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Muscular anatomy of an entoproct creeping-type larva reveals extraordinary high complexity and potential shared characters with mollusks.

Merkel J, Lieb B, Wanninger A - BMC Evol. Biol. (2015)

Bottom Line: Applying fluorescent markers and 3D modeling, we found that this larval type has the most complex musculature hitherto described for any lophotrochozoan larva.Interestingly, we found distinct muscle sets that are also present in several mollusks.The evolutionary driving forces that have led to the emergence of the extraordinarily complex muscular architecture in this short-lived, non-feeding entoproct larval type remain unknown, as are the processes that give rise to the highly different and much simpler muscular bodyplan of the adult entoproct during metamorphosis.

View Article: PubMed Central - PubMed

Affiliation: Institute of Zoology, Johannes Gutenberg University, 55099, Mainz, Germany. Julia_Merkel82@gmx.de.

ABSTRACT

Background: Entoprocta (Kamptozoa) is an enigmatic, acoelomate, tentacle-bearing phylum with indirect development, either via a swimming- or a creeping-type larva and still debated phylogenetic position within Lophotrochozoa. Recent morphological and neuro-anatomical studies on the creeping-type larva support a close relationship of Entoprocta and Mollusca, with a number of shared apomorphies including a tetraneurous nervous system and a complex serotonin-expressing apical organ. However, many morphological traits of entoproct larvae, in particular of the putative basal creeping-type larva, remain elusive.

Results: Applying fluorescent markers and 3D modeling, we found that this larval type has the most complex musculature hitherto described for any lophotrochozoan larva. The muscle systems identified include numerous novel and most likely creeping-type larva-specific structures such as frontal organ retractors, several other muscle fibers originating from the frontal organ, and longitudinal prototroch muscles. Interestingly, we found distinct muscle sets that are also present in several mollusks. These include paired sets of dorso-ventral muscles that intercross ventrally above the foot sole and a paired enrolling muscle that is distinct from the musculature of the body wall.

Conclusion: Our data add further morphological support for an entoproct-mollusk relationship (Tetraneuralia) and strongly argue for the presence of an enrolling musculature as well as seriality (but not segmentation) in the last common tetraneuralian ancestor. The evolutionary driving forces that have led to the emergence of the extraordinarily complex muscular architecture in this short-lived, non-feeding entoproct larval type remain unknown, as are the processes that give rise to the highly different and much simpler muscular bodyplan of the adult entoproct during metamorphosis.

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Confocal micrographs revealing the myoanatomy of different embryonic stages of Loxosomella murmanica. Scale bars: 20 μm. Nucleic acid staining (blue), F-actin staining (red). a: Ventro-lateral view of an early embryonic stage showing developing prototroch ring muscles (pm), body wall musculature (bm) and early prototroch longitudinal muscle fibers (plm). b: Lateral view of an early embryo. Developing body wall musculature (bm), prototroch ring muscles (pm) and prototroch longitudinal muscles (plm) are visible. The paired lateral longitudinal muscles (pllm) have formed. c: Apical view of an early embryo with a meshwork of concentric and longitudinal muscle fibers and developing apical ring muscles (am), body wall musculature (bm) and paired lateral longitudinal muscles (pllm). d: Ventral view of an older embryonic stage showing the prominent ring muscles of the prototroch (pm) and the frontal organ (fm). Prototroch longitudinal muscles (plm) and frontal organ retractor muscles (frm) have thickened. The left and right protonephridial porus with stained ring muscles (arrowheads) are visible on both sides of the embryo. e: Lateral view of an older embryonic stage with prominent frontal organ retractor muscles (frm). f: Fronto-lateral view of a late embryonic stage, probably close to hatching. The musculature resembles that of a fully developed creeping-type larva
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Fig3: Confocal micrographs revealing the myoanatomy of different embryonic stages of Loxosomella murmanica. Scale bars: 20 μm. Nucleic acid staining (blue), F-actin staining (red). a: Ventro-lateral view of an early embryonic stage showing developing prototroch ring muscles (pm), body wall musculature (bm) and early prototroch longitudinal muscle fibers (plm). b: Lateral view of an early embryo. Developing body wall musculature (bm), prototroch ring muscles (pm) and prototroch longitudinal muscles (plm) are visible. The paired lateral longitudinal muscles (pllm) have formed. c: Apical view of an early embryo with a meshwork of concentric and longitudinal muscle fibers and developing apical ring muscles (am), body wall musculature (bm) and paired lateral longitudinal muscles (pllm). d: Ventral view of an older embryonic stage showing the prominent ring muscles of the prototroch (pm) and the frontal organ (fm). Prototroch longitudinal muscles (plm) and frontal organ retractor muscles (frm) have thickened. The left and right protonephridial porus with stained ring muscles (arrowheads) are visible on both sides of the embryo. e: Lateral view of an older embryonic stage with prominent frontal organ retractor muscles (frm). f: Fronto-lateral view of a late embryonic stage, probably close to hatching. The musculature resembles that of a fully developed creeping-type larva

Mentions: The early embryo already exhibits a prominent prototroch ring muscle which consists of a few (four to five) muscle bundles which start to connect to neighboring muscles (pm; Fig. 3a). The body wall musculature runs in parallel to the prototroch and appears to form the precursor of the apical organ ring muscles (am, bm; Fig. 3a-c). Anlagen of prototroch longitudinal muscles are present, but are not as distinct as in older developmental stages (plm; Fig. 3a, b, d, f). Muscle fibers running from the dorso-lateral region of the early embryo seem to connect to some posteriorly positioned prototroch longitudinal muscles (Fig. 3b, c). The musculature of the apical region appears as a meshwork of concentric and longitudinal fibers (Fig. 3c).Fig. 3


Muscular anatomy of an entoproct creeping-type larva reveals extraordinary high complexity and potential shared characters with mollusks.

