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Myoanatomy and serotonergic nervous system of the ctenostome Hislopia malayensis: evolutionary trends in bodyplan patterning of ectoprocta.

Schwaha T, Wood TS, Wanninger A - Front. Zool. (2011)

Bottom Line: The apertural muscles show high similarity within Ectoprocta and always consist of two sets of muscles.Gymnolaemates and Phylactolaemates show clear differences within their digestive tract musculature, the former showing smooth and longitudinal muscles to a much greater extent than the latter.The complex musculature at the lophophoral base appears promising for inferring phylogenetic relationships, but sufficient comparative data are currently lacking.

View Article: PubMed Central - HTML - PubMed

Affiliation: University of Vienna, Department of Morphology, Althanstra├če 14, 1090 Vienna, Austria. thomas.schwaha@univie.ac.at.

ABSTRACT

Background: Ectoprocta is a large lophotrochozoan clade of colonial suspension feeders comprising over 5.000 extant species. Their phylogenetic position within the Lophotrochzoa remains controversially discussed, but also the internal relationships of the major ectoproct subclades -Phylactolaemata, Stenolaemata, and Gymnolaemata - remains elusive. To gain more insight into the basic configuration of ectoproct muscle systems for phylogenetic considerations, we analysed the adult myoanatomy and the serotonergic nervous system as well as myogenesis in budding stages of the ctenostome Hislopia malayensis.

Results: In adults, the serotonergic nervous system is restricted to the lophophoral base with a high concentration in the cerebral ganglion and serotonergic perikarya between each pair of tentacles. Prominent smooth apertural muscles extend from the basal cystid wall to each lateral side of the vestibular wall. The musculature of the tentacle sheath consists of regular strands of smooth longitudinal muscles. Each tentacle is supplied with two bands of longitudinal muscles that show irregular striation. At the lophophoral base several muscles are present: (i) Short muscle fibres that proximally diverge from a single point from where they split distally into two separate strands. (ii) Proximally of the first group are smooth, longitudinal fibres that extend to the proximal-most side of the lophophoral base. (iii) Smooth muscle fibres, the buccal dilatators, traverse obliquely towards the pharynx, and (iv) a circular ring of smooth muscle fibres situated distally of the buccal dilatators. Retractor muscles are mainly smooth with short distal striated parts. The foregut consists mainly of striated ring musculature with only few longitudinal muscle fibres in the esophagus, while the remaining parts of the digestive tract solely exhibit smooth musculature. During budding, apertural and retractor muscles are first to appear, while the parietal muscles appear at a later stage.

Conclusions: The apertural muscles show high similarity within Ectoprocta and always consist of two sets of muscles. Gymnolaemates and Phylactolaemates show clear differences within their digestive tract musculature, the former showing smooth and longitudinal muscles to a much greater extent than the latter. The complex musculature at the lophophoral base appears promising for inferring phylogenetic relationships, but sufficient comparative data are currently lacking.

No MeSH data available.


