The new head hypothesis revisited.

In 1983, a new theory, the New Head Hypothesis, was generated within the context of the Tunicate Hypothesis of deuterostome evolution. The New Head Hypothesis comprised four claims: (1) neural crest, neurogenic placodes, and muscularized hypomere are unique to vertebrates, (2) the structures derived from these tissues allowed a shift from filter feeding to active predation, (3) the rostral head of vertebrates is a neomorphic unit, and (4) neural crest and neurogenic placodes evolved from the epidermal nerve plexus of ancestral deuterostomes. These claims are re-examined within the context of evolutionary developmental biology. The first may or may not be valid, depending on whether protochordates have these tissues in rudimentary form. Regarding the second, clearly, the elaboration of these tissues in vertebrates is correlated with a shift from filter feeding to active predation. The third claim is clarified, i.e., that the elaboration of the alar portion of the rostral brain and the development of olfactory organs and their associated connective tissues represent a neomorphic unit, which appears to be valid. The fourth is rejected. When the origin of neural crest and neurogenic placodes is examined within the context of developmental biology, it appears they evolved due to the rearrangement of germ layers in the blastulae of the deuterostomes that gave rise to chordates. Deuterostome evolution and the origin of vertebrates are also re-examined in the context of new data from developmental biology and taxonomy. The Tunicate Hypothesis is rejected, and a new version of the Dipleurula Hypothesis is presented. Copyright 2005 Wiley-Liss, Inc.