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Review
. 2008 Apr 27;363(1496):1493-501.
doi: 10.1098/rstb.2007.2239.

Acoel development supports a simple planula-like urbilaterian

Affiliations
Review

Acoel development supports a simple planula-like urbilaterian

Andreas Hejnol et al. Philos Trans R Soc Lond B Biol Sci. .

Abstract

Molecular approaches to the study of development and evolution have had profound effects on our understanding of the nature of the evolutionary process. Developmental biologists became intoxicated with fanciful notions of reconstructing genetic pathways of morphogenesis while evolutionary biologists were sobered by the fallacy of reconstructing organismal relationships along increasing grades of morphological complexity. Increased taxon sampling and improvements in analytical techniques are providing a new approach and are forcing biologists to move past historical biases to allow more accurate mapping of morphological and developmental characters through evolutionary time. Here, we discuss the possible developmental and morphological features of the 'urbilaterian', the triploblastic animal with anterior-posterior and dorsoventral axes and predecessor of the protostome-deuterostome ancestor. We argue that this animal, with features resembling acoelomorph flatworms, was far simpler morphologically than the protostome-deuterostome ancestor despite possessing a nearly complete eubilaterian genome. We show that the deployment of some genes expected to pattern the protostome-deuterostome ancestor is not deployed in acoels in the predicted manner and thus might have been co-opted after the evolution of the urbilaterian. We also identify the developmental changes related to gastrulation that gave rise to the urbilaterian from a simpler cnidarian-like ancestor.

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Figures

Figure 1
Figure 1
Phylogenetic position of the Acoela. The phylogenetic position of the Acoelomorpha based on molecular and morphological evidence (monophyletic Acoelomorpha: Ehlers 1985; sister to Eubilateria: Ruiz-Trillo et al. 1999, 2002, 2004; Jondelius et al. 2002; Telford et al. 2003). The position of the ‘urbilaterian’—the stem species of the Bilateria—is distinct from the eubilaterian stem species (protostome–deuterostome ancestor). Synapomorphies are indicated by filled squares.
Figure 2
Figure 2
Old (protostome–deuterostome ancestor) and new urbilaterian. (a) The old depiction of the stem species of the Bilateria based on gene expression data from both protostomes and deuterostomes. (b) The ground pattern of the Bilateria in the light of recent molecular phylogenies suggests that the urbilaterian was far less complex than thought before. (c) Comparison of the gene expression data and organs present in the hypothetical ancestor.
Figure 3
Figure 3
Morphology of the acoel C. longifissura. (a) Adult with ripe female (fo) and male genital (mg) organs. A pair of eyes (ey) is located at the anterior end. (b) At hatching, the juvenile possesses a statocyst (st) and a pair of lateral eyes. The mouth opening (mo) is ventral, anterior to the left. (c) Confocal image of a juvenile to visualize the nervous system. Actin is visualized with Alexa-488 phalloidin (green) and microtubules with anti-tubulin antibody (red). Dorsal view, the nervous system runs orthogonally with bilateral nerve chords on the dorsal and ventrolateral side (dnc, vnc), sensory cells (sc) are connected with the main nerve chords. The muscular system is composed out of longitudinal and circular musculature. The position of the mouth opening (mo) is indicated with a circle. (d) Lateral view of a juvenile (green phalloidin, red anti-serotonin). The serotonergic subset of the nervous system is labelled in red.
Figure 4
Figure 4
Gene expression of ClEvx, ClCdx, ClVax, ClPax6 and ClEmx during acoel development and NvEvx in the sea anemone Nematostella vectensis and CapI-cdx, CapI-vax in the annelid Capitella sp. I. (a) Expression of ClEvx in an acoel embryo with approximately 250 cells. The expression seems to be sparsely distributed in isolated cell (arrows). (b) ClEvx expression in a hatchling of C. longifissura. The expression is found in median neurons anterior and posterior to the statocyst. Lateral view, anterior to the left. (c) NvEvx expression in a planula of the sea anemone N. vectensis. NvEvx is expressed in isolated neural cells in the ectoderm (arrows). Later in the polyp (d), Nvevx is expressed in cells at the base of each tentacle (arrow); oral pole to the left. (e,f) ClCdx expression in a C. longifissura hatchling. ClCdx is expressed in the nervous system along the whole body. (e) Ventral view, (f) lateral view; asterisk indicates anterior end at left. (g) Cdx expression in the annelid Capitella sp. I is expressed all along the body axis, mainly in the mesodermal layer (dorsal view; Fröbius & Seaver 2006). (h) Expression of the gene ClVax in a C. longifissura hatchling. The gene is expressed in the ectoderm ventral and anterior to the mouth opening to the anterior tip of the animal (ventral view). (i) Lateral view of (h). (j) CapI-vax expression in the annelid Capitella sp. I. CapI-vax is expressed in the ectoderm anterior to the mouth opening (mo) on the dorsal side and in the dorsal hemisphere of the prototroch (not shown); lateral view. (k) Expression of the ‘anterior’ gene ClEmx in the acoel C. longifissura. ClEmx is in the late embryo along the entire length of the body; lateral view. In the hatchling (l) it is expressed in the nervous system, primarily on the ventral side (lateral view). (m) ClPax6 expression in a late embryo of C. longifissura. ClPax6 is expressed in an ectodermal ring of cells, separating the dorsal and ventral hemispheres of the embryo, but not in the position of the eyespots (dorsal view).

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