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The Acoela: on Their Kind and Kinships, Especially with Nemertodermatids and Xenoturbellids (Bilateria Incertae Sedis)

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The Acoela: on Their Kind and Kinships, Especially with Nemertodermatids and Xenoturbellids (Bilateria Incertae Sedis) Org Divers Evol (2013) 13:267–286 DOI 10.1007/s13127-012-0112-4 REVIEW The Acoela: on their kind and kinships, especially with nemertodermatids and xenoturbellids (Bilateria incertae sedis) Johannes G. Achatz & Marta Chiodin & Willi Salvenmoser & Seth Tyler & Pedro Martinez Received: 19 April 2012 /Accepted: 12 September 2012 /Published online: 29 September 2012 # The Author(s) 2012. This article is published with open access at Springerlink.com Abstract Acoels are among the simplest worms and there- understanding these animals. Taking all available data into fore have often been pivotal in discussions of the origin of consideration, clear-cut conclusions cannot be made; howev- the Bilateria. Initially thought primitive because of their er, in our view it becomes successively clearer that acoelo- “planula-like” morphology, including their lumenless diges- morphs are a “basal” but “divergent” branch of the Bilateria. tive system, they were subsequently dismissed by many mor- phologists as a specialized clade of the Platyhelminthes. Keywords Acoelomorpha . Xenoturbella . Morphology . However, since molecular phylogenies placed them outside Development . Systematics . Phylogeny 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, in- Introduction cluding information regarding their morphology, develop- ment, systematics, and phylogenetic relationships, and put Acoels are bilaterally symmetric, microscopic worms, typical- some of these topics in a historical perspective to show how ly in the millimeter-size range, that are found predominantly the application of new methods contributed to the progress in in benthic marine habitats. They can easily be recognized by the presence of a characteristic statocyst at the anterior end J. G. Achatz : M. Chiodin : P. Martinez (see sensory organs; Figs. 1, 2a, b, d). Most are translucent or Department of Genetics, University of Barcelona, somewhat milky, but some are colored by pigmentation, by Av. Diagonal, edifici annex, planta 2a, algal symbionts, or by glandular secretions called rhabdoids 08028 Barcelona, Spain (Figs. 1, 2a, b, 5a). Their body shapes correlate with their J. G. Achatz (*) : W. Salvenmoser habitat: species living in sand are long and slender, those mov- Department of Evolutionary Developmental Biology, ing on or in mud are compact and droplet-shaped, those moving University of Innsbruck, on or beneath stones and corals are broad and flat, epiphytic Technikerstrasse 25, species have ventrally enrolled sides, and pelagic species have a 6020 Innsbruck, Austria e-mail: [email protected] disc-shaped body or enrolled sides (Figs. 1, 3, 5a). Acoels are acoelomate, the space between gut and body S. Tyler wall being filled with parenchymal cells that occasionally School of Biology and Ecology, University of Maine, contain chordoid vacuoles and the insunk bodies of epidermal 5751 Murray Hall, ‘ ’ Orono, ME 04469, USA and gland cells. The name acoel comes from their lack of a cavity in the gut, which is typically a solid syncytium. P. Martinez (*) Of the nearly 400 described species (Tyler et al. 2012,The Institució Catalana de Recerca i Estudis Avançats (ICREA), Turbellarian Taxonomic Database, http://turbellaria.umaine. Passeig Lluís Companys, 23, – 08010 Barcelona, Spain edu; Wallberg 2012, The Stylet Diversity and Systematics e-mail: [email protected] of Acoela and Nemertodermatida, http://acoela.myspecies. 268 J.G. Achatz et al. at the tip where the doublets 4–7 terminate (Tyler 1979; Ehlers 1985; Smith and Tyler 1985a; Smith et al. 1986; Rieger et al. 1991). Even more distinctive of the cilia is their rootlet system, which interconnects them: from the major, rostrally directed rootlet on each cilium, two lateral rootlets project and connect to the tips of the adjacent cilia, and from a caudal rootlet two bundles of fibers project to join the knee-like bend of those same adjacent rootlets (Hendelberg and Hedlund 1974;see Fig. 1 F in Rieger et al. 1991). Glands Unicellular glands that typically richly populate the epidermis include the above-mentioned rhabdoid glands (Smith et al. 1982), which may be colored, and mucous glands. Glands occurring at special positions include sag- Fig. 1 Images of various live acoels found in a beaker of sublittoral ittocytes that produce needle-shaped extrusomes (sagitto- sand from the Indian Ocean. Animals are oriented with the anterior end cysts, Fig. 4c) predominantly near the