Limits...
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

First chaetiger ciliary band – later stage. Scale bars = 50 μm, anterior is to the left. A, C, F. Phalloidin staining shown in red anti-acetylated tubulin staining in green, and nuclear staining in blue. Prototroch (prot), metatroch (met), ciliary band of peristomium (pcb), ciliary bands of chaetigers (BS) and telotroch (tel). Additional labeling as in B, E, H. Phalloidin staining. D, G. Phalloidin staining, depth coded (in μm). A. Same embryo as in B. Ventral view. The ventral longitudinal muscles (VLM) have elongated towards the pygidium. The first transverse muscles (arrow) differentiate. Mouth region (stom) clearly visible. C, D. Same Embryo as in E. Ventrolateral view. The dorsal (DLM) and ventral longitudinal muscles (VLM) have reached the pygidium. Adjacent to the autofluorescent chaetae (ch) lie transverse muscles, the anlage of the paraopodial muscles, laterally and ventrally (arrows). The ventral longitudinal muscles extend into the prostomium, forming three projections (dVLM, asterisk). The jaw apparatus (ja) is apparent ventral to the mouth opening (stom). F, G. Same Embryo as in H. Ventrolateral view. One transverse parapodial muscle anlage (arrow) is always present just anterior and just posterior of a ciliary band (pcb, BS). DLM-dorsal longitudinal muscle, VLM-ventral longitudinal muscle, ch-chaetae, stom-mouth opening.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC2254616&req=5

Figure 5: First chaetiger ciliary band – later stage. Scale bars = 50 μm, anterior is to the left. A, C, F. Phalloidin staining shown in red anti-acetylated tubulin staining in green, and nuclear staining in blue. Prototroch (prot), metatroch (met), ciliary band of peristomium (pcb), ciliary bands of chaetigers (BS) and telotroch (tel). Additional labeling as in B, E, H. Phalloidin staining. D, G. Phalloidin staining, depth coded (in μm). A. Same embryo as in B. Ventral view. The ventral longitudinal muscles (VLM) have elongated towards the pygidium. The first transverse muscles (arrow) differentiate. Mouth region (stom) clearly visible. C, D. Same Embryo as in E. Ventrolateral view. The dorsal (DLM) and ventral longitudinal muscles (VLM) have reached the pygidium. Adjacent to the autofluorescent chaetae (ch) lie transverse muscles, the anlage of the paraopodial muscles, laterally and ventrally (arrows). The ventral longitudinal muscles extend into the prostomium, forming three projections (dVLM, asterisk). The jaw apparatus (ja) is apparent ventral to the mouth opening (stom). F, G. Same Embryo as in H. Ventrolateral view. One transverse parapodial muscle anlage (arrow) is always present just anterior and just posterior of a ciliary band (pcb, BS). DLM-dorsal longitudinal muscle, VLM-ventral longitudinal muscle, ch-chaetae, stom-mouth opening.

Mentions: With time, the embryo lengthens and the mandibles of the jaw apparatus (ja) become discernable due to weak autofluorescence (Fig 5E). The dorsal and ventral longitudinal muscle strands (DLM, VLM) elongate towards the posterior, reaching the pygidium at the end of this developmental stage (Fig. 5B,E,H). They consist of distinct fiber bundles, which decrease in thickness from anterior-to-posterior. The pair of ventral longitudinal muscles forms an anterior loop, with three terminal spikes at the ventral midline in front of the mouth opening (Fig. 5E). These represent the first muscles of the protostome, which correspond with the diagonally running ventral longitudinal muscles (dVLM) mentioned above (Fig. 2B–D).


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)

First chaetiger ciliary band – later stage. Scale bars = 50 μm, anterior is to the left. A, C, F. Phalloidin staining shown in red anti-acetylated tubulin staining in green, and nuclear staining in blue. Prototroch (prot), metatroch (met), ciliary band of peristomium (pcb), ciliary bands of chaetigers (BS) and telotroch (tel). Additional labeling as in B, E, H. Phalloidin staining. D, G. Phalloidin staining, depth coded (in μm). A. Same embryo as in B. Ventral view. The ventral longitudinal muscles (VLM) have elongated towards the pygidium. The first transverse muscles (arrow) differentiate. Mouth region (stom) clearly visible. C, D. Same Embryo as in E. Ventrolateral view. The dorsal (DLM) and ventral longitudinal muscles (VLM) have reached the pygidium. Adjacent to the autofluorescent chaetae (ch) lie transverse muscles, the anlage of the paraopodial muscles, laterally and ventrally (arrows). The ventral longitudinal muscles extend into the prostomium, forming three projections (dVLM, asterisk). The jaw apparatus (ja) is apparent ventral to the mouth opening (stom). F, G. Same Embryo as in H. Ventrolateral view. One transverse parapodial muscle anlage (arrow) is always present just anterior and just posterior of a ciliary band (pcb, BS). DLM-dorsal longitudinal muscle, VLM-ventral longitudinal muscle, ch-chaetae, stom-mouth opening.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2254616&req=5

Figure 5: First chaetiger ciliary band – later stage. Scale bars = 50 μm, anterior is to the left. A, C, F. Phalloidin staining shown in red anti-acetylated tubulin staining in green, and nuclear staining in blue. Prototroch (prot), metatroch (met), ciliary band of peristomium (pcb), ciliary bands of chaetigers (BS) and telotroch (tel). Additional labeling as in B, E, H. Phalloidin staining. D, G. Phalloidin staining, depth coded (in μm). A. Same embryo as in B. Ventral view. The ventral longitudinal muscles (VLM) have elongated towards the pygidium. The first transverse muscles (arrow) differentiate. Mouth region (stom) clearly visible. C, D. Same Embryo as in E. Ventrolateral view. The dorsal (DLM) and ventral longitudinal muscles (VLM) have reached the pygidium. Adjacent to the autofluorescent chaetae (ch) lie transverse muscles, the anlage of the paraopodial muscles, laterally and ventrally (arrows). The ventral longitudinal muscles extend into the prostomium, forming three projections (dVLM, asterisk). The jaw apparatus (ja) is apparent ventral to the mouth opening (stom). F, G. Same Embryo as in H. Ventrolateral view. One transverse parapodial muscle anlage (arrow) is always present just anterior and just posterior of a ciliary band (pcb, BS). DLM-dorsal longitudinal muscle, VLM-ventral longitudinal muscle, ch-chaetae, stom-mouth opening.
Mentions: With time, the embryo lengthens and the mandibles of the jaw apparatus (ja) become discernable due to weak autofluorescence (Fig 5E). The dorsal and ventral longitudinal muscle strands (DLM, VLM) elongate towards the posterior, reaching the pygidium at the end of this developmental stage (Fig. 5B,E,H). They consist of distinct fiber bundles, which decrease in thickness from anterior-to-posterior. The pair of ventral longitudinal muscles forms an anterior loop, with three terminal spikes at the ventral midline in front of the mouth opening (Fig. 5E). These represent the first muscles of the protostome, which correspond with the diagonally running ventral longitudinal muscles (dVLM) mentioned above (Fig. 2B–D).

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