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

Bergter A, Brubacher JL, Paululat A - Front. Zool. (2008)

Bottom Line: Four embryonic parapodia differentiate in an anterior-to-posterior progression, significantly contributing to the somatic musculature.These circular fibers are only weakly developed, and do not appear to form complete muscle circles.These findings provide significant clues for the interpretation of evolutionary changes in annelid musculature.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Zoology, University of Osnabrueck, Barbarastr, 11, D-49069 Osnabrueck, Germany. paululat@biologie.uni-osnabrueck.de.

ABSTRACT

Background: The standard textbook information that annelid musculature consists of oligochaete-like outer circular and inner longitudinal muscle-layers has recently been called into question by observations of a variety of complex muscle systems in numerous polychaete taxa. To clarify the ancestral muscle arrangement in this taxon, we compared myogenetic patterns during embryogenesis of Ophryotrocha diadema with available data on oligochaete and polychaete myogenesis. This work addresses the conflicting views on the ground pattern of annelids, and adds to our knowledge of the evolution of lophotrochozoan taxa.

Results: Somatic musculature in Ophryotrocha diadema can be classified into the trunk, prostomial/peristomial, and parapodial muscle complexes. The trunk muscles comprise strong bilateral pairs of distinct dorsal and ventral longitudinal strands. The latter are the first to differentiate during myogenesis. They originate within the peristomium and grow posteriorly through the continuous addition of myocytes. Later, the longitudinal muscles also expand anteriorly and form a complex arrangement of prostomial muscles. Four embryonic parapodia differentiate in an anterior-to-posterior progression, significantly contributing to the somatic musculature. Several diagonal and transverse muscles are present dorsally. Some of the latter are situated external to the longitudinal muscles, which implies they are homologous to the circular muscles of oligochaetes. These circular fibers are only weakly developed, and do not appear to form complete muscle circles.

Conclusion: Comparison of embryonic muscle patterns showed distinct similarities between myogenetic processes in Ophryotrocha diadema and those of oligochaete species, which allows us to relate the diverse adult muscle arrangements of these annelid taxa to each other. These findings provide significant clues for the interpretation of evolutionary changes in annelid musculature.

No MeSH data available.


Related in: MedlinePlus

Three to four chaetigerous ciliary bands: dorsal and lateral view. Scale bars = 50 μm, anterior is to the left. A-F. Phallodin staining (B, E also include anti-acetylated tubulin staining in green and nuclear staining in blue). Prototroch (prot), metatroch (met), ciliary band of peristomium (pcb), ciliary band of chaetigers (BS) and telotroch (tel). C, F. Depth coded (in μm). A-C. Lateral view. In addition to the diagonal ventral longitudinal muscle (dVLM), the outer dorsal longitudinal muscle (oDLM) now extends into the prostomium. The pharynx (phar) is ventrally situated. The ventral longitudinal muscle (VLM) elongates straight posteriorly, whereas inner branches of the dorsal longitudinal muscle (DLM) run dorsomedially toward the midline. The arrowhead marks a circle of transverse muscle anterior to the pygidium. D-F. Dorsal view. Anteriorly, the outer dorsal longitudinal muscles (oDLM) and the ventral diagonal muscle (dVLM) connect within the prostomium, although the median projection of the dVLM (asterisk) remains weakly developed. Inner branches of the dorsal longitudinal muscle (DLM) intersect at the dorsal midline (circle). The anterior (adPM) and posterior dorsal parapodial muscles (pdPM) extend from the dorsal side into the parapodial muscle complex (pmc). The arrowhead marks the transverse muscle circle within the region anterior to the pygidium.
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Figure 8: Three to four chaetigerous ciliary bands: dorsal and lateral view. Scale bars = 50 μm, anterior is to the left. A-F. Phallodin staining (B, E also include anti-acetylated tubulin staining in green and nuclear staining in blue). Prototroch (prot), metatroch (met), ciliary band of peristomium (pcb), ciliary band of chaetigers (BS) and telotroch (tel). C, F. Depth coded (in μm). A-C. Lateral view. In addition to the diagonal ventral longitudinal muscle (dVLM), the outer dorsal longitudinal muscle (oDLM) now extends into the prostomium. The pharynx (phar) is ventrally situated. The ventral longitudinal muscle (VLM) elongates straight posteriorly, whereas inner branches of the dorsal longitudinal muscle (DLM) run dorsomedially toward the midline. The arrowhead marks a circle of transverse muscle anterior to the pygidium. D-F. Dorsal view. Anteriorly, the outer dorsal longitudinal muscles (oDLM) and the ventral diagonal muscle (dVLM) connect within the prostomium, although the median projection of the dVLM (asterisk) remains weakly developed. Inner branches of the dorsal longitudinal muscle (DLM) intersect at the dorsal midline (circle). The anterior (adPM) and posterior dorsal parapodial muscles (pdPM) extend from the dorsal side into the parapodial muscle complex (pmc). The arrowhead marks the transverse muscle circle within the region anterior to the pygidium.

Mentions: From here, the main events in myogenesis prior to hatching are the continued development of the prostomial muscles and the formation of the parapodial muscles in the first four chaetigers. The most prominent muscles of the prostomium are still the diagonal ventral longitudinal muscles (dVLM) (Fig. 7A–B and Fig. 8A). The middle branch of this muscle remains relatively thin, while the outer branches increase in thickness. They have already formed the connection with the straight ventral and the outer dorsal longitudinal muscles (Fig. 8D). However, the latter are only weakly developed at this stage, and the anterior muscle cap is not completely developed before hatching.


