New Developmental Evidence Clarifies the Evolution of Wrist Bones in the Dinosaur–Bird Transition

Abstract

A new study that integrates developmental and paleontological data reveals previously unsuspected evolutionary transformations during the emergence of the bird wrist, consistent with its derivation from non-avian dinosaurs.

Abstract

From early dinosaurs with as many as nine wrist bones, modern birds evolved to develop only four ossifications. Their identity is uncertain, with different labels used in palaeontology and developmental biology. We examined embryos of several species and studied chicken embryos in detail through a new technique allowing whole-mount immunofluorescence of the embryonic cartilaginous skeleton. Beyond previous controversy, we establish that the proximal–anterior ossification develops from a composite radiale+intermedium cartilage, consistent with fusion of radiale and intermedium observed in some theropod dinosaurs. Despite previous claims that the development of the distal–anterior ossification does not support the dinosaur–bird link, we found its embryonic precursor shows two distinct regions of both collagen type II and collagen type IX expression, resembling the composite semilunate bone of bird-like dinosaurs (distal carpal 1+distal carpal 2). The distal–posterior ossification develops from a cartilage referred to as “element x,” but its position corresponds to distal carpal 3. The proximal–posterior ossification is perhaps most controversial: It is labelled as the ulnare in palaeontology, but we confirm the embryonic ulnare is lost during development. Re-examination of the fossil evidence reveals the ulnare was actually absent in bird-like dinosaurs. We confirm the proximal–posterior bone is a pisiform in terms of embryonic position and its development as a sesamoid associated to a tendon. However, the pisiform is absent in bird-like dinosaurs, which are known from several articulated specimens. The combined data provide compelling evidence of a remarkable evolutionary reversal: A large, ossified pisiform re-evolved in the lineage leading to birds, after a period in which it was either absent, nonossified, or very small, consistently escaping fossil preservation. The bird wrist provides a modern example of how developmental and paleontological data illuminate each other. Based on all available data, we introduce a new nomenclature for bird wrist ossifications.

Author Summary

When birds diverged from nonavian dinosaurs, one of the key adaptations for flight involved a remodelling of the bones of the wrist. However, the correspondence between bird and dinosaur wrist bones is controversial. To identify the bones in the bird wrist, data can be drawn from two radically different sources: (1) embryology and (2) the fossil record of the dinosaur–bird transition. Currently, identifications are uncertain, but new developmental data can help resolve apparent conflicts. The modern bird wrist comprises four ossifications, arranged roughly in a square with its sides running proximal/distal and anterior/posterior. Our study integrates developmental and paleontological data and clarifies the relationship between each of these four ossifications and those found in nonavian dinosaurs. This integrative approach resolves previous disparities that have challenged the support for the dinosaur–bird link and reveals previously undetected processes, including loss, fusion, and in one case, re-evolution of a transiently lost bone.