Merkel J, Lieb B, Wanninger A - BMC Evol. Biol. (2015)

Confocal micrographs revealing the myoanatomy of different embryonic stages of Loxosomella murmanica. Scale bars: 20 μm. Nucleic acid staining (blue), F-actin staining (red). a: Ventro-lateral view of an early embryonic stage showing developing prototroch ring muscles (pm), body wall musculature (bm) and early prototroch longitudinal muscle fibers (plm). b: Lateral view of an early embryo. Developing body wall musculature (bm), prototroch ring muscles (pm) and prototroch longitudinal muscles (plm) are visible. The paired lateral longitudinal muscles (pllm) have formed. c: Apical view of an early embryo with a meshwork of concentric and longitudinal muscle fibers and developing apical ring muscles (am), body wall musculature (bm) and paired lateral longitudinal muscles (pllm). d: Ventral view of an older embryonic stage showing the prominent ring muscles of the prototroch (pm) and the frontal organ (fm). Prototroch longitudinal muscles (plm) and frontal organ retractor muscles (frm) have thickened. The left and right protonephridial porus with stained ring muscles (arrowheads) are visible on both sides of the embryo. e: Lateral view of an older embryonic stage with prominent frontal organ retractor muscles (frm). f: Fronto-lateral view of a late embryonic stage, probably close to hatching. The musculature resembles that of a fully developed creeping-type larva
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4490756&req=5

Fig3: Confocal micrographs revealing the myoanatomy of different embryonic stages of Loxosomella murmanica. Scale bars: 20 μm. Nucleic acid staining (blue), F-actin staining (red). a: Ventro-lateral view of an early embryonic stage showing developing prototroch ring muscles (pm), body wall musculature (bm) and early prototroch longitudinal muscle fibers (plm). b: Lateral view of an early embryo. Developing body wall musculature (bm), prototroch ring muscles (pm) and prototroch longitudinal muscles (plm) are visible. The paired lateral longitudinal muscles (pllm) have formed. c: Apical view of an early embryo with a meshwork of concentric and longitudinal muscle fibers and developing apical ring muscles (am), body wall musculature (bm) and paired lateral longitudinal muscles (pllm). d: Ventral view of an older embryonic stage showing the prominent ring muscles of the prototroch (pm) and the frontal organ (fm). Prototroch longitudinal muscles (plm) and frontal organ retractor muscles (frm) have thickened. The left and right protonephridial porus with stained ring muscles (arrowheads) are visible on both sides of the embryo. e: Lateral view of an older embryonic stage with prominent frontal organ retractor muscles (frm). f: Fronto-lateral view of a late embryonic stage, probably close to hatching. The musculature resembles that of a fully developed creeping-type larva
Mentions: The early embryo already exhibits a prominent prototroch ring muscle which consists of a few (four to five) muscle bundles which start to connect to neighboring muscles (pm; Fig. 3a). The body wall musculature runs in parallel to the prototroch and appears to form the precursor of the apical organ ring muscles (am, bm; Fig. 3a-c). Anlagen of prototroch longitudinal muscles are present, but are not as distinct as in older developmental stages (plm; Fig. 3a, b, d, f). Muscle fibers running from the dorso-lateral region of the early embryo seem to connect to some posteriorly positioned prototroch longitudinal muscles (Fig. 3b, c). The musculature of the apical region appears as a meshwork of concentric and longitudinal fibers (Fig. 3c).Fig. 3

Bottom Line: Applying fluorescent markers and 3D modeling, we found that this larval type has the most complex musculature hitherto described for any lophotrochozoan larva.Interestingly, we found distinct muscle sets that are also present in several mollusks.The evolutionary driving forces that have led to the emergence of the extraordinarily complex muscular architecture in this short-lived, non-feeding entoproct larval type remain unknown, as are the processes that give rise to the highly different and much simpler muscular bodyplan of the adult entoproct during metamorphosis.

View Article: PubMed Central - PubMed

Affiliation: Institute of Zoology, Johannes Gutenberg University, 55099, Mainz, Germany. Julia_Merkel82@gmx.de.

ABSTRACT

Background: Entoprocta (Kamptozoa) is an enigmatic, acoelomate, tentacle-bearing phylum with indirect development, either via a swimming- or a creeping-type larva and still debated phylogenetic position within Lophotrochozoa. Recent morphological and neuro-anatomical studies on the creeping-type larva support a close relationship of Entoprocta and Mollusca, with a number of shared apomorphies including a tetraneurous nervous system and a complex serotonin-expressing apical organ. However, many morphological traits of entoproct larvae, in particular of the putative basal creeping-type larva, remain elusive.

Results: Applying fluorescent markers and 3D modeling, we found that this larval type has the most complex musculature hitherto described for any lophotrochozoan larva. The muscle systems identified include numerous novel and most likely creeping-type larva-specific structures such as frontal organ retractors, several other muscle fibers originating from the frontal organ, and longitudinal prototroch muscles. Interestingly, we found distinct muscle sets that are also present in several mollusks. These include paired sets of dorso-ventral muscles that intercross ventrally above the foot sole and a paired enrolling muscle that is distinct from the musculature of the body wall.

Conclusion: Our data add further morphological support for an entoproct-mollusk relationship (Tetraneuralia) and strongly argue for the presence of an enrolling musculature as well as seriality (but not segmentation) in the last common tetraneuralian ancestor. The evolutionary driving forces that have led to the emergence of the extraordinarily complex muscular architecture in this short-lived, non-feeding entoproct larval type remain unknown, as are the processes that give rise to the highly different and much simpler muscular bodyplan of the adult entoproct during metamorphosis.

Show MeSH