[JAC: In response to my own and other readers' questions about turtle morphology and evolution, Greg kindly put up another post to clarify matters.]
by Greg Mayer
To really appreciate what turtles have done with their shells, it helps to see into one. So here’s a view into a turtle’s shell. The shell has been cut parasagitally, to the right of the midline, so we can see the vertebrae, but the rest of the skeleton– head, neck, limbs, girdles, and tail– are left intact so we can see their relation to the shell. (As Turtle Dundee once said, “That’s not an evolutionary novelty– that’s an evolutionary novelty.”)
Note that the shoulder and pelvic girdles are both within the dome of the carapace. And in turtles, the shoulder girdle is a bigger affair than it is in mammals. Turtles not only have a scapula, but also a coracoid as a major bony element, plus turtle scapulas are two pronged affairs with an acromial process nearly as big as the main part of the scapula itself, so that the whole girdle is a tri-radiate structure.
The shell itself is composed of epidermal, dermal, and deeper skeletal elements, and all three can be seen in this view. The horny scutes on the exterior of the shell, made of the same material as scales and fingernails, are epidermal, with a layer of live cells between the scutes and the bone. The bony part composes parts of the deeper axial skeleton: the vertebrae and ribs, which are preformed in cartilage during development; and the more superficial dermal bones, that ossify directly in the dermis without being preformed in cartilage. The plastron (bottom shell) consists of just epidermal and dermal elements. The plastral bones may be homologous to some of the dermal bones of the shoulder girdle (clavicle and interclavicle) and the gastralia of other reptiles.
As mentioned in the previous post, what the new paper by Lyson and colleagues (see previous turtle post for references) has especially done is to try to interpret the disputed turtle precursor Eunotosaurus in terms of the developmental processes proposed to underlie the evolution of the shell as seen in the undoubted turtle precursor Odontochelys and more derived turtles. Much of that recent developmental work has come from the Laboratory of Evolutionary Morphology at the RIKEN Center for Developmental Biology in Japan, especially this 2009 paper by Hiroshi Nagashima and colleagues (see additional figures in RIKEN’s press release; and a nice review by Shigeru Kuratani and colleagues from 2011).Lyson and colleagues integrate Eunotosaurus into Nagashima and colleagues’ developmental scenario by proposing that the rib broadening seen in Eunotosaurus is homologous with that in Odontochelys and Proganochelys. One problem that I see with this attempt is that, if I’m interpreting Eunotosaurus correctly, the distal ends of its ribs curve ventrally and tuck in around the lateral edge of the body, while in turtles the ribs grow out straight to the sides towards a feature in the embryo called the carapacial ridge; this is how, in fact, the scapula gets inside the ribs. It could be argued, though, that this straightness is a later evolved feature, although it’s the straight lateral growth that is associated with getting the cartilaginous ribs associated withe bone-producing dermis that produces the broad plates of bone.
To stress again how profound are turtles’ morphological changes in skeletal and soft tissues, and how they ramify throughout its physiology, ecology and behavior, let me quote from the famous morphologist and paleontologist Rainer Zangerl (1969; and who, in the quoted paper, also refers to the development of the turtle shell as “astounding”):
This shell did not merely cover the pre-existing anatomical structures of the body, but it modified them profoundly. The drastic alteration was probably the consequence of an intimate involvement of the dermal shield with parts of the axial skeleton (vertebrae and ribs) and with dermal portions of the primary skeleton (clavicles, interclavicle and gastralia). The restructuring had far reaching morphological, physiological, evolutionary, and ecological consequences . Anatomically, the presence of a rigid shell led to extensive modification of the structure of the body wall, and to the differentiation of the locomotor apparatus, of the neck region and of the copulatory mechanism, to mention just a few . Functionally it necessitated changes in the mode of respiration ; it impaired locomotion, especially on the ground, and restricted aquatic locomotion to the “paddle types” ; it delimited the storage capacity of the body for air, food, water, fats (oil in the shell bones of sea turtles), and waste materials . It probably affected the permeability of the body wall and hence modified the capacity of the animal to retain water . It drastically modified the behavioral pattern of the animal.
Kuratani, S., S. Kuraku, and H. Nagashima. 2011. Evolutionary developmental perspective for the origin of turtles: the folding theory for the shell based on the developmental nature of the carapacial ridge Evolution & Development 13:1-14. abstract
Nagashima, H. et al. 2009. Evolution of the turtle body plan by the folding and creation of new muscle connections Science 325: 193-196. pdf
Zangerl, R. 1969. The turtle shell. Biology of the Reptilia 1: 311-339. pdf