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Amniote skulls are diverse in shape and skeletal composition, which is the basis of much adaptive diversification within this clade. Major differences in skull shape are established early in development, at a critical developmental interval spanning the initial outgrowth and fusion of the facial processes. In birds, this is orchestrated by domains of Shh and Fgf8 expression, known as the frontonasal ectodermal zone (FEZ). It is unclear whether this model of facial development applies to species with diverse facial skeletons, especially species possessing a skull morphology representative of early amniotes. By investigating facial morphogenesis in the lizard, Anolis sagrei, we show that reptilian skull development is driven by the same genes as mammals and birds, but the manner in which those genes regulate facial development is clade-specific. These genes are not expressed in the frontal-nasal prominence, the region of the avian FEZ. Downregulating Shh and Fgf8 signaling disrupts normal facial development, but in pathway-specific ways. Our results demonstrate that early facial morphogenesis in lizards does not conform to the FEZ model. Lizard skull development may be more representative of the ancestral amniote than other model species with highly derived facial skeletons suggesting that the FEZ may be an avian-specific novelty. 

Abstract Phenotypic variation among species is a product of evolutionary changes to developmental programs^1,2. However, how these changes generate novel morphological traits remains largely unclear. Here we studied the genomic and developmental basis of the mammalian gliding membrane, or patagium—an adaptative trait that has repeatedly evolved in different lineages, including in closely related marsupial species. Through comparative genomic analysis of 15 marsupial genomes, both from gliding and non-gliding species, we find that theEmx2locus experienced lineage-specific patterns of acceleratedcis-regulatory evolution in gliding species. By combining epigenomics, transcriptomics and in-pouch marsupial transgenics, we show thatEmx2is a critical upstream regulator of patagium development. Moreover, we identify differentcis-regulatory elements that may be responsible for driving increasedEmx2expression levels in gliding species. Lastly, using mouse functional experiments, we find evidence thatEmx2expression patterns in gliders may have been modified from a pre-existing program found in all mammals. Together, our results suggest that patagia repeatedly originated through a process of convergent genomic evolution, whereby regulation ofEmx2was altered by distinctcis-regulatory elements in independently evolved species. Thus, different regulatory elements targeting the same key developmental gene may constitute an effective strategy by which natural selection has harnessed regulatory evolution in marsupial genomes to generate phenotypic novelty.