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The embryonic development of the flatworm Macrostomum sp.

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Abstract

Macrostomid flatworms represent a group of basal bilaterians with primitive developmental and morphological characteristics. The species Macrostomum sp., raised under laboratory conditions, has a short generation time of about 2–3 weeks and produces a large number of eggs year round. Using live observation, histology, electron microscopy and immunohistochemistry we have carried out a developmental analysis of Macrostomum sp. Cleavage (stages 1–2) of this species follows a modified spiral pattern and results in a solid embryonic primordium surrounded by an external yolk layer. During stage 3, cells at the anterior and lateral periphery of the embryo evolve into the somatic primordium which gives rise to the body wall and nervous system. Cells in the center form the large yolk-rich gut primordium. During stage 4, the brain primordium and the pharynx primordium appear as symmetric densities anterior-ventrally within the somatic primordium. Organ differentiation commences during stage 5 when the neurons of the brain primordium extend axons that form a central neuropile, and the outer cell layer of the somatic primordium turns into a ciliated epidermal epithelium. Cilia also appear in the lumen of the pharynx primordium, in the protonephridial system and, slightly later, in the lumen of the gut. Ultrastructurally, these differentiating cells show the hallmarks of platyhelminth epithelia, with a pronounced apical assembly of microfilaments (terminal web) inserting at the zonula adherens, and a wide band of septate junctions underneath the zonula. Terminal web and zonula adherens are particularly well observed in the epidermis. During stage 6, the somatic primordium extends around the surface dorsally and ventrally to form a complete body wall. Muscle precursors extend myofilaments that are organized into a highly regular orthogonal network of circular, diagonal and longitudinal fibers. Neurons of the brain primordium differentiate a commissural neuropile that extends a single pair of ventro-lateral nerve trunks (the main longitudinal cords) posteriorly. The primordial pharynx lumen fuses with the ventral epidermis anteriorly and the gut posteriorly, thereby generating a continuous digestive tract. The embryo adopts its final shape during stages 7 and 8, characterized by the morphallactic lengthening of the body into a U-shaped form and the condensation of the nervous system.

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Acknowledgements

We would like to thank Dennis Montoya, Willi Salvenmoser, and Birgitta Sjostrand for their technical support. This work was supported by NSF grant IBN-0110718 to V.H., FWF grants P15204 and 16618 to R.M.R. and the Ruth L. Kirschstein National Research Service Award GM07185 to J.M.

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Authors and Affiliations

  1. Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, CA, 90095, USA

    Joshua Morris, Ramachandra Nallur & Volker Hartenstein

  2. Institute of Zoology and Limnology, University of Innsbruck, Technikerstrasse 25, 6020, Innsbruck, Austria

    Peter Ladurner, Bernhard Egger & Reinhard Rieger

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  1. Joshua Morris
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  2. Ramachandra Nallur
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  3. Peter Ladurner
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Correspondence to Volker Hartenstein.

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Morris, J., Nallur, R., Ladurner, P. et al. The embryonic development of the flatworm Macrostomum sp.. Dev Genes Evol 214, 220–239 (2004). https://doi.org/10.1007/s00427-004-0406-4

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