Muscle formation during embryogenesis of the polychaete Ophryotrocha diadema (Dorvilleidae) – new insights into annelid muscle patterns

Bergter, Annette; Brubacher, John L.; Paululat, Achim

doi:10.1186/1742-9994-5-1

Cited by 49 publications

(66 citation statements)

References 48 publications

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“…The same situation was described for several species of Sipuncula (Wanninger et al, 2005;Schulze and Rice, 2009;Kristof et al, 2011). In most other annelids, the circular muscle fibers appear in an anteroposterior direction, which might represent the ground pattern of muscle formation in annelid trochophores (Seaver et al, 2005;Bergter and Paululat, 2007;Bergter et al, 2008;Wanninger, 2009;Helm et al, 2013). Summarizing, we find that the nervous system and the body musculature of this stage already resemble that of adult individuals in terms of complexity.…”

Section: B C D E F Amentioning

confidence: 49%

An immunocytochemical window into the development of Platynereis massiliensis (Annelida, Nereididae)

Helm¹,

Adamo²,

Hourdez³

et al. 2014

Int. J. Dev. Biol.

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The nereidid annelid Platynereis dumerilii emerged as a well-understood model organism. P. dumerilii and P. massiliensis are sister taxa, which are morphologically indistinguishable as adults. Interestingly, they exhibit highly contrasting life-histories: while P. dumerilii is a gonochorostic species with planktonic feeding larvae, P. massiliensis is a protandric hermaphrodite with lecitotrophic semi-direct -development in brood tubes. Using light microscopy and immunohistochemical methods coupled with confocal laser scanning microscopy, we describe the development of P. massiliensis. Musculature was stained with phalloidin-rhodamine. FMRFamide, acetylated a-tubulin, and serotonin were targeted by antibodies for the staining of neuronal structures. Additionally, eye development was investigated with the specific 22C10-antibody. The development of P. massiliensis is characterized by the absence of a free-swimming stage, a late development of food uptake, and the presence of a large amount of yolk even in late juvenile stages. Most notably, early juvenile stages already exhibit an organization of several organ systems that resembles those of adults. Larval characters present in the free-swimming feeding larvae of P. dumerilii, as e.g. the apical organ and larval eyes, are absent and regarded to be lost in developing stages of P. massiliensis. Many of the differences found in the development of these two species can be described in the context of heterochronic changes. We strongly advocate expanding evolutionary developmental studies from the well-established model annelid P. dumerilii to the closely related P. massiliensis to study the evolutionary conservation and divergence of genetic pathways involved in developmental processes. KEY WORDS: cLSM, evodevo, eye development, heterochrony, model organism, polychaeteThe vast majority of bilaterian animals are classified into three large clades: Deuterostomia, Ecdysozoa and Lophotrochozoa. Whereas several animal model systems for evolutionary developmental research are well established for the former two taxa, lophotrochozoans are underrepresented in this regard (GIGA Community of Scientists, 2014). However, especially in the last decade the annelid Platynereis dumerilii emerged as a well-understood model species (Fischer and Dorresteijn, 2004;Fischer et al., 2010;Simakov et al., 2013). Consequently, techniques as whole mount in situ hybridization, cell ablation, RNAinterference, and morpholino knockdowns are well established (Tessmar-Raible and Arendt, 2003;Veedin-Rajan et al., 2013). Moreover, transgenic lineages have been created (Backfisch et al., 2013) and a genome sequencing project is underway for this species (http://4dx.embl.de/platy/). Evolutionary developmental studies on Platynereis dumerilii provided important insights into the evolution of segmentation, vision and Int. J. Dev. Biol. 58: 613-622 (2014) doi: 10.1387/ijdb.140081cb the nervous system in Bilateria (Prud'homme et al., 2003;Arendt et al., 2004; Denes et al., 2007;Tessmar-Raible et al...

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Section: B C D E F Amentioning

confidence: 49%

An immunocytochemical window into the development of Platynereis massiliensis (Annelida, Nereididae)

Helm¹,

Adamo²,

Hourdez³

et al. 2014

Int. J. Dev. Biol.

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“…In the direct developing Ophryotrocha diadema (Dorvilleidae) longitudinal muscles are arranged in prominent ventral and dorsal bands and complete circular muscles do not develop (Bergter et al, 2008). Instead, parapodial muscle complexes are formed.…”

Section: Conclusion On the Muscular Ground Pattern In Annelida: A Comentioning

confidence: 98%

“…(Hill and Boyer, 2001), Pomatoceros lamarckii (McDougall et al, 2006) and Ophryotrocha diadema (Bergter et al, 2008). Whereas fully differentiated muscular systems usually show only little similarity between clitellates and polychaetes, as well as among different polychaete groups, the identification of distinct muscles or muscle groups appearing throughout development enables us to propose which muscles are characteristic for annelids in general.…”

Section: Introductionmentioning

confidence: 96%

“…Two prominent longitudinal ventral bands separated by the nerve cord are characteristic for most polychaete taxa (Tzetlin and Filippova, 2005;Purschke and Mü ller, 2006). Several recent investigations on polychaete muscular systems revealed, that circular muscles are often small or absent (Tzetlin et al, 2002;Tzetlin and Filippova, 2005;Mü ller and Worsaae, 2006;Bergter et al, 2008). This challenged the idea of an earthworm-like ancestral pattern of the annelid muscular system, which is further supported by increasing evidence that Clitellata form a derived clade within the paraphyletic polychaetes rather than being their sister group Fauchald, 1995, 1997;Purschke, 2002;Erséus and Kä llersjö, 2004;Halanych, 2004;Struck and Purschke, 2005;Rousset et al, 2007;Struck et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

“…Moreover, myocytes were proposed to be the most ancestral mesodermal cells in bilaterians with an essential role for the evolution of the mesoderm itself (Rieger and Ladurner, 2003). Investigations on muscle pattern formation in annelids facilitate our current understanding of mesoderm specification and differentiation during development (Bergter et al, , 2008.…”

Section: Introductionmentioning

confidence: 99%

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

Hunnekuhl

Bergter

Purschke

et al. 2009

Journal of Morphology

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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.

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Evolution, Development and Ecology ofCapitellasp. I: A Waxing Model for Polychaete Studies

Hill

Savage

2009

Annelids in Modern Biology

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Muscle formation during embryogenesis of the polychaete Ophryotrocha diadema (Dorvilleidae) – new insights into annelid muscle patterns

Cited by 49 publications

References 48 publications

An immunocytochemical window into the development of Platynereis massiliensis (Annelida, Nereididae)

An immunocytochemical window into the development of Platynereis massiliensis (Annelida, Nereididae)

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

Evolution, Development and Ecology ofCapitellasp. I: A Waxing Model for Polychaete Studies

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