Are platyhelminthes coelomates without a coelom? An argument based on the evolution of Hox genes

American Zoologist, Dec 1998 by Balavoine, Guillaume

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/acoeloid 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.

INTRODUCTION

"We are asked [by the supporters of the enterocoele theory] to believe that the Turbellaria have lost their coelom, lost their anus, lost their nephrostomes. This is asking too much of one's credulity." Libbie H. Hyman, (1959, p. 753).

The debate on whether platyhelminths (or flatworms) were originally simply organized animals or secondarily simplified from a more complex ancestor is in fact a very old one and has always been linked with the controversy about the origin of bilaterally symmetrical metazoans (Bilateria). However, in the past decades, the vehement point of view of Hyman (that is genuine simplicity) has been dominating. The flatworms, in most textbooks of zoology, are uncritically presented as the first group emerging in the history of the bilaterians. In some books with insights into embryogenesis, the flatworms are placed emerging at the base of the protostomes (Brusca and Brusca, 1990; Nielsen, 1995). But the basic assumption remains that evolution proceeded from a simple acoelomate condition to the more complex coelomate organisation and that flatworms are modern representatives of the former step. Before challenging this dogma on molecular grounds, it is useful to expose two important historical concepts which have been in competition for explaining the origin of the bilaterians: the planuloid-acoeloid theory and the archecoelomate theory (reviewed in Willmer, 1990). We can then ask what predictions can be made for the topology of the metazoan tree under each of these schemes.

The planuloid-acoeloid concept

This scheme has been defended by Hyman (1940) among others. It states that the flatworms retain in their body plan the simplicity of an ancestral bilaterally symmetrical metazoan. The main argument is the comparison between the pelagic larva of many cnidarians, called the planula, and a group of very simple flatworms, the acoels. Planula larvae are radially symmetrical with distinct anterior and posterior ends. They are formed by an external ciliated epidermal layer (ectoderm) and an internal solid cell mass (entoderm). Acoels are small marine worms. They have either a simple pharynx or none at all. They have no permanent gut cavity (only a digestive cell mass), no protonephridia and no well delimitated gonads. Usually the nervous system has a net-like organisation, although in some species, there is an anterior "brain" from which originate pairs of nerves. Planula larvae and acoels have been considered to be almost unchanged descendants of two consecutive hypothetical ancestral bilaterians, the planuloid and the acoeloid. When the planuloid evolved into the more complex acoeloid (Fig. 1), it acquired bilateral symmetry, some centralization of the nervous system, sensory organs and a gut cavity.

The notion that flatworms are primitively simple does not imply that they should be placed as a single branch at the base of the bilaterian tree. The phylum Platyhelminthes contains in fact very diverse animals (Brusca and Brusca, 1990). The rhabditophorans, which form the bulk of the phylum Platyhelminthes (including the marine polyclads, the triclads and the parasitic neodermatans), have a more complex level of organization than the acoels described above. Rhabditophorans possess complex nervous, reproductive and excretory systems. In addition to the acoels, the catenulids are distinguished by their relative simplicity. The catenulids are small and roundish, with an anterior mouth. Contrary to acoels, they have a nephridium and a ciliated gut. In the context of the planula hypothesis, there is no strong reason to consider the flatworms as monophyletic, because most of their defining traits are supposed to be plesiomorphic in the Bilateria. Diverse groups of flatworms and also of minute "flatworm-like" animals (gnathostomulids, rotifers) may constitute a sort of stem group in which coelomate phyla are rooted. This is the point of view of Willmer (1990). Smith and Tyler (1985a) and Smith et al. (1986) emphasize the dissimilarity between acoels and rhabditophoran flatworms, and they pinpoint the lack of evidence for the monophyly of platyhelminths. Haszprunar (1996), in a recent cladistic analysis, has singled out the acoelomorphs and the catenulids, which, in his opinion, are not related to the rhabditophorans, but may represent independent early offshoots of the bilaterian tree. The acoelomorphs group the orders Acoela and Nemertodermatida on the basis of shared ultrastructural characters (Smith and Tyler, 1985b). The question of how the acoels and the catenulids are actually phylogenetically related to the other flatworms is thus of particular interest.