Nonpathological inflammation drives the development of an avian flight adaptation

Author:

Rashid Dana J.1ORCID,Sheheen Joseph R.2ORCID,Huey Tori2ORCID,Surya Kevin3ORCID,Sanders Jackson B.2,Horner John R.4ORCID,Voyich Jovanka1,Chapman Susan C.2ORCID

Affiliation:

1. Department of Microbiology and Cell Biology, Montana State University, Bozeman, MT 59717

2. Department of Biological Sciences, Clemson University, Clemson, SC 29634

3. Molecular Biosciences Program, Montana State University, Bozeman, MT 59717

4. Schmid College of Science and Technology, Chapman University, Orange, CA 92866

Abstract

The development of modern birds provides a window into the biology of their dinosaur ancestors. We investigated avian postnatal development and found that sterile inflammation drives formation of the pygostyle, a compound structure resulting from bone fusion in the tail. Inflammation is generally induced by compromised tissue integrity, but here is involved in normal bone development. Transcriptome profiling and immuno/histochemistry reveal a robust inflammatory response that resembles bone fracture healing. The data suggest the involvement of necroptosis and multiple immune cell types, notably heterophils (the avian equivalent of neutrophils). Additionally, nucleus pulposus structures, heretofore unknown in birds, are involved in disc remodeling. Anti-inflammatory corticosteroid treatment inhibited vertebral fusion, substantiating the crucial role of inflammation in the ankylosis process. This study shows that inflammation can drive developmental skeletogenesis, in this case leading to the formation of a flight-adapted tail structure on the evolutionary path to modern avians.

Funder

SC-TRIMH

Gerry Ohrstrom

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

Reference56 articles.

1. L. M. Chiappe, Glorified Dinosaurs: The Origin and Early Evolution of Birds (University of New South Wales or John Wiley & Sons Inc., Sydney, Australia or Hoboken, NJ USA), 2007).

2. Morphological coevolution of the pygostyle and tail feathers in Early Cretaceous birds;Wang W.;Vertebrate PalAsiatica,2017

3. A pygostyle from a non-avian theropod

4. A new piscivorous ornithuromorph from the Jehol Biota

5. J. Baumel, Functional Morphology of the Tail Apparatus of the Pigeon (Columba livia) (Springer-Verlag, Berlin Heidelberg, ed. 1, 1988). p. 115.

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