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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

Two chaetigerous ciliary bands. Scale bars = 50 μm, anterior is to the left. A-E. Phalloidin staining (red) and in A, D anti-acetylated tubulin staining (green). Prototroch (prot), metatroch (met), ciliary band of peristomium (pcb), ciliary bands of chaetigers (BS) and telotroch (tel). A. Ventral view. Square marks region depicted in B. Labeling as in C. B. Close-up from A, ventral view, phalloidin staining, depth coded (in μm). The parapodial muscle anlage (pma) adjacent to the ciliary bands lie sublongitudinally, i.e., internal to the ventral longitudinal muscle (VLM). C. Same embryo as in A. Ventral view, phalloidin staining. The median ventral longitudinal muscle has now formed (mVLM). Its anterior splits, with branches running around each side of the pharyngeal muscles (phar). The ventral longitudinal muscles (VLM) project into the prostomium as the diagonal ventral longitudinal muscles (dVLM) and the straight ventral longitudinal muscles (sVLM) D. Lateral view. The parapodial muscle anlage (pma) runs on the lateral side of the embryo towards posterior. Each ciliary band (BS) lies between a set of parapodial muscle anlagen (pma). Autofluorescent chaetae (ch) are visible. E. Same embryo as in D. Lateral view, phalloidin staining only. The parapodial muscle anlagen (pma) adjacent to ciliary bands span from the ventral longitudinal muscle (VLM) dorsally to the dorsal longitudinal muscle (DLM). The musculature of the pharynx (phar) exhibits a basket-like shape.
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Figure 6: Two chaetigerous ciliary bands. Scale bars = 50 μm, anterior is to the left. A-E. Phalloidin staining (red) and in A, D anti-acetylated tubulin staining (green). Prototroch (prot), metatroch (met), ciliary band of peristomium (pcb), ciliary bands of chaetigers (BS) and telotroch (tel). A. Ventral view. Square marks region depicted in B. Labeling as in C. B. Close-up from A, ventral view, phalloidin staining, depth coded (in μm). The parapodial muscle anlage (pma) adjacent to the ciliary bands lie sublongitudinally, i.e., internal to the ventral longitudinal muscle (VLM). C. Same embryo as in A. Ventral view, phalloidin staining. The median ventral longitudinal muscle has now formed (mVLM). Its anterior splits, with branches running around each side of the pharyngeal muscles (phar). The ventral longitudinal muscles (VLM) project into the prostomium as the diagonal ventral longitudinal muscles (dVLM) and the straight ventral longitudinal muscles (sVLM) D. Lateral view. The parapodial muscle anlage (pma) runs on the lateral side of the embryo towards posterior. Each ciliary band (BS) lies between a set of parapodial muscle anlagen (pma). Autofluorescent chaetae (ch) are visible. E. Same embryo as in D. Lateral view, phalloidin staining only. The parapodial muscle anlagen (pma) adjacent to ciliary bands span from the ventral longitudinal muscle (VLM) dorsally to the dorsal longitudinal muscle (DLM). The musculature of the pharynx (phar) exhibits a basket-like shape.

Mentions: At this stage, the first transverse muscles of the body segments begin to differentiate ventrally, in close proximity to the ventral longitudinal muscles (Fig. 5E,H, arrows). They extend towards the dorsal longitudinal muscles and the ventral midline, and are situated in a sublongitudinal position, i.e. deep to the longitudinal muscles (Fig. 6B) and are the anlage of the anterior and posterior parapodial muscles (pma). These muscles display a repetitive pattern with respect to the primordial body segments, such that a transverse fiber is always present directly anterior and another directly posterior to a ciliary band (Fig. 5B–H and Fig. 6A–E, arrows). Early signs of (autofluorescent) chaetae are already visible in what will become first three body segments. These emerge just anterior to chaetigerous ciliary bands, which mark the posterior margins of body segments at this developmental stage (Fig. 5H). Chaetae develop in an anterior to posterior progression, so the more posterior ones represent an earlier stage of development than those in anterior segments.


