Among limbed (and many limbless) amniotes, elements of the shoulder girdle and sternum partially encircle the ribcage to form a structural yoke that indirectly connects the forelimbs to the axial skeleton. Herein referred to as the pectoral apparatus, this skeletogenous nexus demonstrates enormous taxonomic variation and multiple (independent) instances of elements appearing to have been lost and/or insensibly combined. Furthermore, the pectoral apparatus includes both dermal and replacement bones. These features underline the difficulty of determining homology for various pectoral components.
Historical observations from both the fossil record and ontogenetic studies initially provided a well-structured scenario of the morphological transformation of mammals from the earliest stem synapsids. However, subtle yet important evolutionary details are only now being understood through the use of experimental methods and detailed developmental analyses at the level of the cell.
Among reptiles, sister group to mammals, the situation is less clear. Despite an increased knowledge of embryology and phylogenetics, and an abundance of new palaeontological data, the prevalent hypothesis regarding the homology of the reptilian coracoid has remained largely unchanged for more than 80 years. Unlike in mammals, there has been little consideration given to the development of the reptilian pectoral apparatus as a whole. This paper has three main objectives: (1) to review the morphology and development of the pectoral apparatus in both extinct and extant amniotes; (2) to re-address homology of the reptilian coracoid; and (3) to re-evaluate the scenario of coracoid evolution in amniotes.
Early evolution of the pectoral apparatus – a brief review
Except for the sternum, most pectoral elements were present in osteichthyians well before the appearance of limbs. Among non-digit-bearing members (Fig. 1A) this region is dominated by dermal elements, including the cleithrum, clavicle and unpaired interclavicle. These components are linked to the caudalmost portion of the head skeleton overlying the gill chamber. Articulation with the humerus occurs at the relatively small and laterally obscured primary girdle, the undivided scapulocoracoid. [The primary girdle includes those elements preforming in cartilage that develop before the dermal pectoral contributions. This includes the scapulocoracoid and all derivatives thereof.]
With the evolution of digit-bearing limbs (Fig. 1B) elements linking the head skeleton with the pectoral apparatus were lost, resulting in a decoupling of the dermal girdle from the skull (Clack, 2002). Furthermore, the once modest scapulocoracoid adopted a more prominent and laterally facing profile. Further reduction of the dermal girdle (in particular the cleithrum) and enlargement of the primary girdle characterizes more deeply nested non-amniote tetrapods (Fig. 1C). Among these and more derived tetrapods, the singular scapulocoracoid is partitioned into two elements, a dorsal scapula and a ventral coracoid.
Among basal amniotes (Fig. 1D,E) the lone coracoid is replaced by two discrete components, a cranial procoracoid and a caudal metacoracoid (see Table 1 for a listing of coracoid synonyms). For modern taxa, the scapula is the most widely conserved element of the pectoral apparatus, absent only in some lepidosauromorphs (e.g. ophidians). Monotremes are unique in retaining both the procoracoid and the metacoracoid, whereas therian mammals (marsupials and eutherians) and reptiles (including birds) each maintain only one of the two elements; in therians the procoracoid no longer forms a discrete entity and the metacoracoid is a rudiment that fuses with the scapula, giving rise to the coracoid process. Conversely, in reptiles it has long been assumed that the metacoracoid has disappeared and only the procoracoid remains. The procoracoid is understood to be equivalent to the coracoid of non-amniote tetrapods. Consequently, modern authors typically refer to this element in reptiles as simply the coracoid (e.g. McGonnell, 2001), a designation adopted hereafter to avoid unnecessary confusion.
|Cranialmost coracoid||Caudalmost coracoid||Therian coracoid process||Reptilian coracoid|
|Williston, 1911, 1925||procoracoid||metacoracoid||coracoid (=procoracoid)||procoracoid|
|Gregory & Camp, 1918†||epicoracoid||coracoid||coracoid||coracoid|
|Klima, 1973, 1987||procoracoid||metacoracoid||metacoracoid||procoracoid|
In comparison with the rest of the pectoral apparatus, the sternum is often poorly preserved or entirely absent from fossil taxa. This observation is usually explained in the context of histology; unlike other pectoral components that ossify, the sternum often remains cartilaginous. Notwithstanding its poor palaeontological representation, the sternum is considered characteristic of virtually all tetrapods [including lissamphibians and most amniotes, with the exception of turtles (although see below) and ophidians], with preserved material dating back to at least the Late Permian (256–248 million years ago; Vaughn, 1955).
A question of homology – the coracoid conundrum
Questions concerning the homology of various pectoral elements rank as some of the oldest in comparative anatomy. In a celebrated series of woodcuts, Belon (1555) compared the skeletons of a man and a bird. Using a series of labels, Belon accurately identified the majority of the homologous elements between the two specimens. One of his few misinterpretations was to pair the avian coracoid with the human clavicle. Although this particular hypothesis has long since become abandoned, the homology of the coracoid element(s) remained as a topic of considerable debate for early anatomists.
