How did our face evolve from fish-like ancestors?

Abstract

Face, the frontal portion of the head of vertebrates, plays a crucial role in the physical and social life in human and other animals. The face of human is thought to represent one’s identity and personality. Indeed, the word “person” or “people” in modern English is the etymological descendant of the ancient Greek word “πρόσωπον” or prosopon . It was only later realized that similar facial features shared by human and other vertebrates have common origins. Since then, the evolution of face has long been the spotlight issue in evolutionary biology. A series of important advances in evolutionary genomics, evolutionary developmental biology and paleontology has renewed our understanding of the vertebrate face evolution from fish to human. In this paper we briefly reviewed some of these advances following the steps of the vertebrate facial evolution from the architecture of craniates, “a new head”, to the emergence of the expressive mask in human. The “new head”, with supporting skull and novel sensory organs, vastly improved the sensory and overall evolutionary potentials of vertebrates. The developmental foundation of this innovation is the migration of neural crest cells and the formation of placodes. The origin of jaw is another key innovation in the rise of modern jawed vertebrate face. The traditional hypothesis that takes the jaw as the derivate of the anterior gill arch is under challenge. The intersection of developmental biology and paleontological evidences contributes to a well-supported new model, in which the disassociation of the naso-hypophyseal complex is a prerequisite for the origin of the jaw. The similarity between jaws and gill arches might be secondary. The recent discovery of Silurian maxillate placoderms illuminates the origin of marginal dermal jaw bones that leads to the primary functional jaw bones in most modern vertebrates including ourselves. We now have a clear picture of how facial organs such as noses, eyes, ears and teeth adapt to great transitions in vertebrate evolution such as that from water to land. The nose, originally an olfactory organ, secondarily adapts to become a part of the respiration system in the rise of terrestrial vertebrates. Early Devonian tetrapodomorph fish Kenichthys shows a rare transitional condition in the evolution of the nose, in which the premaxilla and maxilla split to display a notch, representing the posterior external nostril before it moved into the oral cavity to become the choana. The ear, after various innovative transformations, especially the incorporation of the novel middle ear and pinna, is modified to become an exquisite sound detection apparatus from its original function of balance. In contrast, the design of the camera-type eyes in all vertebrates is hardly changed since its initial emergence, with minor changes in its auxiliary organs. Competing hypotheses are forwarded to explain the origin and evolution of tooth and dentition. The enamel, the hardest tissue in vertebrate body first emerged on the surface of dermal scales in early bony fishes as a protection, and only covered the teeth secondarily. The pharyngeal muscles, which first evolved for feeding and respiration, immigrate to the frontal region of face in mammals to become mimetic muscles that control the facial gestures. All these shifts in the structures and functions of vertebrate faces finally result in the advent of facial features in modern Homo sapiens . In light of the facial evolution in our mammalian close relatives, the polishing of our hominine mask with personality has dual evolutionary controlling factors, physical and social. In addition, the foundation of the dominant importance of face in human social life lies in the modification of the facial traits in the common ancestors of human and other animals over deep time.