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Dinosaur mineralized tissues formation through metaplasia

Ben Creisler

A new online paper:

John R. Horner, Holly N. Woodward & Alida M. Bailleul (2015)
Mineralized tissues in dinosaurs interpreted as having formed through
metaplasia: A preliminary evaluation.
Comptes Rendus Palevol (advance online publication)

Evolutionary biologists define “metaplasia” as the permanent
transformation of a cell identity, and there are many examples of such
transformations in living vertebrates (e.g., chondrocytes transforming
directly into osteoblasts). These metaplasias have been observed
during the mineralization of “ossified” tendons of living birds. In
the present study, we examined “ossified” tendons in Bubo and
Meleagris and used the characteristics of these metaplastic tissues to
recognize them in several non-avian dinosaur taxa. The fossilized
skeletal elements that form our sample are varied and include
hadrosaurian tendons and a nasal bone, an ankylosaur tail club
“handle”, sauropod neural spines, and some dromaeosaur tail rods. The
extant avian mineralized tendons were formed of a primary tissue
(analogous to primary bone) and secondary reconstructions (SRs;
analogous to secondary osteons). Both were composed of fiber bundles
(or fascicles) that were closely packed together and separated by
arc-shaped spaces in cross-section. When viewed longitudinally, they
were arranged in a herringbone pattern. There is no evidence of
osteocytes within the primary tendon matrix; what was previously
interpreted as osteocyte lacunae are instead arc-shaped spaces between
fiber fascicles, and tissue immediately surrounding vascular spaces is
dense, avascular and apparently hypermineralized. Mineralization of
fibers began centrally and moved in a centrifugal direction. In the
non-avian dinosaurs examined, primary and secondary tissue structures
were virtually identical to those found within the avian mineralized
tendons. Indeed, (1) they were densely fibrous; (2) they showed fiber
fascicles separated by arcuate-shaped spaces when viewed
transversally, and (3) they were arranged in a herringbone pattern
longitudinally. SRs differ from typical Haversian systems in
possessing highly irregular borders, suggesting destruction of the
fibrous matrix and formation of initial vascular spaces was
accomplished perhaps by phagocytosis or enzymatic lysis with
subsequent remodeling by fibrocytes, fibroblasts, or an as of yet
unknown cell type. Osteocytes with canaliculi were only observed in
“mature” SRs, found deep within the elements (and never close to their
external borders). Because fossilized primary and secondary tissue
structures were identical to those found within the avian mineralized
tendons examined, it is likely that identical processes are
responsible for their formation. Biomechanical properties were also
likely similar, potentially affording carbon fiber-like,
trauma-resistant properties to the “ossified” tendons and nasal bones
of hadrosaurs, the tail “handles” of ankylosaurs, and the tail rods of
dromaeosaurs. In contrast, the primary tissue from a sauropod
mineralized nuchal ligament appears to be made of hypermineralized
fibrocartilage, but the SRs interdigitating with the hypermineralized
fibrocartilage resemble the reconstructions observed in the other
fossil skeletal elements and likely formed by the same processes.
Since no osteocyte lacunae were observed in any of these dinosaurian
primary tissues, we hypothesize that the fossilized cranial and
skeletal elements examined here formed through metaplastic
transformation (perhaps from fibroblasts) rather than by periosteal
and intramembranous ossification. This study suggests that alternative
modes of mineralization might be more abundant in non-avian dinosaurs
than previously reported.