JACOBS, David K; GATES, Ruth D: Is reproductive signaling antecedent to metazoan sensory and neural organization?

We explored the POU/Homeodomain containing developmental genes down the tree of life, recovering bilaterian, cnidarians, ctenophore and sponges sequence. The genes in question include a sense organ specific gene – Brain3, a pituitary specific gene – Pit1 and a neural marker associated with serotonergic neurons – Brain1. The statocyst and eye of the cnidarian rhopalia express Brain3, consistent with this genes function in bilaterian sense organ development. Presence of the gene in sponges suggests an antecedent function possibly associated with the sensory capacity of choanocytes. Even more surprising is our recovery of Pit1 from cnidarians, ctenophores, and sponges. This gene, absent from the nematode and fly, functions in the pituitary development of chordates. The vertebrate pituitary evolved from an external organ that functioned in the reception of water-borne reproductive signals. Gene-tree analysis supports a basal position for Pit1 among metazoan POU genes, followed by the divergence of Brain3 and Brain1. This suggests a scenario where: 1) A Pit1- like gene involved in differentiating an organ that functioned in reproductive signaling predated the evolution of the Metazoa. 2) Gene duplication produced Brain3 associated with the evolution of sense organ precursors in the metazoan stem. 3) Further gene duplications led to Brain1 and other POU genes that were co-opted for roles in development of an evolving nervous system. Thus, reproductive signaling may have been the precursor to the evolution of metazoan sensory and neural organization, a hypothesis which can be further tested by examination of other gene families with related functions.