A comparative study of cranial osteogenesis in turtles: implications for the diversification of skull morphology

Reptilian skull morphology is highly diverse and broadly categorized into three architectural patterns: anapsid, synapsid, and diapsid. The anapsid condition where the temporal region is completely roofed by bones is observed in both basal reptiles and turtles. According to recent phylogenetic studies, turtles are derived from diapsid reptiles, implying that the temporal fenestrae were secondarily closed in turtles. Although the repeated evolution of dermatocranial bone reductions in the skull’s temporal region of the anapsid skull and the biomechanical factors driving the evolution of the anapsid skull in turtles have been actively discussed, its developmental basis for the anapsid skull remains poorly understood. To investigate the developmental mechanisms underlying the morphological evolution of turtle skulls, here we describe the cranial osteogenesis of three cryptodiran turtle species with distinct skull morphologies: Chelonia mydas (Cheloniidae), Mauremys reevesii (Geoemydidae), and Pelodiscus sinensis (Trionychidae). Our interspecific comparison of embryonic cranial osteogenesis suggests that the growth pattern of skull bone elements is presumed to be highly conserved during embryogenesis across cryptodiran turtles. We found that the growth pattern of the five dermatocranial elements that construct the temporal region of the skull (the parietal, postorbital, jugal, quadratojugal, and squamosal) is highly conserved among turtle species, and that the morphological diversity of turtle skulls arises from slight differences in growth patterns. Our study also suggests that interspecific morphological differences in the cheloniid adult skulls may become apparent in the post-hatching growth period rather than during embryogenesis.