Extensive chondroid bone in juvenile duck limbs hints at accelerated growth mechanism in avian skeletogenesis
2019
Modern altricial birds are the fastest growing vertebrates, whereas various degrees of precocity (functional
maturity) result in slower growth. Diaphyseal osteohistology, the best proxy for inferring relative growth rates
in fossils, suggests that in the earliest birds, posthatching growth rates were more variable than in modern
representatives, with some showing considerably slow growth that was attributed to their assumed precocial
flight abilities. For finding clues how precocial or altricial skeletogenesis and related growth acceleration could
be traced in avian evolution, as a case study we investigated the growing limb diaphyseal histology in an
ontogenetic series of ducks which, among several other avian taxa, show a combination of altricial wing and
precocial leg development. Here we report the unexpected discovery that chondroid bone, a skeletal tissue
family intermediate between cartilage and bone, extensively contributes to the development of limb bone
shaft in ducks up to at least 30 days posthatching age. To our knowledge, chondroid bone has never been
reported in such quantities and with an ontogenetically extended deposition period in post-embryonic, nonpathological periosteal bone formation of any tetrapod limb. It shows transitional cellular/lacunar
morphologies and matrix staining properties between cartilage and woven bone and takes a significant part in
the diametric growth of the limb bone shaft. Its amount and distribution through duckling ontogeny seems to
be associated with the disparate functional and growth trajectories of the altricial wings vs. precocial legs
characteristic of duck limb development. The presence of isogenous cell groups in the periosteal chondroid
bone implies that cartilage-like interstitial growth took place before matrix mineralization complementing
appositional bone growth. Based on these characteristics and on its fast formation rate in all previously
reported normal as well as pathological cases, we suggest that chondroid bone in ducks significantly
accelerates diametric limb bone growth. Related to this growth acceleration, we hypothesize that chondroid
bone may be generally present in the growing limb bones of modern birds and hence may have key
skeletogenic importance in achieving extreme avian growth rates and placing birds among the fastest growing
vertebrates. Thus, we encourage future studies to test this hypothesis by investigating the occurrence of
chondroid bone in a variety of precocial and altricial bird species, and to explore the presence of similar tissues
in the growing limbs of other extant and extinct tetrapods in order to understand the evolutionary significance
of chondroid bone in accelerated appendicular skeletogenesis.
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