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

Bergter A, Brubacher JL, Paululat A - Front. Zool. (2008)

Three to four chaetigerous ciliary bands: dorsal and lateral view. Scale bars = 50 μm, anterior is to the left. A-F. Phallodin staining (B, E also include anti-acetylated tubulin staining in green and nuclear staining in blue). Prototroch (prot), metatroch (met), ciliary band of peristomium (pcb), ciliary band of chaetigers (BS) and telotroch (tel). C, F. Depth coded (in μm). A-C. Lateral view. In addition to the diagonal ventral longitudinal muscle (dVLM), the outer dorsal longitudinal muscle (oDLM) now extends into the prostomium. The pharynx (phar) is ventrally situated. The ventral longitudinal muscle (VLM) elongates straight posteriorly, whereas inner branches of the dorsal longitudinal muscle (DLM) run dorsomedially toward the midline. The arrowhead marks a circle of transverse muscle anterior to the pygidium. D-F. Dorsal view. Anteriorly, the outer dorsal longitudinal muscles (oDLM) and the ventral diagonal muscle (dVLM) connect within the prostomium, although the median projection of the dVLM (asterisk) remains weakly developed. Inner branches of the dorsal longitudinal muscle (DLM) intersect at the dorsal midline (circle). The anterior (adPM) and posterior dorsal parapodial muscles (pdPM) extend from the dorsal side into the parapodial muscle complex (pmc). The arrowhead marks the transverse muscle circle within the region anterior to the pygidium.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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Figure 8: Three to four chaetigerous ciliary bands: dorsal and lateral view. Scale bars = 50 μm, anterior is to the left. A-F. Phallodin staining (B, E also include anti-acetylated tubulin staining in green and nuclear staining in blue). Prototroch (prot), metatroch (met), ciliary band of peristomium (pcb), ciliary band of chaetigers (BS) and telotroch (tel). C, F. Depth coded (in μm). A-C. Lateral view. In addition to the diagonal ventral longitudinal muscle (dVLM), the outer dorsal longitudinal muscle (oDLM) now extends into the prostomium. The pharynx (phar) is ventrally situated. The ventral longitudinal muscle (VLM) elongates straight posteriorly, whereas inner branches of the dorsal longitudinal muscle (DLM) run dorsomedially toward the midline. The arrowhead marks a circle of transverse muscle anterior to the pygidium. D-F. Dorsal view. Anteriorly, the outer dorsal longitudinal muscles (oDLM) and the ventral diagonal muscle (dVLM) connect within the prostomium, although the median projection of the dVLM (asterisk) remains weakly developed. Inner branches of the dorsal longitudinal muscle (DLM) intersect at the dorsal midline (circle). The anterior (adPM) and posterior dorsal parapodial muscles (pdPM) extend from the dorsal side into the parapodial muscle complex (pmc). The arrowhead marks the transverse muscle circle within the region anterior to the pygidium.
Mentions: From here, the main events in myogenesis prior to hatching are the continued development of the prostomial muscles and the formation of the parapodial muscles in the first four chaetigers. The most prominent muscles of the prostomium are still the diagonal ventral longitudinal muscles (dVLM) (Fig. 7A–B and Fig. 8A). The middle branch of this muscle remains relatively thin, while the outer branches increase in thickness. They have already formed the connection with the straight ventral and the outer dorsal longitudinal muscles (Fig. 8D). However, the latter are only weakly developed at this stage, and the anterior muscle cap is not completely developed before hatching.

Bottom Line: Four embryonic parapodia differentiate in an anterior-to-posterior progression, significantly contributing to the somatic musculature.These circular fibers are only weakly developed, and do not appear to form complete muscle circles.These findings provide significant clues for the interpretation of evolutionary changes in annelid musculature.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Zoology, University of Osnabrueck, Barbarastr, 11, D-49069 Osnabrueck, Germany. paululat@biologie.uni-osnabrueck.de.

ABSTRACT

Background: The standard textbook information that annelid musculature consists of oligochaete-like outer circular and inner longitudinal muscle-layers has recently been called into question by observations of a variety of complex muscle systems in numerous polychaete taxa. To clarify the ancestral muscle arrangement in this taxon, we compared myogenetic patterns during embryogenesis of Ophryotrocha diadema with available data on oligochaete and polychaete myogenesis. This work addresses the conflicting views on the ground pattern of annelids, and adds to our knowledge of the evolution of lophotrochozoan taxa.

Results: Somatic musculature in Ophryotrocha diadema can be classified into the trunk, prostomial/peristomial, and parapodial muscle complexes. The trunk muscles comprise strong bilateral pairs of distinct dorsal and ventral longitudinal strands. The latter are the first to differentiate during myogenesis. They originate within the peristomium and grow posteriorly through the continuous addition of myocytes. Later, the longitudinal muscles also expand anteriorly and form a complex arrangement of prostomial muscles. Four embryonic parapodia differentiate in an anterior-to-posterior progression, significantly contributing to the somatic musculature. Several diagonal and transverse muscles are present dorsally. Some of the latter are situated external to the longitudinal muscles, which implies they are homologous to the circular muscles of oligochaetes. These circular fibers are only weakly developed, and do not appear to form complete muscle circles.

Conclusion: Comparison of embryonic muscle patterns showed distinct similarities between myogenetic processes in Ophryotrocha diadema and those of oligochaete species, which allows us to relate the diverse adult muscle arrangements of these annelid taxa to each other. These findings provide significant clues for the interpretation of evolutionary changes in annelid musculature.

No MeSH data available.


Related in: MedlinePlus