Evolutionary assembly of crown reptile anatomy clarified by late Paleozoic relatives of Neodiapsida

Living reptiles include more than 20,000 species with disparate ecologies. Direct anatomical evidence from Neodiapsida, which includes the reptile crown-group and its closest extinct relatives, shows that this diversity originates from a single common ancestor that lived over 255 million years ago in the Paleozoic. However, the evolutionary assembly of crown reptile traits is poorly understood due to the lack of anatomically close relatives of Neodiapsida. We present a substantially revised phylogenetic hypothesis, informed by new anatomical data from high-resolution synchrotron tomography of Paleozoic stem reptiles. We find strong evidence placing the clade Millerettidae as the sister group to Neodiapsida, which uniquely share a suite of derived features. This grouping, for which we name the new clade Parapleurota, replaces previous phylogenetic paradigms by rendering the group Parareptilia as a polyphyletic assemblage of stem-reptiles, of which millerettids are the most crownward. Our findings address long-standing issues in Paleozoic reptile evolution, such as firm support for the placement of captorhinids outside of crown Amniota and most varanopids as synapsids. These results greatly improve the fit of early amniote phylogeny to the observed stratigraphic record and reveal stepwise origin of crown reptile anatomy, including a middle Permian origin of tympanic hearing and loss of the lower temporal bar. This evolutionary framework provides a platform for investigating the diversification of the reptile crown group in the Early Triassic that was foundational to the origins of important living and extinct groups including dinosaurs (including birds), marine reptiles, crocodilians, and lepidosaurs.