How the turtle got its shell – Pharyngula.
by PZ Myers shared by A.E.
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.