Shuo Wang, Josef Stiegler, Ping Wu, Cheng-Ming Chuong, Dongyu Hu, Amy Balanoff, Yachun Zhou, and Xing Xu (2017)
Heterochronic truncation of odontogenesis in theropod dinosaurs provides insight into the macroevolution of avian beaks.
Proceedings of the National Academy of Sciences (advance online publication)
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We identified truncation of tooth development during postnatal ontogeny in two theropod dinosaurs, a caenagnathid oviraptorosaur and the Early Cretaceous bird Sapeornis. Developmental and paleontological evidence each suggests dental reduction and beak evolution are coupled, and a sequence of common morphologies is identified that characterizes the multiple transitions to toothless beaks in theropod dinosaurs and birds. Shifts toward earlier cessation of postnatal tooth development can be identified in fish, amphibians, and mammals that are edentulous as adults; therefore the identification of similar transitions in multiple Mesozoic theropod dinosaur lineages strongly implies that heterochronic truncation of odontogenesis played an important role in the macroevolution of beaks in modern birds.
Beaks are innovative structures characterizing numerous tetrapod lineages, including birds, but little is known about how developmental processes influenced the macroevolution of these important structures. Here we provide evidence of ontogenetic vestigialization of alveoli in two lineages of theropod dinosaurs and show that these are transitional phenotypes in the evolution of beaks. One of the smallest known caenagnathid oviraptorosaurs and a small specimen of the Early Cretaceous bird Sapeornis both possess shallow, empty vestiges of dentary alveoli. In both individuals, the system of vestiges connects via foramina with a dorsally closed canal homologous to alveoli. Similar morphologies are present in Limusaurus, a beaked theropod that becomes edentulous during ontogeny; and an analysis of neontological and paleontological evidence shows that ontogenetic reduction of the dentition is a relatively common phenomenon in vertebrate evolution. Based on these lines of evidence, we propose that progressively earlier postnatal and embryonic truncation of odontogenesis corresponds with expansion of rostral keratin associated with the caruncle, and these progenesis and peramorphosis heterochronies combine to drive the evolution of edentulous beaks in nonavian theropods and birds. Following initial apomorphic expansion of rostral keratinized epithelia in perinatal toothed theropods, beaks appear to inhibit odontogenesis as they grow postnatally, resulting in a sequence of common morphologies. This sequence is shifted earlier in development through phylogeny until dentition is absent at hatching, and odontogenesis is inhibited by beak formation in ovo.