On the absence of sternal elements in Anchiornis (Paraves) and Sapeornis (Aves) and the complex early evolution of the avian sternum

Compensatory Morphologies.

It is commonly accepted that Archaeopteryx and Sapeornis were volant (4, 34), thus they may have compensated for the absence of a sternum through other morphologies. In crocodilians, several muscles attach to the gastralia and the cranial pair of gastralia articulates with the sternum (35). This plesiomorphic condition is retained, and the gastralia are observed to articulate with the sternum in some theropods and basal birds (Jeholornis, Confuciusornis, Eopengornis, Parabohaiornis; SI Appendix, Fig. S11 A and B). Gastralia are notably highly modified within Theropoda compared with other groups of amniotes, and proximally fused gastralia have been proposed to function similarly to the sternum in tyrannosaurids (35). Gastralia are absent in living birds, considered functionally redundant in the presence of the large ossified sternum that characterizes Neornithes (35), thus bridging the possibility that the large gastral basket in Sapeornis (5) may have functioned as a compensatory feature in the absence of a sternum and that the extensive gastral basket of basal birds with sterna may also have participated in supporting or reinforcing the sternum and the flight muscles (SI Appendix, Fig. S1). However, the absence of a sternum in Sapeornis and Anchiornis would have left the gastral basket free, suggesting it would have lacked the rigidity to support large flight muscles. If the fused cranial row in tyrannosaurids functioned similar to the sternum of more derived theropods (35), potentially the same may be true regarding Archaeopteryx and Sapeornis. Although the first pair of gastralia in Sapeornis appears to be similarly fused, the gastral basket is otherwise void of modifications to suggest it was the attachment site of robust musculature. We do not fully understand how the gastralia may have supported the musculature necessary for volant activity, but in the absence of a sternum, these muscles clearly would have had to find attachment elsewhere.

The morphology of the coracoid in Sapeornis also differs from that of other basal birds in which this bone definitively articulates with a sternum. Potentially the large coracoid of Sapeornis may also have compensated for the absence of the sternum in some way (7). Compared with other Cretaceous birds, the coracoid is proportionately wide and short (SI Appendix, Fig. S2E). The morphology in Sapeornis, which is similar to that of Anchiornis (SI Appendix, Fig. S2C) and Archaeopteryx, is plesiomorphic to a larger group of theropods, including nonavian paravians with an ossified sternum. Caudipteryx, with its simple oval sternal plates, also has a plesiomorphic proportionately short coracoid (SI Appendix, Fig. S2B). In contrast, the supposedly volant Microraptor has a proportionately more narrow and elongate coracoid relative to other derived maniraptorans, somewhat resembling that of basal birds such as Jeholornis (SI Appendix, Fig. S2 A and D and Table S4). It is interesting to note that in all supposedly volant taxa with sterna (Microraptor, Jeholornis, Confuciusornithiformes, and ornithothoracines), the coracoid is elongated relative to the plesiomorphic condition, suggesting these two features are correlated.

In the plesiomorphic theropod coracoid morphology, present in Archaeopteryx and Sapeornis, the distal margin is convex, especially along the distolateral margin, whereas in Microraptor and more derived avian taxa, the sternal margins are straight for articulation with the sternum (e.g., Jeholornis, Confuciusornis, ornithothoracines). This convexity is particularly pronounced in troodontid taxa without sterna (e.g., Mei long, Anchiornis), which also have proportionately short coracoids (slightly wider than long; SI Appendix, Table S4). Proximally, the sternolateral margin of the coracoid in Sapeornis is expanded along the distal half (SI Appendix, Fig. S2E), which may also have served to provide a larger proximal attachment surface for the pectoral muscles. Unfortunately, this hypothesis is also not supported by any local rugosity, tubercle, or other indicator on the coracoid to suggest that this convexity was, in fact, a site of muscle attachment.

The Absence of Sternum in Archaeopteryx.