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)

Two chaetigerous ciliary bands. Scale bars = 50 μm, anterior is to the left. A-E. Phalloidin staining (red) and in A, D anti-acetylated tubulin staining (green). Prototroch (prot), metatroch (met), ciliary band of peristomium (pcb), ciliary bands of chaetigers (BS) and telotroch (tel). A. Ventral view. Square marks region depicted in B. Labeling as in C. B. Close-up from A, ventral view, phalloidin staining, depth coded (in μm). The parapodial muscle anlage (pma) adjacent to the ciliary bands lie sublongitudinally, i.e., internal to the ventral longitudinal muscle (VLM). C. Same embryo as in A. Ventral view, phalloidin staining. The median ventral longitudinal muscle has now formed (mVLM). Its anterior splits, with branches running around each side of the pharyngeal muscles (phar). The ventral longitudinal muscles (VLM) project into the prostomium as the diagonal ventral longitudinal muscles (dVLM) and the straight ventral longitudinal muscles (sVLM) D. Lateral view. The parapodial muscle anlage (pma) runs on the lateral side of the embryo towards posterior. Each ciliary band (BS) lies between a set of parapodial muscle anlagen (pma). Autofluorescent chaetae (ch) are visible. E. Same embryo as in D. Lateral view, phalloidin staining only. The parapodial muscle anlagen (pma) adjacent to ciliary bands span from the ventral longitudinal muscle (VLM) dorsally to the dorsal longitudinal muscle (DLM). The musculature of the pharynx (phar) exhibits a basket-like shape.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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Figure 6: Two chaetigerous ciliary bands. Scale bars = 50 μm, anterior is to the left. A-E. Phalloidin staining (red) and in A, D anti-acetylated tubulin staining (green). Prototroch (prot), metatroch (met), ciliary band of peristomium (pcb), ciliary bands of chaetigers (BS) and telotroch (tel). A. Ventral view. Square marks region depicted in B. Labeling as in C. B. Close-up from A, ventral view, phalloidin staining, depth coded (in μm). The parapodial muscle anlage (pma) adjacent to the ciliary bands lie sublongitudinally, i.e., internal to the ventral longitudinal muscle (VLM). C. Same embryo as in A. Ventral view, phalloidin staining. The median ventral longitudinal muscle has now formed (mVLM). Its anterior splits, with branches running around each side of the pharyngeal muscles (phar). The ventral longitudinal muscles (VLM) project into the prostomium as the diagonal ventral longitudinal muscles (dVLM) and the straight ventral longitudinal muscles (sVLM) D. Lateral view. The parapodial muscle anlage (pma) runs on the lateral side of the embryo towards posterior. Each ciliary band (BS) lies between a set of parapodial muscle anlagen (pma). Autofluorescent chaetae (ch) are visible. E. Same embryo as in D. Lateral view, phalloidin staining only. The parapodial muscle anlagen (pma) adjacent to ciliary bands span from the ventral longitudinal muscle (VLM) dorsally to the dorsal longitudinal muscle (DLM). The musculature of the pharynx (phar) exhibits a basket-like shape.
Mentions: At this stage, the first transverse muscles of the body segments begin to differentiate ventrally, in close proximity to the ventral longitudinal muscles (Fig. 5E,H, arrows). They extend towards the dorsal longitudinal muscles and the ventral midline, and are situated in a sublongitudinal position, i.e. deep to the longitudinal muscles (Fig. 6B) and are the anlage of the anterior and posterior parapodial muscles (pma). These muscles display a repetitive pattern with respect to the primordial body segments, such that a transverse fiber is always present directly anterior and another directly posterior to a ciliary band (Fig. 5B–H and Fig. 6A–E, arrows). Early signs of (autofluorescent) chaetae are already visible in what will become first three body segments. These emerge just anterior to chaetigerous ciliary bands, which mark the posterior margins of body segments at this developmental stage (Fig. 5H). Chaetae develop in an anterior to posterior progression, so the more posterior ones represent an earlier stage of development than those in anterior segments.

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