Insight into the growth pattern and bone fusion of basal birds from an Early Cretaceous enantiornithine bird

Abstract

Bird skeletons exhibit remarkable modifications that allow for flight. The most distinguishable features are the fusion of the bones in the hand, feet, and pelvis into composite rigid and bony structures. However, the historical origins of these avian bone fusions remain elusive because of the rarity of transitional fossils and developmental studies on modern birds. Here, we describe an Early Cretaceous bird (120 Mya) that has fully fused alular-major metacarpals and pelvis. We discuss the manus and pelvis fusions across Paravian phylogeny and demonstrate that these features evolved independently across nonavian theropods, Enantiornithes, and Ornithuromorpha. The fusions of these bones are rare in known nonavian theropods and Early Cretaceous birds but are well established among Late Cretaceous and modern birds, revealing a complicated evolution pattern unrecognized previously. We posit that the developments of bone fusion were polymorphic close to the origin of birds, resulting in the varying degrees of fusion in Paraves. However, that development polymorphism appears to be fundamentally restricted along the line to modern birds by the Late Cretaceous, where all birds have a completely fused manus and pelvis. Such changes likely correspond to a refinement of flight capability. Alternatively, the degree of bone fusion in this primitive bird may have been related to modifications in genes or developmental paths. Future studies and fossil discoveries are required to clarify these hypotheses and pinpoint the developmental pathways involving the bone fusions in early avian evolution through to their modern pattern.

Birds have peramorphic skulls, too: anatomical network analyses reveal oppositional heterochronies in avian skull evolution

“…Tracing the evolutionary history of bone fusion in the manus and pelvis along maniraptoran theropods indicates that these features evolved many times independently across nonavialan theropods, Enantiornithes, and Ornithuromorpha, while bone fusion events within different body regions are uncoupled from each other and furthermore do not correlated with the growth pattern, i.e. neither duration nor speed of somatic growth impact bone fusion patterns 18 .…”

“…Interestingly, this ontogenetic pattern is paralleled to a lesser degree in Tarbosaurus, where the fusion of the frontal bones causes a reduction in the number of modules. Because bone fusion generally requires a previous contact of bones in form of a suture, it represents the more derived state with respect to the suture, both at the ontogenetic 13,19 and evolutionary level 18,20 . Therefore, we hypothesize that the intense fusion in the skull ontogeny of crown birds represents a peramorphic heterochrony (i.e., the developmental exaggeration of the ancestral adult trait) with respect to their non-avian theropod ancestors that evolved very late during avian evolution, at the origin of crown-birds.…”

“…While palaeognaths still have an intermediate stage, the most advanced skull kinesis is realized in neognath birds 28 . If skull bone fusion is further related with the short, accelerated growth mode of crown birds still need to be tested, but examples from other body regions indicate that bone fusion and growth strategy are not necessarily linked with each other 18 .…”

A new clade of basal Early Cretaceous pygostylian birds and developmental plasticity of the avian shoulder girdle

“…The semilunate carpal is fused with the proximal ends of the major and minor metacarpals, forming a carpometacarpus, as in other Aves except Archaeopteryx (21,22). The alular metacarpal is only fused proximally with the major metacarpals similar to most other Early Cretaceous avian clades (21). The alular metacarpal is rectangular and bears no extensor process.…”

“…The ulna is longer than the humerus, as in the majority of volant birds, as opposed to Archaeopteryx and most nonavian theropods (13,19). The semilunate carpal is fused with the proximal ends of the major and minor metacarpals, forming a carpometacarpus, as in other Aves except Archaeopteryx (21,22). The alular metacarpal is only fused proximally with the major metacarpals similar to most other Early Cretaceous avian clades (21).…”