Evolution of the turtle bauplan: the topological relationship of the scapula relative to the ribcage

Abstract

The turtle shell and the relationship of the shoulder girdle inside or 'deep' to the ribcage have puzzled neontologists and developmental biologists for more than a century. Recent developmental and fossil data indicate that the shoulder girdle indeed lies inside the shell, but anterior to the ribcage. Developmental biologists compare this orientation to that found in the model organisms mice and chickens, whose scapula lies laterally on top of the ribcage. We analyse the topological relationship of the shoulder girdle relative to the ribcage within a broader phylogenetic context and determine that the condition found in turtles is also found in amphibians, monotreme mammals and lepidosaurs. A vertical scapula anterior to the thoracic ribcage is therefore inferred to be the basal amniote condition and indicates that the condition found in therian mammals and archosaurs (which includes both developmental model organisms: chickens and mice) is derived and not appropriate for studying the developmental origin of the turtle shell. Instead, among amniotes, either monotreme mammals or lepidosaurs should be used.

Figure 1.

(a) Illustrations and (b) photographs of the shoulder girdle of taxa representing each of the major amniote clades (Mammalia, Monotremata, Theria, Testudines, Lepidosauria, Squamata, Archosauria, Aves and Crocodylia). The scapula is situated dorsal to the ribcage in therian mammals and archosaurs, including the two developmental model organisms: the house mouse and the domestic chicken. A vertically oriented scapula, anterior to the ribcage is found in turtles, the basal most stem turtle Eunotosaurus africanus [21], the stem turtle Proganochelys quenstedti, lepidosaurs, monotreme mammals and the amphibian Rana catesbeiana, indicating this is the basal amniote condition. The numbers represent the three hypotheses for turtle origins: 1, turtles as sister to diapsids (lepidosaurs + archosaurs) is supported by most morphological [21,22] and developmental data [23]; 2, turtles as sister to lepidosaurs is supported by some morphological [24] and molecular data [25]; 3, turtles as sister to archosaurs is supported by nuclear and mitochondrial genetic data [26].