as from many extant amniotes. Even in birds, where the shoulder blades proper (the scapulae) are horizontal and overlap many ribs, the coracoids (the long green bars that extend to the midline in the first figure) lie in front of the ribcage.

    The second-to-last figure also neglects to mention that Odontochelys did have a carapace. It had the extra plates on top of the vertebrae and the extra plates on top of each rib; it just so happens that the carapace wasn’t very tightly sutured together, so that, in the fossils, the plates on top of the vertebrae are slightly separated from the vertebrae and each rib, with its plate on top, has separated and points in a different direction.

  3. #3 David Marjanović
    Museum für Naturkunde, Berlin
    August 30, 2012

    In the drawings, blue is cartilage and red is bone; this is a common way of staining skeletons.

  4. #4 Herly cyning
    August 31, 2012

    Thanks for the post. I really enjoy these which give a glimpse into the simplistic yet paradoxically intricate processes of evolution. Sharing.

  5. #5 Kobe Boy
    August 31, 2012

    There are some nice animations that show this clearly – they good to use in presentations etc. http://www.cdb.riken.jp/en/05_development/0506_turtle01.html .

  6. #6 Stephen
    New Hampshire
    August 31, 2012

    I’m curious, fascinated really, at what force or threat could encourage the evolution of a creature like the Odontochelys.

    Evolution doesn’t seem to work with an end-goal in mind; any change or mutation that is kept needs to make sense, have a benefit or at least be unobtrusive, to that organism’s individual lifespan.

    So my question to those who know the subject is, what benefit is there for this prehistoric proto-sea turtle to have a flattened body, so well-prepared to be encased in a shell?

    Clearly the turtle as we have it today enjoys a strong defense and a lifestyle adapted around its form, but especially for transitional forms… “why?” What did the individual Odontochelys gain by being more broad and flat than its unaltered cousins?

    Obviously that kind of question can be asked of almost any “transitional form” seen in evolution, but hopefully an answer pertaining just to our friend the turtle will satisfy me.

  7. #7 Eric Elliott
    California
    August 31, 2012

    This has put me in mind of the horned lizard (or horny-toad) of the American Southwest. It has a flattened and broadened body plan and is covered in spikes which may built by ossification of the dermis. Now I’m wondering about its ribs and scapulae… can anyone point me to information on this critter?

  8. #8 Zach Miller
    Anchorage
    August 31, 2012

    Now, there is the possibility that Odontochelys is actually transitioning away from having a complete upper shell to having a “leatherback”-style shell, as an aquatic turtle. So it might not tell us too much about the initial evolution of the shell, but rather how the shell is LOST.

    But it could also be an ancestral turtle. Either way, it’s an awesome critter.

  9. #9 David Marjanović
    Museum für Naturkunde, Berlin
    September 1, 2012

    So my question to those who know the subject is, what benefit is there for this prehistoric proto-sea turtle to have a flattened body, so well-prepared to be encased in a shell?

    Clearly the turtle as we have it today enjoys a strong defense and a lifestyle adapted around its form, but especially for transitional forms… “why?” What did the individual Odontochelys gain by being more broad and flat than its unaltered cousins?

    As I explained above, don’t blame Odontochelys, because it already has a shell, its components just aren’t tightly sutured, and the outer ring of bone plates is missing. It’s also not actually a particularly flat animal; it just has somewhat straighter ribs than usual. Compare Eunotosaurus (google for it).

    This has put me in mind of the horned lizard (or horny-toad) of the American Southwest. It has a flattened and broadened body plan and is covered in spikes which may built by ossification of the dermis. Now I’m wondering about its ribs and scapulae… can anyone point me to information on this critter?

    Again, Google can. I’m sure any dermal ossifications are outside the shoulder girdle, but the ribs are behind the shoulder girdle where they belong.

  10. #10 Jim Baughman
    West Hollywood CA USA
    September 1, 2012

    TychaBrahe said:

    Whenever I see things like this, I marvel at the simplicity and elegance through which nature, seeking the least energy-expensive solution to changes in the availability of environmental niches. And I think how annoying and unsatisfying and crude are explanations like, “God just did it.”

    Yet another example of Occam’s Razor at work.

  11. #11 Skoki
    United States
    September 1, 2012

    How interesting to know how turtles got its shell. I have not known this information up until this post. This made me think of also how businessmen have have come of ideas about their businesses, such as http://www.bbjlinenstore.com!

  12. [...] How the turtle got its shell – Pharyngula. [...]

  13. #13 Sage Carrington
    September 4, 2012

    Thanks for the post. This is very insightful now I know why turtles got their shells. Nature is so wonderful and full of mystery.

  14. #14 Scott Gilbert
    Swarthmore, PA
    September 4, 2012

    Thanks for using some of my research here. I often begin my talks, especially those to general audiences, with quotations from the creationist literature, including, “Turtles appear abruptly in the fossil record. This is a problem not easily explainable by the evolutionist, but it is easily explained in the Biblical creation model.” from the current turtle exhibit at the Creation Museum. It actually isn’t as difficult as one might think to get a turtle, once the ribs travel the wrong way and get into the skin!

    Thanks and best wishes,
    Scott

  15. #15 Howard Brazee
    Colorado
    September 6, 2012

    I wonder how often an evolutionary change is not explained by incremental changes in the result – but better explained by looking at the structure of the chromosomes. A gene migrating by touching a different part of the chromosome might have a quantum change in results.

  16. #16 David Marjanović
    Museum für Naturkunde, Berlin
    September 6, 2012

    Usually, it doesn’t matter at all which chromosome a gene is on. The only exception is when it gets too close to an enhancer or silencer of another gene.

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