Evolution and functional significance of derived sternal ossification patterns in ornithothoracine birds

Abstract

The midline pattern of sternal ossification characteristic of the Cretaceous enantiornithine birds is unique among the Ornithodira, the group containing birds, nonavian dinosaurs and pterosaurs. This has been suggested to indicate that Enantiornithes is not the sister group of Ornithuromorpha, the clade that includes living birds and their close relatives, which would imply rampant convergence in many nonsternal features between enantiornithines and ornithuromorphs. However, detailed comparisons reveal greater similarity between neornithine (i.e. crown group bird) and enantiornithine modes of sternal ossification than previously recognized. Furthermore, a new subadult enantiornithine specimen demonstrates that sternal ossification followed a more typically ornithodiran pattern in basal members of the clade. This new specimen, referable to the Pengornithidae, indicates that the unique ossification pattern observed in other juvenile enantiornithines is derived within Enantiornithes. A similar but clearly distinct pattern appears to have evolved in parallel in the ornithuromorph lineage. The atypical mode of sternal ossification in some derived enantiornithines should be regarded as an autapomorphic condition rather than an indication that enantiornithines are not close relatives of ornithuromorphs. Based on what is known about molecular mechanisms for morphogenesis and the possible selective advantages, the parallel shifts to midline ossification that took place in derived enantiornithines and living neognathous birds appear to have been related to the development of a large ventral keel, which is only present in ornithuromorphs and enantiornithines. Midline ossification can serve to medially reinforce the sternum at a relatively early ontogenetic stage, which would have been especially beneficial during the protracted development of the superprecocial Cretaceous enantiornithines.

Keywords: Aves; Enantiornithes; Neornithes; Ornithothoraces; development; keel; ossification; sternum.

Fig. 1

Pengornithidae indet. STM29-15: (a), photograph of main slab preserving the sternum; (b), interpretive line drawing. Scale bar equals 1 cm; light grey denotes poorly preserved bone. Anatomical abbreviations: al, alular metacarpal; al 1, first phalanx of alular digit; al 2, ungual phalanx of alular digit; cor, coracoid; dv, dorsal vertebrae; fem, femur; fib, fibula; gas, gastralia; hum, humerus; hx, hallux; ili, ilium; isc, ischium; ma, major metacarpal; ma 1, first phalanx of major digit; ma 2, second phalanx of major digit; ma 3, ungual phalanx of major digit; mi, minor metacarpal; mi 1, first phalanx of minor digit; mt1, metatarsal I; mt2, metatarsal II; mt3 4, fourth phalanx of third pedal digit; mt4, metatarsal IV; pub, pubis; pyg, pygostyle; rad, radius; sca, scapula; sl, semilunate carpal; stn, sternum; syn, synsacrum; tbt, tibiotarsus; ul, ‘ulnare’; uln, ulna.

Fig. 2

Close-up photographs of the sternum in: (a), subadult Microraptor STM5-11 (Maniraptora: Dromaeosauridae), plates medially unfused, scale bar equals 1 cm; (b), subadult Confuciusornis STM14-183 (Aves: Confuciusornithiformes), plates medially unfused, scale bar equals 1 cm; (c), subadult pengornithid STM29-15 (Ornithothoraces: Enantiornithes), plates medially unfused, scale bar equals 5 mm; (d), subadult pengornithid IVPP V18632, plates fused, scale bar equals 1 cm; (e), juvenile enantiornithine STM34-1 with derived ossification pattern, scale bar equals 5 mm; (f), enantiornithine Longirostravis hani, IVPP V11309, scale bar equals 1 cm; (g), basal ornithuromorph Archaeorhynchus spathula, scale bar equals 1 cm; (h), songlingornithid Jehol ornithuromorph Songlingornis linghensis IVPP V10913, scale bar equals 1 cm; (i), ornithuromorph Yixianornis grabauensis IVPP V12631 showing large ventral keel in lateral view, scale bar equals 1 cm. Anatomical abbreviations: cl, craniolateral process; f, fenestra; it, intermediate trabecula; k, keel; lp, lateral process; l cor, left coracoid; lt, lateral trabecula; r cor, right coracoid; xp, xiphoid process; xr, xiphial region; 1–3, numbers designating ossification centres.

Fig. 3

Simplified phylogenetic tree showing the distribution of inferred sternal ossification patterns and morphologies (blue represents the chondrified sternum; red represents ossification centres) within Maniraptora. Grey branches are those in which the sternum was apparently lost. Red branches represent lineages with midline ossification. Although we correlate the presence of a keel with midline ossification, there is no direct evidence concerning when midline ossification appeared in the neornithine lineage, and this uncertainty is indicated by the dashed branches and opaque reconstructions for the basal Ornithuromorpha. The ‘?’ next to Jeholornis acknowledges that the position of the ossification centres that form the ‘lateral trabeculae’ remains unclear.

Fig. 4

Hypothetical model of various modes of paravian sternogenesis and the emergence of the keel, based on the diversity of observed sternal morphologies and current knowledge of skeletal morphogenesis. First precursor cells migrate medially from the lateral plate mesoderm (LPM), induced by the Tbx5 gene and others (1); the precartilage (dashed line) expands and chondrification (cartilage indicated by blue) begins (2), initiated by BMP4 (activity indicated by orange dots); both precartilage and cartilaginous regions continue to expand (3, 4), forming the paired sternal plates (e.g. Velociraptor; 5–6A). Ossification (bone indicated by red) is initiated by BMP2 (activity indicated by pink dots; 5A, 6B). In some nonavian maniraptorans (e.g. Linheraptor, Citipati) and basal birds (e.g. Confuciusornis, Eopengornis, STM29-15), BMP4 activity continues in localized regions, forming trabeculae and other processes prior to ossification (5B,C), and fusion of the plates occurs late in ontogeny (7B–9B). In derived enantiornithines and nongalliform neognaths (5D, 6E), the plates begin to form a single mass prior to the ventral outgrowth of the cartilaginous carina (BMP4). The keel forms, perhaps in response to in ovo mechanical stresses (green arrows; 5D, 7E); formation of the large cartilaginous keel causes a spatial shift (grey arrows) in the pattern of PTHrP/Ihh activity (indicated by purple and yellow), producing medially located ossification centres (BMP2; 6D, 8E). In vivo mechanical stress (blue arrows) begins upon hatching (8E–10E) and is notably greater in enantiornithines (bold arrows, 6D–9D). Three additional ossification centres appear in enantiornithines (and an additional pair is known in Rapaxavis and Concornis); in ornithuromorphs, other centres were reported by Parker (1867) and are likely present, but cannot currently be confirmed except in galliforms (in which they are ribs and not truly sternal ossifications) and the Rhea (Palaeognathae). In extant ornithuromorphs (E), the ontogenetic stages of the sternum succeed one another more rapidly and under less in vivo mechanical stress.