Evo‐Devo of Specialized Bone Joints Formed During Pre‐Natal and Post‐Natal Ontogeny in Turtles With Shell‐Closing Systems

Abstract

The evolution of complex skeletal traits is often the result of functional variation in developmental genes during pre‐natal life stages. However, in some vertebrates, the development of such traits extends into post‐natal ontogeny, during which the relationship between functional genetic variation and phenotypic change is less clear. The objective of this study was to characterize pre‐natal and post‐natal development of a complex skeletal trait in turtles. We focused on phylogenetic comparisons of turtles with shell‐closing systems, an adaptation that enables some turtles to fully conceal appendages during predator attacks. We combined classical embryological approaches with modern geometric morphometrics to describe and quantify developmental change in bone tissues of deeply divergent lineages. We validated previous observations on the embryonic development of a specialized bone joint that articulates the dorsal scapula with the ventral shell. This joint is critical for the function of shell‐closing systems and forms via secondary subdivision of cartilage tissue. We then quantified a dramatic anatomical transformation associated with the post‐natal development of an external bone joint on the ventral shell of a lineage with the most derived form of the shell‐closing phenotype. This joint was not present in neonate turtles but likely developed in sub‐adult/adult age classes via tissue remodeling that was mechanically induced (due to muscle abduction). Remarkably, the turtle shell‐closing system is a complex skeletal trait that could feature both genetically‐ and epigenetically‐activated developmental programs. We are currently studying the genetic basis of this phenotype but will explore options to test hypotheses on epigenetic mechanisms.Grant Funding Source: NSF