Myogenesis during the budding process of Hislopia malayensis. Maximum-intensity projections of confocal laserscanning image stacks. (a) Early budding stage showing the polypide anlage and the first anlagen of the developing apertural and retractor muscles at its distal and proximal side, respectively. (b) More advanced budding stage with distinct tentacle anlagen (asterisk), in which the cystid of the bud has widened distally and the apertural and retractor muscle anlagen have grown and are more pronounced. (c) Advanced budding stage where first anlagen of the digestive tract musculature have formed and the parietal muscles are present laterally of the polypide anlage. Both, the apertural and the retractor muscle anlagen are most prominent. The former consists of loosely smooth muscle fibres, whereas the prospective retractor muscles have differentiated into two elongated muscle fibre bundles. (d) Almost completely developed zooid where most parts of the digestive tract, especially the most prominent proventriculus, are formed similar to the adult. Compare to Figures 3 and 4 for details on the musculature of adult specimens. Abbreviations: am - apertural muscles, ama - apertural muscle anlage, cae - caecum, ds - diaphragmatic sphincter, dt - distal tip of the cystid of the bud, dtm - developing digestive tract musculature, ep - epizooic organism, int - intestine, lb - lophophore base, pa - polypide anlage, pma - parietal muscle anlage, pm - parietal muscles, pv - proventriculus, rm - retractor muscles, rma - retractor muscle anlage, vwm - vestibular wall musculature.
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Figure 5: Myogenesis during the budding process of Hislopia malayensis. Maximum-intensity projections of confocal laserscanning image stacks. (a) Early budding stage showing the polypide anlage and the first anlagen of the developing apertural and retractor muscles at its distal and proximal side, respectively. (b) More advanced budding stage with distinct tentacle anlagen (asterisk), in which the cystid of the bud has widened distally and the apertural and retractor muscle anlagen have grown and are more pronounced. (c) Advanced budding stage where first anlagen of the digestive tract musculature have formed and the parietal muscles are present laterally of the polypide anlage. Both, the apertural and the retractor muscle anlagen are most prominent. The former consists of loosely smooth muscle fibres, whereas the prospective retractor muscles have differentiated into two elongated muscle fibre bundles. (d) Almost completely developed zooid where most parts of the digestive tract, especially the most prominent proventriculus, are formed similar to the adult. Compare to Figures 3 and 4 for details on the musculature of adult specimens. Abbreviations: am - apertural muscles, ama - apertural muscle anlage, cae - caecum, ds - diaphragmatic sphincter, dt - distal tip of the cystid of the bud, dtm - developing digestive tract musculature, ep - epizooic organism, int - intestine, lb - lophophore base, pa - polypide anlage, pma - parietal muscle anlage, pm - parietal muscles, pv - proventriculus, rm - retractor muscles, rma - retractor muscle anlage, vwm - vestibular wall musculature.

Mentions: Buds start as distal or lateral outgrowths of the cystid of a zooid that soon become constricted off from the mother zooid (Figure 3b). Further development leads to a tube-like elongation of the cystid, slightly broadened at its distal tip. In the middle of the bud the polypide anlage develops. The retractor and apertural muscles are first to appear in the bud. The anlagen of the retractor muscles are V-shaped: Proximally, they originate from the cystid wall from a single site, whereas distally the bundles split and insert at the developing polypide. The apertural muscles form as two small bands on each side of the prospective aperture (Figure 5a).


Myoanatomy and serotonergic nervous system of the ctenostome Hislopia malayensis: evolutionary trends in bodyplan patterning of ectoprocta.

Schwaha T, Wood TS, Wanninger A - Front. Zool. (2011)

Myogenesis during the budding process of Hislopia malayensis. Maximum-intensity projections of confocal laserscanning image stacks. (a) Early budding stage showing the polypide anlage and the first anlagen of the developing apertural and retractor muscles at its distal and proximal side, respectively. (b) More advanced budding stage with distinct tentacle anlagen (asterisk), in which the cystid of the bud has widened distally and the apertural and retractor muscle anlagen have grown and are more pronounced. (c) Advanced budding stage where first anlagen of the digestive tract musculature have formed and the parietal muscles are present laterally of the polypide anlage. Both, the apertural and the retractor muscle anlagen are most prominent. The former consists of loosely smooth muscle fibres, whereas the prospective retractor muscles have differentiated into two elongated muscle fibre bundles. (d) Almost completely developed zooid where most parts of the digestive tract, especially the most prominent proventriculus, are formed similar to the adult. Compare to Figures 3 and 4 for details on the musculature of adult specimens. Abbreviations: am - apertural muscles, ama - apertural muscle anlage, cae - caecum, ds - diaphragmatic sphincter, dt - distal tip of the cystid of the bud, dtm - developing digestive tract musculature, ep - epizooic organism, int - intestine, lb - lophophore base, pa - polypide anlage, pma - parietal muscle anlage, pm - parietal muscles, pv - proventriculus, rm - retractor muscles, rma - retractor muscle anlage, vwm - vestibular wall musculature.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3117780&req=5