reproductive organs; to the top. Note the statocyst in all and mature oocytes in some animals. prominent mucous glands of the frontal organ that discharge Scale bar: 200 μm together through a pore at the anterior terminal end of the body (Smith and Tyler 1985b, 1986; Klauser et al. 1986; info), by far the majority are free-living, but seven are para- Smith et al. 1986;Riegeretal.1991;Figs.2b, 3); and sites or endosymbionts in the digestive system of echinoderms frontal glands of a variety of types that discharge near the (Jennings 1971), and two are found in fresh water (Ax and anterior tip. The nuclei of all these gland cells with the Dörjes 1966; Faubel and Kolasa 1978). Their diet varies as exception of most pigment cells are usually positioned be- much as their habitat, ranging from bacteria and unicellular low the body-wall musculature. algae to crustaceans, small bivalves, and worms (including other acoels); some are known for cannibalism (e.g., Sensory organs Specifically distinctive of acoels, the stato- Conaperta flavibacillum). cyst comprises a lithocyte bearing one statolith encompassed in a capsule formed by two lining parietal cells (Ehlers 1985; Figs. 2d, 3, 4a). Occasionally, animals that have been repro- Morphology duced asexually may lack the statocyst (Hanson 1960, Hendelberg and Åkesson 1988; Åkesson et al. 2001; see Epidermis Like most microscopic worms, acoels move pre- Fig. 5a), whereas panther worms (Hofsteniidae) have been dominantly by ciliary gliding. The epidermis is multiciliated, reported to occasionally possess more statoliths after regener- and the cilia have the common configuration of nine periph- ation of the anterior body region (Steinböck 1966). eral microtubule doublets and two central microtubules (9×2 In a small percentage of species paired eyespots, which +2). The shape of the cilia is distinctive, having a marked shelf are probably photoreceptive, occur at the anterior end Fig. 2 Images of sensory structures of live Symsagittifera roscoffensis. eyes, white arrow to statocyst, black arrow to frontal organ. c Eye of an a Hatchling. Arrowheads point to eyes, arrow to statocyst. Note adult. Asterisk marks nucleus, arrowhead points to concrements. d absence of symbionts and presence of orange rhabdoids. b Anterior Statocyst of an adult. Abbreviations: l lithocyte; p parietal cells. Scale end of adult with symbionts and rhabdoids. White arrowheads point to bars: a 100 μm; b 50 μm; c 10 μm; d 10 μm The Acoela: on their kind and kinships 269 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 (Figs. 2a, b, c). Lanfranchi (1990) described the eyespots of Mamkaev 1985), and such eyespots have subsequently been Otocelis rubropunctata as specialized epidermal cells with recognized to be characteristic for a derived group within the typical 9×2+2 cilia and with pigment granules and many Acoela, the Convolutida (Hooge and Tyler 2005; Achatz et synapses and axonemal outgrowths on the basal surface, but al. 2010). In all likelihood, many species of the Acoela can he was unable to prove photoreceptive function. Yamasu detect light (and behave accordingly) through photorecep- (1991) suggested the photoreceptive capacity of the eyes of tive sensory cells of the epidermis—cells that are difficult to Praesagittifera naikaiensis by relating experimental ablation identify because they are not accompanied by pigment cells. with behavioral assays. In this and some other species, the Other known sensory organs in acoels are single-celled eyespots don’t have ciliary or rhabdomeric elements but receptors, which are mostly monociliary. These can be clas- consist of a pigment cell containing a vacuole with refractive sified into several types on a morphological basis (Todt and inclusions called concrements and up to three nerve cells to Tyler 2007 and references therein), each type occurring in a relay the stimulus. The same configuration of cells has also specific region of the body that is species-specific (Todt and long been known in Convoluta convoluta (Popova and Tyler 2007; Bery et al. 2010). Fig. 4 Electron micrographs of structures with phylogenetic signifi- apparatus of Convolutriloba hastifera consisting of a sagittocyst (black cance. a Statocyst of a hatchling of Isodiametra pulchra with two arrowhead) and a wrapping muscle mantle. Abbreviations: m muscle parietal cells (p) and a lithocyte (l). b Sperm of Convoluta niphoni mantle; n nucleus of muscle mantle; rb refractive body; p parietal cell. (Convolutidae) with axial microtubules (white arrow) and axonemes Scale bars: a 4 μm; b 0.5 μm; c 2 μm without central microtubules (white arrowheads). c Extrusion 270 J.G. Achatz et al. 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.
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