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Nat Commun
2013 Jan 01;4:1537. doi: 10.1038/ncomms2556.
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Xenoturbella bocki exhibits direct development with similarities to Acoelomorpha.
Nakano H
,
Lundin K
,
Bourlat SJ
,
Telford MJ
,
Funch P
,
Nyengaard JR
,
Obst M
,
Thorndyke MC
.
Abstract
Xenoturbella bocki, a marine animal with a simple body plan, has recently been suggested to be sister group to the Acoelomorpha, together forming the new phylum Xenacoelomorpha. The phylogenetic position of the phylum is still under debate, either as an early branching bilaterian or as a sister group to the Ambulacraria (hemichordates and echinoderms) within the deuterostomes. Although development has been described for several species of Acoelomorpha, little is known about the life cycle of Xenoturbella. Here we report the embryonic stages of Xenoturbella, and show that it is a direct developer without a feeding larval stage. This mode of development is similar to that of the acoelomorphs, supporting the newly proposed phylum Xenacoelomorpha and suggesting that the last common ancestor of the phylum might have been a direct developer.
Figure 1. Eggs and hatchling of Xenoturbella bocki.(a) Unfertilized egg with a transparent layer (arrow). (b) Embryo before hatching within the fertilization envelope (arrowhead), surrounded by the transparent outer layer (arrow). (c) Embryo a day after hatching with anterior end at top left. (d) Embryo 3 days after hatching, uniformly covered with cilia (arrow). Apical tuft (arrowhead) at top right, also shown enlarged in inset. Scale bars, 100 μm.
Figure 2. Free-swimming stages of Xenoturbella bocki.(a–d) Confocal microscopy, 4 days after hatching with anterior at upper left. (a) Epithelial ectoderm (developing to epidermis) with glandular cells (arrows) and vesicles (arrowheads) surrounding the internal cell mass (developing to gastrodermis). (b) Thin dark layer of developing subepidermal muscle cells (arrow) surrounds the gastrodermal cell mass, composed of rounded cells. Arrowheads point to the nuclei of the rounded cells. (c) Large cells in the anterior part of the internal cavity (arrows). (d) Small cells (arrowheads) and extracellular vesicles (inside square) in the posterior part of the internal cavity. (e) Diagram of a 4-day hatchling of Xenoturbella bocki, based on the specimen in a. Anterior to top. (f) Free-swimming specimen 5 days after hatching before (upper panel) and after (lower panel) contracting the body. Anterior end at left. Scale bars, 100 μm (a,e,f); 50 μm (b); 25 μm (c,d).
Figure 3. Transmission electron microscopy of 4-day free-swimming hatchling of Xenoturbella bocki.(a) Cross-section of the body. Note the thin electron-dense cytoplasmic extensions of muscle cells, delimiting the outer epidermal layer from the inner gastrodermal cell mass (arrows). Many rounded bodies, presumed to be symbiotic bacteria, are present in the gastrodermal cells (arrowheads). Scale bar, 2 μm. (b) Surface of a multiciliated epidermal cell with ciliary axonemes and double vertical rootlets. The epidermal cells are laterally interdigitating. Scale bar, 1 μm. (c) Epidermal cell surface with double ciliary rootlets in longitudinal section. Note mitochondria (arrow) close to rootlets. Scale bar, 0.5 μm. (d) Epidermal cell surface with ciliary rootlets. Note microtubuli spreading out from the ciliary basal foot (arrow). Scale bar, 0.5 μm.
Figure 4. Transmission electron microscopy of 4-day free-swimming hatchling of Xenoturbella bocki.(a) Cytoplasmic extension of developing muscle cell, situated between the epidermal cell layer and the gastric cell mass. Scale bar, 0.5 μm. (b) Developing muscle cell with electron-dense cytoplasm and myofilament bundles in cross-section, also seen in oblique section (arrow). Scale bar, 0.5 μm. (c) Part of developing muscle cell, showing myofilaments in longitudinal section. Scale bar, 0.5 μm. (d) Point-core neuronal vesicles and neurotubules in nerve cell synapse. Scale bar, 0.25 μm.
Figure 5. Hypotheses on the evolution of metazoan development.Acquisition of feeding larvae shown with circles, and loss of feeding larvae shown with crosses. (a) Xenacoelomorpha as an early offshoot of the bilaterians suggested by Hejnol et al.3 Similarities with cnidarian planula may indicate an ancestral developmental stage for metazoans. (b,c) Xenacoelomorpha as deuterostomes suggested by Phillipe et al.4 (b) If Xenacoelomorpha direct development was secondarily derived, feeding larvae may have been lost independently in Ecdysozoa, Xenacoelomorpha and Chordata. (c) If Xenacoelomorpha direct development was retained from the metazoan ancestor, planktotrophic larvae with ciliary bands may have been independently acquired in the Ambulacraria and the Lophotrochozoa. Drawings of Acoelomorpha are modified from Ramachandra et al.6, those of Lophotrochozoa and Ambulacraria from Arendt et al.34, and Cnidaria from Kamm et al.35, respectively.
