Various aspects of turtle evolution are the subject of vigorous debate among vertebrate palaeontologists. A newly described fossil species, the oldest yet discovered, adds grist to the mill.
During the Late Triassic, some 220 million years ago, primitive turtles about 40 centimetres in length were preserved in sedimentary deposits in what is now southwestern China. These fossils are examples of a new species of a very early turtle, named Odontochelys semitestacea, which is described by Li et al. on page 497 of this issue1 and which will change ideas about turtle origins and the evolution of their striking body plan.
Turtles are remarkable animals2. They have a horny beak rather than teeth, and a shell like that of no other animal, one that is composed of an upper carapace and a lower plastron, jointed together by a bony bridge. The shell is a composite structure derived from ribs, parts of the shoulder girdle and specialized dermal bones. This precludes the typical costal respiration of tetrapods, in which movable ribs allow the chest cavity to expand and contract. Turtles have overcome this obstacle by having the muscles that control breathing use the limb pockets at the borders of the shell. This shell has become modified as turtles diversified and adapted to terrestrial, amphibious and aquatic environments (Fig. 1). The evolutionary relationships and ecology of turtles through time, and the developmental and evolutionary origins of the shell, are major controversies in studies of vertebrate evolution.
Previously, the fossil evidence for turtle origins came largely from Proganochelys quenstedti from Germany, which lived between 204 million and 206 million years ago, and other less-well-known early turtles. Proganochelys is known from several skeletons. It has a massive shell and spiked armour on the neck and tail, but also retains teeth on the roof of the mouth and has other primitive features in the skull and skeleton. Its osteology has been used to propose3 that turtles are related to pareiasaurs, a group of extinct parareptiles that includes species with extensive dermal armour. And on the basis of evidence from Proganochelys and its close relatives from the Late Triassic of Argentina, Germany and North America, it has been suggested that the earliest turtles lived in terrestrial environments4,5.
The discovery and description of Odontochelys by Li et al.1 challenges these hypotheses. Odontochelys is not only the oldest recognizable turtle, but its skull also shows that it is more primitive than other turtles because it retains a full complement of marginal teeth, rather than a beak, and also possesses free sacral ribs and a long tail. Its osteology contradicts the view that turtles have pareiasaurian affinities, and, along with molecular data, supports evolutionary hypotheses that they are closely related to another group, the diapsid reptiles6,7. Li et al. argue that Odontochelys represents an early stage in the evolution of the turtle shell because the plastron is present and fully developed, but the carapace is apparently absent, with only dorsal ribs and neural (midline) dermal ossifications present. The authors infer, therefore, that the plastron evolved before the carapace, reflecting the timing of shell ossification during embryonic development in living turtles.
Although this evolutionary scenario is plausible, we are particularly excited by an alternative interpretation and its evolutionary consequences. We interpret the condition seen in Odontochelys differently — that a carapace was present, but some of its dermal components were not ossified. The carapace forms during embryonic development when the dorsal ribs grow laterally into a structure called the carapacial ridge, a thickened ectodermal layer unique to turtles8. The presence of long, expanded ribs, a component of the carapace of all turtles, indicates that the controlling developmental tissue responsible for the formation of the turtle carapace was already present in Odontochelys. The expanded lateral bridge that connects the plastron to the carapace in other turtles is also present, implying that the plastron was connected to the laterally expanded carapace. Thus, an alternative interpretation is that the apparent reduction of the carapace in Odontochelys resulted from lack of ossification of some of its dermal components, but that a carapace was indeed present.
This interpretation of Odontochelys leads us to the possibility that its shell morphology is not primitive, but is instead a specialized adaptation. Reduction of dermal components of the shell in aquatic turtles is common: soft-shelled turtles have a greatly reduced bony shell and have lost the dermal peripheral elements of the carapace. Sea turtles and snapping turtles have greatly reduced ossification of the dermal components of the carapace, a condition similar to that seen in Odontochelys.
From the geological context of their fossils, Li et al.1 conclude that Odontochelys lived in a shallow marine environment. That, combined with similarities between its carapace and the reduced shells of modern aquatic turtles, leads us to propose that the absence of most of the dermal carapace in Odontochelys is a secondary loss associated with aquatic habits rather than a primitive condition, as inferred by Li and colleagues. Given the similarities between its shell morphology and early growth stages in living turtles, a simple truncation of carapace ossification, in which the adults retained juvenile features (paedomorphosis), could have been a developmental mechanism in the evolution of the reduced carapace.
Regardless of the primitive or derived nature of its shell, Odontochelys is in evolutionary terms the most 'basal' turtle yet found. Its discovery opens a new chapter in the study of the origins and early history of these fascinating reptiles. Both interpretations alter our views of turtle evolution: Odontochelys either represents the primitive ecology for turtles, consistent with the hypothesis that the turtles' shell evolved in aquatic environments7, or it represents the earliest turtle radiation from terrestrial environments into marine habitats. Either way, these ancient turtles demonstrate yet again the value of new fossil discoveries in changing our understanding of vertebrate history.
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