Development and embryonic pattern of body wall musculature in the crassiclitellate Eisenia andrei (Annelida, Clitellata)

Abstract

During early development of Eisenia andrei (Crassiclitellata), a loose arrangement of primary circular and longitudinal muscles encloses the whole embryo. Circular muscles differentiate in an anterior-posterior progression creating a segmental pattern. Primary circular muscles emerge at the segmental borders while later in development the central part of each segment is filled with circular strands. Longitudinal muscles develop in an anterio-posterior manner as well, but by continuous lengthening. Muscle growth is not restricted by segmental boundaries. The development begins with one pair of prominent longitudinal muscles differentiating ventrally along the right and the left germ band. These first muscles provide a guiding structure for the parallel organization of the afterwards differentiating longitudinal musculature. Additional primary longitudinal muscles emerge and form, together with the initial circular muscles, the primary muscle grid of the embryo. During the following development, secondary longitudinal muscle strands develop and integrate themselves into the primary grid. Meanwhile the primary circular muscles split into thin strands in a ventral to dorsal progression. Thus, a fine structured mesh of circular and longitudinal muscles is generated. Compared to other "Oligochaeta", embryonic muscle patterns in E. andrei are adapted to the development of a lecithotrophic embryo. Nevertheless, two general characteristics of annelid muscle development become evident. The first is the segmental development of the circular muscles from a set of initial muscles situated at the segment borders. Second, there is a continuous development of primary longitudinal muscles starting at the anterior pole. At least one pair of main primary longitudinal strands is characteristic in Annelida. The space between all primary strands is filled with secondary longitudinal strands during further development.

Temporal Plasticity in Annelid Development—Ontogeny of Phyllodoce groenlandica (Phyllodocidae, Annelida) Reveals Heterochronous Patterns

“…Our data reveal an origin of muscular development within the larval episphere of P. groenlandica , posterior to the apical organ. Congruent ontogenetic patterns have been reported for other annelid larvae (Hill, ; Seaver et al, ; Bergter and Paululat, ; Bergter et al, , ; Hunnekuhl et al, ; Fischer et al, ). However, contrary to other planktotrophic trochophores like, for example, Sabellaria alveolata (Sabellaridae), Spirobranchus polycerus (Serpulidae), or Pomatoceros lamarkii (Serpulidae) (Lacalli, ; McDougall et al, ; Brinkmann and Wanninger, ), body musculature in Phyllodoce develops earlier, whereas muscle fibers of the digestive system are hardly recognizable in these early stages.…”

“…The knowledge regarding the evolution of larval organ systems remains more scarce and is restricted to few annelid taxa (Lacalli, , , ; Hay‐Schmidt, ; Hessling and Westheide, ; Voronezhskaya et al, ; Seaver et al, ; Wanninger et al, ; McDougall et al, ; Bergter and Paululat, ; Bergter et al, , ; Brinkmann and Wanninger, ; Kristof et al, ; Hunnekuhl et al, ; Wanninger, ; Fischer et al, ). Concerning the great diversity of annelid larval types and the variance of life cycles, this source of data seems vanishingly low.…”

Integrative analysis of polychaete ontogeny: cell proliferation patterns and myogenesis in trochophore larvae of Sabellaria alveolata

“…Classical descriptions of annelid muscular systems including ultrastructural studies have been summarized and reviewed recently (Purschke 2002; Tzetlin and Filippova 2005; Purschke and Müller 2006). Together with the confocal microscopy data that have become available in the last couple of years, a picture of the ancestral annelid (including sipunculan) muscular system is slowly emerging (Hill and Boyer 2001; Tzetlin et al 2002; Filippova et al 2005; Filippova et al 2006; McDougall et al 2006; Müller and Worsaae 2006; Bergter et al 2007, 2008; Bergter and Paululat 2007; Rüchel and Müller 2007; Hunnekuhl et al 2009; Schulze and Rice 2009). In planktotrophic polychaete trochophores, the larval musculature starts to develop before segment formation (Heimler 1988).…”

Systematics, evolution and phylogeny of Annelida – a morphological perspective

“…by Fauchald and Rouse, 1997) and even though some of these studies were extremely comprehensive, additional morphological characters are needed to develop well-founded homology hypotheses Müller, 2006). Recently, fine structural investigations (cLSM, TEM, SEM) as well as developmental ones have provided such data and may provide better evidence for homology considerations (e.g., Orrhage and Müller, 2005;Müller, 2006;Hunnekuhl et al, 2009;Suschenko and Purschke, 2009;Wilkens and Purschke, 2009a, b;Filippova et al, 2010;Döring et al, 2013;Lehmacher et al, 2014;see also Fauchald, 1977;Fauchald and Rouse, 1997). These studies have mainly focussed on the muscular system, nervous system and sensory organs.…”