Evaluating multiple alternative hypotheses for the origin of Bilateria: an analysis of 18S rRNA molecular evidence

Abstract

Six alternative hypotheses for the phylogenetic origin of Bilateria are evaluated by using complete 18S rRNA gene sequences for 52 taxa. These data suggest that there is little support for three of these hypotheses. Bilateria is not likely to be the sister group of Radiata or Ctenophora, nor is it likely that Bilateria gave rise to Cnidaria or Ctenophora. Instead, these data reveal a close relationship between bilaterians, placozoans, and cnidarians. From this, several inferences can be drawn. Morphological features that previously have been identified as synapomorphies of Bilateria and Ctenophora, e.g., mesoderm, more likely evolved independently in each clade. The endomesodermal muscles of bilaterians may be homologous to the endodermal muscles of cnidarians, implying that the original bilaterian mesodermal muscles were myoepithelial. Placozoans should have a gastrulation stage during development. Of the three hypotheses that cannot be falsified with the 18S rRNA data, one is most strongly supported. This hypothesis states that Bilateria and Placozoa share a more recent common ancestor than either does to Cnidaria. If true, the simplicity of placozoan body architecture is secondarily derived from a more complex ancestor. This simplification may have occurred in association with a planula-type larva becoming reproductive before metamorphosis. If this simplification took place during the common history that placozoans share with bilaterians, then placozoan genes that contain a homeobox, such as Trox2, should be explored, for they may include the gene or genes most closely related to Hox genes of bilaterians.

Figure 1

Six alternative hypotheses for the origin of the Bilateria.

Figure 2

Consensus of five optimal trees by using the criterion of cladistic parsimony in 100 heuristic searches with 1,526 nucleotide characters, 588 were parsimony informative. Trees have a length of 3,500 character changes, rescaled consistency of 0.2468, and retention index of 0.6361. A Bremer support analysis was carried out by consensus evaluations of 24,557 trees with lengths from 3,500 to 3,507, which were obtained by 20 heuristic searches. Bsi, up to seven, are presented at each node.

Figure 3

Optimal trees under the criteria of maximum likelihood (Left) and minimum evolution (Right). In both analyses the HKY85 model of nucleotide evolution was used with a gamma shape parameter of 0.3365. The maximum likelihood analysis included an assumed transition-to-transversion ratio of 1.643.