The embryonic development of the flatworm Macrostomum sp.

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.

Developmental diversity in free-living flatworms

“…The early cleavage pattern is of quartet spiral nature in macrostomids, as was shown in early accounts on M. appendiculatum and Macrostomum viride [39,40]. In M. appendiculatum , the existence of so-called hull cells has been described for the first time in the genus Macrostomum [41], and has later been confirmed to occur also in M. romanicum [42] and M. lignano [38,43]. Interestingly, in M. viride the embryo seemingly retains the spiral nature of cleavage up to the 128-cell stage and even the mesentoblast 4d is described, while no hull cells are mentioned [35].…”

“…(A-I), schematic representations of the early macrostomid (modified from [43]) and polyclad development (adapted from [45,46]). In macrostomids, early cleavage follows the typical quartet spiral cleavage pattern (A) up to the 8-cell stage, after which the four vegetal macromeres 2A-2D flatten (B) and form a yolk mantle that covers the embryo (C-D) that will be eventually replaced by the definitive epidermis.…”

“…The animal pole will become the anterior part, and the vegetal pole the posterior part of the animal. At the future ventral side of the animal, the organ primordia are developing [41,43]. Ciliogenesis of the multiciliary epidermis cells starts at about 50% developmental time in M. hystricinum marinum, M. romanicum and M. lignano [42,43,47].…”

Embryonic and post-embryonic development of the polyclad flatworm Maritigrella crozieri; implications for the evolution of spiralian life history traits

“…However, the sixth cleavage cycle gives rise to significantly larger micromeres than macromeres at the 4 th quartet stage. This may be a derived feature of polyclads, although verification in other archoophoran Rhabditophora such as macrostomids has not been possible as cleavage patterns beyond the third division are obscured by yolk [28]. However, an observation of a similar pattern has been recorded in the neoophoran Lecithoepitheliates [29].…”

The Evolution of Early Neurogenesis

“…2C top, middle). We know little about the first appearance of neural cells; markers used so far indicate that a contiguous cluster within the mesenchymal mass gives rise to the brain (Younossi-Hartenstein et al, 2000; 2001; Younossi-Hartenstein and Hartenstein, 2000; Ramachandra et al, 2002; Morris et al, 2004). It is clear that from later embryonic stages onward, pluripotent stem cells (neoblasts), which, similar to hydrozoan interstitial cells, derive from the mesenchymal mass and then populate the interstitial spaces of the worm, produce most neurons of the central nervous system and nerve plexus.…”