From skin to armor: insights into osteoderm evolution in mammals and crocodilians

Osteoderms are specialized mineralized structures embedded within the dermal layers of the skin across various tetrapod lineages, representing a significant evolutionary adaptation with profound ecological implications. These structures are widespread among reptiles, rarely observed in amphibians and mammals, and completely absent in birds. The recent discovery of osteoderms in the tails of rodents belonging to the Deomyinae subfamily presents a novel opportunity to investigate the origins and evolutionary trajectories of this trait in a model organism that is both experimentally tractable and phylogenetically informative. In this study, we explored the evolutionary dynamics of genes that are candidate components of the regulatory networks that govern osteoderm development across two tetrapod lineages: mammals and crocodilians. We applied several state-of-the-art selection tests to assess the strength of natural selection and identify signatures of diversifying selection. Our main findings revealed evidence of positive selection in genes crucial for osteoderm function in cingulates and crocodilians. In cingulates, we observed evidence of positive selection in Bgn, an important gene for bone integrity and strength. In crocodilians, positive selection was identified in Gli1, a transcription factor central to intramembranous ossification; Satb2, a regulator of osteoblast maturation and differentiation; and Slc8a3, a gene essential for calcium transport and bone mineralization. To our knowledge, this is the first comparative genomics analysis of the genetic basis of osteoderm formation, offering novel insights into how natural selection has influenced the evolution of genes potentially involved in the development, structural integrity, and functional diversity of this unique trait.