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Evolution of Wrist Bones in the Dinosaur–Bird Transition

Ben Creisler

New in PLoS Biology:

João Francisco Botelho, Luis Ossa-Fuentes, Sergio Soto-Acuña, Daniel
Smith-Paredes, Daniel Nuñez-León, Miguel Salinas-Saavedra,Macarena
Ruiz-Flores & Alexander O. Vargas (2014)
New Developmental Evidence Clarifies the Evolution of Wrist Bones in
the Dinosaur–Bird Transition.
PLoS Biol 12(9): e1001957
DOI: 10.1371/journal.pbio.1001957

>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.


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