To Be or Not to Be a Flatworm: The Acoel Controversy

Abstract

Since first described, acoels were considered members of the flatworms (Platyhelminthes). However, no clear synapomorphies among the three large flatworm taxa - the Catenulida, the Acoelomorpha and the Rhabditophora - have been characterized to date. Molecular phylogenies, on the other hand, commonly positioned acoels separate from other flatworms. Accordingly, our own multi-locus phylogenetic analysis using 43 genes and 23 animal species places the acoel flatworm Isodiametra pulchra at the base of all Bilateria, distant from other flatworms. By contrast, novel data on the distribution and proliferation of stem cells and the specific mode of epidermal replacement constitute a strong synapomorphy for the Acoela plus the major group of flatworms, the Rhabditophora. The expression of a piwi-like gene not only in gonadal, but also in adult somatic stem cells is another unique feature among bilaterians. These two independent stem-cell-related characters put the Acoela into the Platyhelminthes-Lophotrochozoa clade and account for the most parsimonious evolutionary explanation of epidermal cell renewal in the Bilateria. Most available multigene analyses produce conflicting results regarding the position of the acoels in the tree of life. Given these phylogenomic conflicts and the contradiction of developmental and morphological data with phylogenomic results, the monophyly of the phylum Platyhelminthes and the position of the Acoela remain unresolved. By these data, both the inclusion of Acoela within Platyhelminthes, and their separation from flatworms as basal bilaterians are well-supported alternatives.

Assessing the root of bilaterian animals with scalable phylogenomic methods

“…S1). The signal for this placement is therefore dependent on widespread gene sampling, although a similar result is obtained by Egger et al (2009) using only 43 genes. The morphological analysis by Ehlers (1985) listed several apomorphies for Acoelomorpha.…”

“…), is consistent with placement for Acoelomorpha as sister to the rest of Bilateria. The stem cell and expression data presented by Egger et al (2009) can reasonably be interpreted as convergence or symplesiomorphy across Bilateria.…”

On the Independent Origins of Complex Brains and Neurons

“…Molecular data from Acoela as a basal bilaterian lineage [however, see Egger et al, 2009] also support a simple planula-like urbilaterian and apparently independent origin of many bilaterian features [Hejnol and Martindale, 2008a, b] including an ancestral uncentralized nervous system in the Urbilateria.…”

Masters of miniaturization: Convergent evolution among interstitial eukaryotes

“…[54,55] Homology statements about pedomorphic characters can be complicated by cryptic convergent evolution, which underscores the importance of building robust molecular phylogenetic frameworks for the meiofunal lineages of interest. [56,57] Acoels, e.g., were only recently hypothesized to be separate and distinct from the Platyhelminthes [38,39,58] because these lineages share a large suite of ancestral bilaterian features. Overall, convergent evolution and the highly reduced body plans of meiofauna make the discovery, delineation, and identification of these lineages difficult.…”