The skull and jaws of extant birds possess secondary cartilage, a tissue that arises after bone formation during embryonic development at articulations, ligamentous and muscular insertions. Using histological analysis, we discovered secondary cartilage in a non-avian dinosaur embryo, Hypacrosaurus stebingeri (Ornithischia, Lambeosaurinae). This finding extends our previous report of secondary cartilage in post-hatching specimens of the same dinosaur species. It provides the first information on the ontogeny of avian and dinosaurian secondary cartilages, and further stresses their developmental similarities. Secondary cartilage was found in an embryonic dentary within a tooth socket where it is hypothesized to have arisen due to mechanical stresses generated during tooth formation. Two patterns were discerned: secondary cartilage is more restricted in location in this Hypacrosaurus embryo, than it is in Hypacrosaurus post-hatchlings; secondary cartilage occurs at far more sites in bird embryos and nestlings than in Hypacrosaurus. This suggests an increase in the number of sites of secondary cartilage during the evolution of birds. We hypothesize that secondary cartilage provided advantages in the fine manipulation of food and was selected over other types of tissues/articulations during the evolution of the highly specialized avian beak from the jaws of their dinosaurian ancestors.

Secondary chondrogenesis investigated in hadrosaurid embryos.
(A) Reconstruction of the embryonic skull of Hypacrosaurus stebingeri, reproduced with permission [21] with anatomical locations 1, 2 and 3 in green. (B) Transverse section of the surangular of a Hadrosauridae indet. (MOR 1038). (C) Close-up of the red box in (B). The dorso-caudal face (Location 1) does not show any remnant of SC. (D) Coronal section of the maxilla of Hypacrosaurus stebingeri (MOR 559). (E) Close-up of the red box in (D). The bucco-caudal face of the maxilla (Location 2) does not show any remnants of SC. (F) Coronal section of the dentary of Hypacrosaurus stebingeri (MOR 559). (G) Close-up of the red box in (F). The arrow indicates a remnant of dentine. (H) Close-up of the red box in (G). (F) and (G) show alveolar bone (white asterisks) and incomplete alveoli with missing teeth (black asterisk; Location 3). (G) and (H) show a SC islet. All sections are shown under natural light. do, dorsal; la, labial; li, lingual; ro, rostral.
doi:10.1371/journal.pone.0056937.g001

Citation: Bailleul AM, Hall BK, Horner JR (2013) Secondary Cartilage Revealed in a Non-Avian Dinosaur Embryo. PLoS ONE 8(2): e56937. doi:10.1371/journal.pone.0056937

Editor: Peter Dodson, University of Pennsylvania, United States Of Amerca