The Acoela: on their kind and kinships, especially with nemertodermatids and xenoturbellids (Bilateria incertae sedis)

Abstract

Acoels are among the simplest worms and therefore have often been pivotal in discussions of the origin of the Bilateria. Initially thought primitive because of their "planula-like" morphology, including their lumenless digestive system, they were subsequently dismissed by many morphologists as a specialized clade of the Platyhelminthes. However, since molecular phylogenies placed them outside the Platyhelminthes and outside all other phyla at the base of the Bilateria, they became the focus of renewed debate and research. We review what is currently known of acoels, including information regarding their morphology, development, systematics, and phylogenetic relationships, and put some of these topics in a historical perspective to show how the application of new methods contributed to the progress in understanding these animals. Taking all available data into consideration, clear-cut conclusions cannot be made; however, in our view it becomes successively clearer that acoelomorphs are a "basal" but "divergent" branch of the Bilateria.

Keywords: Acoelomorpha; Development; Morphology; Phylogeny; Systematics; Xenoturbella.

Fig. 1

Images of various live acoels found in a beaker of sublittoral sand from the Indian Ocean. Animals are oriented with the anterior end to the top. Note the statocyst in all and mature oocytes in some animals. Scale bar: 200 μm

Fig. 2

Images of sensory structures of live Symsagittifera roscoffensis. a Hatchling. Arrowheads point to eyes, arrow to statocyst. Note absence of symbionts and presence of orange rhabdoids. b Anterior end of adult with symbionts and rhabdoids. White arrowheads point to eyes, white arrow to statocyst, black arrow to frontal organ. c Eye of an adult. Asterisk marks nucleus, arrowhead points to concrements. d Statocyst of an adult. Abbreviations: l lithocyte; p parietal cells. Scale bars: a 100 μm; b 50 μm; c 10 μm; d 10 μm

Fig. 3

Image of a mature and live specimen of Isodiametra pulchra without (left) and with superimposed colors (right) to illustrate the general morphology of acoels. From top to bottom: yellow: frontal organ (fo); red: nervous system (ns); green: central syncytium (cs); cyan: testes (t); pink: ovaries (o); gray: mouth; purple: female copulatory organs (fco) composed of seminal bursa, bursal nozzle, and vestibulum (from posterior to anterior); white: chordoid vacuoles (cv); blue: false seminal vesicles and prostatoid glands (fsv); orange: male copulatory organ (cop) composed of muscular seminal vesicle and invaginated penis. Scale bar: 100 μm

Fig. 4

Electron micrographs of structures with phylogenetic significance. a Statocyst of a hatchling of Isodiametra pulchra with two parietal cells (p) and a lithocyte (l). b Sperm of Convoluta niphoni (Convolutidae) with axial microtubules (white arrow) and axonemes without central microtubules (white arrowheads). c Extrusion apparatus of Convolutriloba hastifera consisting of a sagittocyst (black arrowhead) and a wrapping muscle mantle. Abbreviations: m muscle mantle; n nucleus of muscle mantle; rb refractive body; p parietal cell. Scale bars: a 4 μm; b 0.5 μm; c 2 μm

Fig. 5

a Image of a live specimen of Convolutriloba retrogemma reproducing asexually by budding. White arrowheads point to buds. Note the reversed polarity. b, c CLSM projections showing muscles (blue) and serotonin-like immunoreactive nervous system (red) in dorsal (b) and central (c) planes of a mature Isodiametra pulchra. White arrowheads point to neurite bundles, asterisk marks the position of the statocyst. Scale bars: a 1 mm; b and c 50 μm

Fig. 6

Female copulatory organs in Isodiametra pulchra. a Image of female copulatory organs in a live and squeezed specimen. Note the mass of elongated and convoluted sperm in the seminal bursa (sb) that merge towards the bursal nozzle (arrowhead) and a few “heads” extending into the vestibulum (ve). Asterisk marks bursal stalk connecting the bursa with the digestive parenchyma, arrowhead points to bursal nozzle. b Electron micrograph showing cross section through the bursal nozzle (bn). Arrows point to nuclei of cells of the bursal wall. c Counterclockwise rotated detail of b. Note the density of sperm in the duct of the bursal nozzle. Abbreviations: bn bursal nozzle; sb seminal bursa; ve vestibulum. Scale bars: a 50 μm; b 10 μm; c 5 μm

Fig. 7

Cladogram of the Acoelomorpha with partial family-level systematics of the Acoela. 1. Multiciliated epidermis, ciliary rootlet system, frontal organ, basiepidermal nervous system with ring-shaped brain. 2. Statocyst with two lithocytes (statoliths) and many parietal cells, sperm with cork screw-like morphology. 3. Statocyst with one lithocyte (statolith) and two parietal cells, brain sunk below body wall, lateral fibers at knee of rostral rootlet, biflagellated sperm; digestive system becomes depolarized. 4. Position of mouth at the posterior end. 5. Specialized parenchymal tissue for reception, storage, and digestion of sperm (seminal bursa). 6. Subterminal pharynx at anterior end. 7. Ventral crossover muscles and highly branched wrapping cells. 8. Cytoplasmic microtubules of sperm partially lose contact with membrane and change position toward the center of the cell. 9. Cytoplasmic microtubules of sperm change position toward the center of the cell, stacked bursal nozzles with matrix and gland cells. 10. Central microtubules in axonemes of sperm reduced to allow movement in more than one plane. General scheme after Achatz et al. (2010); schemes of cross sections through statocysts from Ehlers (1985), through bodies after Rieger and Ladurner (2003); systematics and branching after Jondelius et al. (2011)

Fig. 8

The Acoela/Acoelomorpha in different schemes of eumetazoan relationships. a Precladistic version assuming a small planula-like worm as the ancestor of all bilaterians and with acoels as its direct descendants (after Hyman 1951). b Scheme based on morphological characters; the Acoela is part of the Acoelomorpha, which is placed within the Platyhelminthes (after Westheide and Rieger 2007). c Phylogeny according to rDNA (Wallberg et al. 2007); the Acoelomorpha forms a paraphylum at the base of the Bilateria. d Phylogeny according to phylogenomics I (Hejnol et al. 2009); Acoelomorpha together with the Xenoturbellida forming a clade that is a sister group to all other Bilateria. e Phylogeny according to phylogenomics II (Philippe et al. 2011); the Acoelomorpha is placed within the Deuterostomia and derived by progenesis from a coelomate ancestor. Abbreviations: d deuterostomia; p protostomia