Figure 5: Myogenesis during the budding process of Hislopia malayensis. Maximum-intensity projections of confocal laserscanning image stacks. (a) Early budding stage showing the polypide anlage and the first anlagen of the developing apertural and retractor muscles at its distal and proximal side, respectively. (b) More advanced budding stage with distinct tentacle anlagen (asterisk), in which the cystid of the bud has widened distally and the apertural and retractor muscle anlagen have grown and are more pronounced. (c) Advanced budding stage where first anlagen of the digestive tract musculature have formed and the parietal muscles are present laterally of the polypide anlage. Both, the apertural and the retractor muscle anlagen are most prominent. The former consists of loosely smooth muscle fibres, whereas the prospective retractor muscles have differentiated into two elongated muscle fibre bundles. (d) Almost completely developed zooid where most parts of the digestive tract, especially the most prominent proventriculus, are formed similar to the adult. Compare to Figures 3 and 4 for details on the musculature of adult specimens. Abbreviations: am - apertural muscles, ama - apertural muscle anlage, cae - caecum, ds - diaphragmatic sphincter, dt - distal tip of the cystid of the bud, dtm - developing digestive tract musculature, ep - epizooic organism, int - intestine, lb - lophophore base, pa - polypide anlage, pma - parietal muscle anlage, pm - parietal muscles, pv - proventriculus, rm - retractor muscles, rma - retractor muscle anlage, vwm - vestibular wall musculature.
Mentions: Buds start as distal or lateral outgrowths of the cystid of a zooid that soon become constricted off from the mother zooid (Figure 3b). Further development leads to a tube-like elongation of the cystid, slightly broadened at its distal tip. In the middle of the bud the polypide anlage develops. The retractor and apertural muscles are first to appear in the bud. The anlagen of the retractor muscles are V-shaped: Proximally, they originate from the cystid wall from a single site, whereas distally the bundles split and insert at the developing polypide. The apertural muscles form as two small bands on each side of the prospective aperture (Figure 5a).

Bottom Line: The apertural muscles show high similarity within Ectoprocta and always consist of two sets of muscles.Gymnolaemates and Phylactolaemates show clear differences within their digestive tract musculature, the former showing smooth and longitudinal muscles to a much greater extent than the latter.The complex musculature at the lophophoral base appears promising for inferring phylogenetic relationships, but sufficient comparative data are currently lacking.

View Article: PubMed Central - HTML - PubMed

Affiliation: University of Vienna, Department of Morphology, Althanstra├če 14, 1090 Vienna, Austria. thomas.schwaha@univie.ac.at.

ABSTRACT

Background: Ectoprocta is a large lophotrochozoan clade of colonial suspension feeders comprising over 5.000 extant species. Their phylogenetic position within the Lophotrochzoa remains controversially discussed, but also the internal relationships of the major ectoproct subclades -Phylactolaemata, Stenolaemata, and Gymnolaemata - remains elusive. To gain more insight into the basic configuration of ectoproct muscle systems for phylogenetic considerations, we analysed the adult myoanatomy and the serotonergic nervous system as well as myogenesis in budding stages of the ctenostome Hislopia malayensis.

Results: In adults, the serotonergic nervous system is restricted to the lophophoral base with a high concentration in the cerebral ganglion and serotonergic perikarya between each pair of tentacles. Prominent smooth apertural muscles extend from the basal cystid wall to each lateral side of the vestibular wall. The musculature of the tentacle sheath consists of regular strands of smooth longitudinal muscles. Each tentacle is supplied with two bands of longitudinal muscles that show irregular striation. At the lophophoral base several muscles are present: (i) Short muscle fibres that proximally diverge from a single point from where they split distally into two separate strands. (ii) Proximally of the first group are smooth, longitudinal fibres that extend to the proximal-most side of the lophophoral base. (iii) Smooth muscle fibres, the buccal dilatators, traverse obliquely towards the pharynx, and (iv) a circular ring of smooth muscle fibres situated distally of the buccal dilatators. Retractor muscles are mainly smooth with short distal striated parts. The foregut consists mainly of striated ring musculature with only few longitudinal muscle fibres in the esophagus, while the remaining parts of the digestive tract solely exhibit smooth musculature. During budding, apertural and retractor muscles are first to appear, while the parietal muscles appear at a later stage.

Conclusions: The apertural muscles show high similarity within Ectoprocta and always consist of two sets of muscles. Gymnolaemates and Phylactolaemates show clear differences within their digestive tract musculature, the former showing smooth and longitudinal muscles to a much greater extent than the latter. The complex musculature at the lophophoral base appears promising for inferring phylogenetic relationships, but sufficient comparative data are currently lacking.

No MeSH data available.