Human-like malformations in anole lizards: Potential cases of "hopeful monsters" resembling chameleon morphology.

Abstract

Vertebrates exhibit remarkable morphological diversity, with the head representing an exceptionally complex anatomical structure shaped by adaptations to feeding ecology, brain size, and sensory organ specialization. Proper fusion of facial prominences and the coordinated growth of the skull and brain are essential for normal craniofacial development in vertebrates, including humans. Disruptions in these processes, whether due to gene mutations or external factors, can result in craniofacial malformations. In this study, we examined two pathological embryos of the brown anole, Anolis sagrei (Iguania: Anolidae), exhibiting notable craniofacial anomalies, including brachycephaly, mandibular prognathism, bilateral palatal clefts, and ocular defects. Comparative 3D reconstructions based on histological serial sections of malformed and normal embryos of similar developmental stages revealed instances of craniosynostosis, the absence of certain endocranial elements, skull shape abnormalities, and asymmetries. Furthermore, a wide range of postcranial anomalies was identified, including syndactyly, missing or shortened digits, and tail abnormalities. To the best of our knowledge, these are the first documented cases of non-experimentally induced craniofacial malformations and limb syndactyly occurring within the same individuals in squamates and non-avian reptiles in general. This rare combination was observed in both malformed embryos. Given the striking morphological resemblance to human craniofacial disorders, particularly Apert syndrome, we hypothesize the involvement of a shared genetic mechanism in mammals and sauropsids that may trace back over 320 million years. However, without molecular data, this remains speculative. Nonetheless, growing evidence suggests that non-avian reptiles, particularly squamates, could be valuable models for studying human craniofacial disorders. While the adaptive significance of the malformations observed here remains uncertain, these cases may represent examples of "hopeful monsters," offering valuable insights into the evolutionary processes that have shaped the distinctive vertebrate morphology of clades such as chameleons. Notably, several traits observed in the malformed anole embryos-including eyelid fusion, upper jaw shortening, syndactyly, and certain skeletal characteristics-appear to reflect features reminiscent of the peculiar chameleon phenotype.