Heading for higher ground: Developmental origins and evolutionary diversification of the amniote face

Amniotes, a clade of terrestrial vertebrates, which includes all of the descendants of the last common ancestor of the reptiles (including dinosaurs and birds) and mammals, is one of the most successful group of animals on our planet. In addition to having an egg equipped with an amnion, an adaptation to lay eggs on land, amniotes possess a number of other major morphological characteristics. Chief among them is the amniote skull, which can be classified into several major types distinguished by the presence and number of temporal fenestrae (windows) in the posterior part. Amniotes evolved from ancestors who possessed a skull composed of a complex mosaic of small bones separated by sutures. Changes in skull composition underlie much of the large-scale evolution of amniotes with many lineages showing a trend in reduction of cranial elements known as the "Williston's Law." The skull of amniotes is also arranged into a set of modules of closely co-evolving bones as revealed by modularity and integration tests. One of the most consistently recovered and at the same time most versatile modules is the "face," anatomically defined as the anterior portion of the head. The faces of amniotes display extraordinary amount of variation, with many adaptive radiations showing parallel tendencies in facial scaling, e.g., changes in length or width. This review explores the natural history of the amniote face and discusses how a better understanding of its anatomy and developmental biology helps to explain the outstanding scale of adaptive facial diversity. We propose a model for facial evolution in the amniotes, based on the differential rate of cranial neural crest cell proliferation and the timing of their skeletal differentiation.