Pattern of body‐wall muscle differentiation during embryonic development of <i>Enchytraeus coronatus</i> (Annelida: Oligochaeta; Enchytraeidae)

Bergter, Annette; Paululat, Achim

doi:10.1002/jmor.10532

Cited by 15 publications

(31 citation statements)

References 59 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.…”

supporting

confidence: 82%

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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supporting

confidence: 82%

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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“…This antero‐posterior pattern is known for many other annelids as well (Seaver et al. ; Bergter & Paululat ; Bergter et al. ; Wanninger ; Helm et al.…”

Section: Discussionsupporting

confidence: 59%

Immunohistochemical investigations of the development of Scoloplos armiger (“intertidalis clade”) indicate a paedomorphic origin of Proscoloplos cygnochaetus (Annelida, Orbiniidae)

Helm

Krause

Bleidorn

2015

Invertebrate Biology

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The embryology of Scoloplos armiger ("intertidalis clade") was described in detail using light microscopy in a landmark paper by DT Anderson in 1959. To expand these investigations, we used immunohistochemical staining techniques (phalloidin, anti-FMRF amide, anti-serotonin, and anti-a-tubulin) coupled with confocal laser scanning microscopy to describe the early development of musculature and nervous system of this species. Moreover, we applied the same methods (and Azan staining) to adults of the putatively paedomorphic orbiniid species Proscoloplos cygnochaetus. Our results showed comparable patterns for stainings of the nervous and muscle system for juveniles of Scoloplos and adults of Proscoloplos. Both show scarce transverse musculature and only a few dorsoventral muscle fibers in the anterior body region. For the nervous system, the observed immunoreactive pattern is nearly superimposable for juveniles of Scoloplos armiger and adults of Proscoloplos. Moreover, the intraepidermal and basiepithelial position of the ventral nervous system only found in juvenile Scoloplos is comparable with the conditions exhibited in adults of Proscoloplos. In summary, our data are in congruence with the hypothesis of a paedomorphic origin for Proscoloplos as derived from molecular phylogenetic analyses.

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“…as in E. coronatus , except for those at the ventral side of the embryo. In E. coronatus , the ventral primary longitudinal muscles of either side merge at the ventral midline during the movement of the ventral nerve cord into its position within the coelomic cavity (neurulation), closing the homogenous muscle layer (Bergter and Paululat 2007). Hence, there are no secondary longitudinal muscles formed at the ventral side of the E. coronatus embryo.…”

Section: Discussionmentioning

confidence: 99%

“…Our initial investigation of muscle differentiation in the terrestrial oligochaete Enchytraeus coronatus (Enchytraeidae, Fig. 1) revealed that patterns in the somatic musculature during embryogenesis are similar to those found in adult polychaetes (Bergter et al 2004; Bergter and Paululat 2007). Therefore, we propose that an examination of muscle patterns in developing stages will have a significant impact on our understanding of the muscle arrangement of the annelida (Purschke and Müller 2006; Bergter and Paululat 2007).…”

Section: Introductionmentioning

confidence: 91%

“…Although the diverse muscle patterns of polychaetes and the homogenous muscle fiber grid present in clitellates bear little resemblance to each other, a comparison of muscle patterns during embryogenesis of an assortment of annelid species constitutes a promising approach to uncover similarities and therefore truly annelid‐specific, plesiomorphic characteristics (Bergter and Paululat 2007). Only the assemblage of morphological data in combination with a reliable annelid phylogeny can lead to an understanding of the direction of evolutionary changes within this taxon.…”

Section: Introductionmentioning

confidence: 99%

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Evolutionary aspects of pattern formation during clitellate muscle development

Bergter

Hunnekuhl

Schniederjans

et al. 2007

Evolution and Development

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As a taxon of the lophotrochozoans, annelids have re-entered scientific investigations focusing on plesiomorphic bilaterian features and the evolutionary changes therein. The view of a clitellate-like plesiomorphic muscle arrangement in annelids has been challenged by recent investigations of polychaete muscle organization. However, there are few investigations of muscle formation in clitellate species that address this problem. Direct comparison of potential homologous muscles between these annelid groups is thus hampered. Somatic muscle formation during embryogenesis of two clitellates-the oligochaete Limnodrilus sp. and the hirudinean Erpobdella octoculata-occurs by distinct processes in each species, even though they share a closed outer layer of circular and an inner layer of longitudinal muscles characteristic of clitellates. In E. octoculata, the first emerging longitudinal muscles are distributed irregularly on the body surface of the embryo whereas the circular muscles appear in an orderly repetitive pattern along the anterioposterior axis. Both primary muscle types consist of fiber-bundles that branch at both their ends. This way the circular muscle bundles divide into a fine muscle-grid. The primary longitudinal muscles are incorporated into a second type of longitudinal muscles, the latter starting to differentiate adjacent to the ventral nerve cord. Those secondary muscles emerge in a ventral to dorsal manner, enclosing the embryo of E. octoculata. In Limnodrilus sp., one dorsal and one ventral bilateral pair of primary longitudinal muscles are established initially, elongating toward posterior. Initial circular muscles are emerging in a segmental pattern. Both muscle layers are completed later in development by the addition of secondary longitudinal and circular muscles. Some features of embryonic longitudinal muscle patterns in Limnodrilus sp. are comparable to structures found in adult polychaete muscle systems. Our findings show that comparative studies of body-wall muscle formation during clitellate embryogenesis are a promising approach to gain further information on annelid muscle arrangements.

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Pattern of body‐wall muscle differentiation during embryonic development of Enchytraeus coronatus (Annelida: Oligochaeta; Enchytraeidae)

Cited by 15 publications

References 59 publications

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

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

Immunohistochemical investigations of the development of Scoloplos armiger (“intertidalis clade”) indicate a paedomorphic origin of Proscoloplos cygnochaetus (Annelida, Orbiniidae)

Evolutionary aspects of pattern formation during clitellate muscle development

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