Vertebrate cranial placodes as evolutionary innovations--the ancestor's tale

Evolutionary innovations often arise by tinkering with preexisting components building new regulatory networks by the rewiring of old parts. The cranial placodes of vertebrates, ectodermal thickenings that give rise to many of the cranial sense organs (ear, nose, lateral line) and ganglia, originated as such novel structures, when vertebrate ancestors elaborated their head in support of a more active and exploratory life style. This review addresses the question of how cranial placodes evolved by tinkering with ectodermal patterning mechanisms and sensory and neurosecretory cell types that have their own evolutionary history. With phylogenetic relationships among the major branches of metazoans now relatively well established, a comparative approach is used to infer, which structures evolved in which lineages and allows us to trace the origin of placodes and their components back from ancestor to ancestor. Some of the core networks of ectodermal patterning and sensory and neurosecretory differentiation were already established in the common ancestor of cnidarians and bilaterians and were greatly elaborated in the bilaterian ancestor (with BMP- and Wnt-dependent patterning of dorsoventral and anteroposterior ectoderm and multiple neurosecretory and sensory cell types). Rostral and caudal protoplacodal domains, giving rise to some neurosecretory and sensory cells, were then established in the ectoderm of the chordate and tunicate-vertebrate ancestor, respectively. However, proper cranial placodes as clusters of proliferating progenitors producing high-density arrays of neurosecretory and sensory cells only evolved and diversified in the ancestors of vertebrates.