Are Platyhelminthes Coelomates without a Coelom ? An Argument Based on the Evolution of Hox Genes

SYNOPSIS. TWO fundamentally opposed theories have been proposed to account for the origin of the body plan of the flatworms. Each theory relates to a different concept of the evolution of the early metazoans. For the defenders of the classical planuloid/acoeloi'd theory, the simple organization of the flatworms is reminiscent of an hypothetical acoelomate worm-like ancestor of all bilaterians. Flatworms therefore emerge very early in the bilaterian tree before the appearance of the coelomate organisms. For the proponents of the more disputed archecoelomate theory, all the bilaterians are descendants of a primitively coelomate ancestor. Flatworms would have lost the coelom secondarily. Since their acoelomate condition is no longer indicative of a primitive origin, most of their characters put them in the protostomes, with the spiralian phyla. These competing theories about the position of flatworms in the metazoan phylogenetic tree can now be tested with molecular markers. This article reviews the arguments from 18S rDNA and Hox gene evolution. There is convergence between these data in favor of a late emergence of at least the rhabditophoran platyhelminths. Planarian Hox genes show more similarities with the Hox genes of annelids. On this basis, flatworms can be convincingly grouped with the spiralian coelomate protostomes. This position suggests the ancestors of flatworms lost both the anus and the coelom. Progenesis has been proposed as a possible mechanism by which these losses have occurred. This hypothesis is re-examined in the light of the affinity of the flatworms with other spiralian phyla.