The iconic “first bird” Archaeopteryx is known from 10 published skeletal specimens (36). Of these specimens, six are nearly complete and articulated (the Berlin, Eichstätt, London, Munich, Solnhofen, and Thermopolis specimens), four of which also preserve feather impressions. No specimen preserves evidence of sternal plates or ribs, although a complete or nearly complete gastral basket is preserved in several specimens (well preserved in the Berlin, Eichstätt, Munich, Solnhofen, and Thermopolis specimens); preservation of the latter, which is formed of numerous small, delicate bones, suggests that the absence of sternal elements is not taphonomic. What was described as the sternum in the Munich specimen (2) has been reinterpreted as part of the coracoid (3). However, because this element has such a centripetal role in neornithine-powered flight and is present in other nonavian maniraptorans, it was considered that a cartilaginous sternum was present (37). Because of the small sample size (n = 10), the absence of an ossified sternum may potentially be due to preservational or ontogenetic bias. Archaeopteryx is in many ways morphologically similar to the nonavian maniraptorans Anchiornis and Xiaotingia (13). These taxa share more than the absence of a sternum in all known specimens: They have similar skull morphologies with small conical unserrated teeth; a short, quadrangular coracoid; a tetra-radiate ischium; and a gastral basket composed of 12–14 pairs of gastralia. These taxa have even been resolved together in an “archaeopterygid” clade outside of Dromaeosauridae + Troodontidae (10), highlighting the similarity between these taxa. We have provided convincing evidence that the absence of an ossified sternum in Anchiornis is not due to ontogenetic or preservational bias; we further propose that in light of the excellent preservation of soft tissue in numerous specimens, it is safe to conclude a chondrified sternum was also absent. Considering the morphological similarity between Anchiornis and Archaeopteryx and the absence of a sternum in Sapeornis, we argue a chondrified sternum may also have been absent in the earliest bird, Archaeopteryx.

Sternal Morphology and Avian Origins.

Sternal plates (unfused and cartilaginous) are plesiomorphic for the tetrapod crown group, only known to be lost in turtles and various limbless clades like snakes and caecilians (1). We have provided strong evidence that Anchiornis and Archaeopteryx, taxa inferred to cross the dinosaurian-avian transition (Fig. 2), had no sternum. This observation has important repercussions for theories regarding volant activity in the earliest birds. Given the phylogenetic proximity of Troodontidae to the base of Aves and the absence of a sternum in Archaeopteryx, it is most parsimonious to interpret that this feature was the plesiomorphic avian condition. Its absence in the basal pygostylian Sapeornis may further suggest the avian lineage leading to Ornithothoraces also did not have a sternum; this observation suggests the sterna in Jeholornis and Confuciusornis could have evolved independently and may not be strictly homologous. Alternatively, current popular phylogenetic hypotheses regarding basal bird relationships are incorrect (7); some analyses have resolved Sapeornis as basal to Jeholornis (38, 39), which would suggest a single origin event for the sternum within Aves (but multiple origins for the pygostyle). Placing Archaeopteryx in Troodontidae would also require less “steps” with regards to sternal evolution. However, among derived maniraptorans, the sternum is highly homoplastic, as evidenced by the repeated parallel evolution of features such as a keel and lateral trabeculae; this observation highlights the apparent plasticity of this compound synstotic element (21), exemplified by the novel ossification pattern evolved by some enantiornithines (21).

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Fig. 2.

A simplified cladogram of derived maniraptoran theropods showing sternal morphology. The size of the circle reflects body size; blue indicates the absence of sternal ossifications, also indicated by short dashed branches (yellow, present). The number inside the circle indicates the number of gastralia (long dash indicates branch where gastralia are absent). The smaller circle inside the larger circle for Neornithes is meant to indicate the extreme size range occupied by fossil and extant members of this clade.

The absence of a sternum in Archaeopteryx and Sapeornis goes beyond its importance to the flight apparatus: This element is present in all tetrapods with forelimbs (with the unique exception of turtles in which the ribs are enlarged). Intuitively, we must infer a cartilaginous sternum was present not only because of its phylogenetic distribution but also because we can infer no reasonable benefit to volant activity gained through the loss of this feature, which provides the major point of attachment for the primary flight muscles (6). Most researchers tend to agree that Archaeopteryx had extremely limited flight capabilities. Although Sapeornis possesses features that are considerably more advanced such as its small pygostyle, long rectrices arranged into a fan, elongate forelimbs, and carpometacarpus with reduced manual digits (5, 26), derived features are notably absent from the shoulder girdle. This observation may suggest that Sapeornis retained a primitive form of flight and was not capable of a powerful up stroke, as inferred for Archaeopteryx (8).