Prior to the late 1800s, it was commonly held that of the two coracoid elements present in basal amniotes and monotremes, only the caudalmost element, the metacoracoid, was retained by modern reptiles and therians (e.g. Parker, 1868; Flower, 1876; Fig. 2A). The cranialmost element, the procoracoid, was assumed to be lost. Soon, however, new developmental and palaeontological evidence began to confuse the issue. Howes (1887, 1893) observed that the developing scapula of a generic rabbit consisted of three discrete centres – one giving rise to the blade and scapular spine, one forming the coracoid process and one contributing to the glenoid. He interpreted these centres as corresponding to the scapula, procoracoid and metacoracoid of monotremes, therefore suggesting that the procoracoid was not lost (Fig. 2B).
An alternative opinion was expressed by Lydekker (1893), who compared the development of the coracoid process of a sloth with the dual coracoid elements of what was then considered a basal reptile (namely †Dicynodon sp., now considered to be a basal synapsid). He concluded that the procoracoid was homologous with the therian coracoid process of the scapula, and that the caudalmost element, what he named the metacoracoid, was the only coracoid element of reptiles (Fig. 2C). This was later rebutted by Broom (1899), who returned to the notion that modern amniotes, with the exception of monotremes, had lost the procoracoid.
Although aspects of the debate continued, e.g. Gregory & Camp (1918; see also Hanson, 1920) argued that basal amniotes originally had three coracoid elements – the epicoracoid, coracoid and metacoracoid, the work of Williston (1911, 1925) is often cited as the basis for our modern interpretation of reptilian coracoid homology (Broom, 1912; Case & Williston, 1913; Hanson, 1920; Romer, 1922, 1956). Williston examined a variety of what were then considered to be fossil ‘reptilian’ taxa (most of which have since been recollected as Amniota outgroups) and noted that whereas the scapula and procoracoid were generally fused, the metacoracoid, if present at all, was often poorly sutured or completely unattached. Williston and others (e.g. Broom, 1912; Case & Williston, 1913) interpreted this as evidence for the anagenetic disappearance of the metacoracoid among modern reptiles.
Adopting the interpretation of Williston, Romer (1956; see also 1922) expanded the argument. Observing that non-amniote tetrapods (e.g. †Seymouria spp., lissamphibians), therians and modern reptiles have only one coracoid element, whereas some basal amniotes (e.g. †Dimetrodon spp.; see below) had two. Romer formulated an evolutionary scenario (Fig. 3) in which the procoracoid was the primitive element. This procoracoid was retained by reptiles and some synapsids (e.g. monotremes). Among basal synapsids a second more caudal element, the metacoracoid, developed. In therians the procoracoid disappears whereas the metacoracoid is retained, albeit in a reduced form as the coracoid process of the scapula. Among those fossil reptiles that demonstrated both coracoid elements, Romer suggested that for some taxa this reflected a proximate genealogy with synapsids. For others he stated ‘[w]e must assume either that the general reptile stem early acquired a second coracoid element which survived only in synapsids, other reptiles rapidly losing it again, or that parallelism occurred, with the development of a second coracoid in two or more lines. The second assumption is the more reasonable, but the situation is far from clear.’ (Romer, 1956, p. 309). Indeed, the situation remains uncertain, for as alluded to above, revised phylogenetic hypotheses of Amniota (Fig. 4) have weakened some of the fundamental underpinnings to the theory of reptilian coracoid homology as established by Williston (1911, 1925).
Elucidating the evolution and development of a morphological complex such as the pectoral apparatus is a daunting task. Variation in the embryological origin, adult phenotype and overall number of constituent elements often leads to confusion regarding each component's anatomical and phylogenetic identity. Atchley & Hall (1991) created a model for understanding complex structures that begins with the identification of fundamental developmental units. At the cellular level, these fundamental developmental units are cell condensations characterized as ‘… the raw material of morphology …’ (Hall & Miyake, 1992, p. 108). All organs, bones included, begin as aggregations of cells (Atchley & Hall, 1991; Eames et al. 2003), with those condensations presaging the skeleton referred to (collectively) as the membranous skeleton (Grüneberg, 1963; Hall & Miyake, 1992). Unlike adult skeletal elements, which may fail to form or become insensibly assimilated into other bones and cartilages, cell condensations are present (at least briefly) as discretely recognizable units. During both development and evolution, cell condensations may experience variation as a result of changes in mitosis (cell proliferation), identity (differentiation), the size of the aggregation, and/or localized heterochrony (Atchley & Hall, 1991; Hall & Miyake, 1992; Dollé et al. 1993). Consequently, cell condensations provide a useful means for establishing homology of elements in a multipartite structure (Hall & Miyake, 1992; see also Klima, 1973, 1987), and are critical for the study of the evolution and development of the pectoral apparatus.