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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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Myoanatomy of an adult Loxosomella murmanica specimen. Confocal micrograph with two embryos (arrowheads). Oral (i.e., ventral) facing upwards. Scale bar: 50 μm. Nucleic acid staining (blue), F-actin staining (red). arm, atrial ring muscles; bp, (empty) brood pouch; ca, calyx; ilm, intestinal longitudinal muscles; irm, intestinal ring muscles; lsm, longitudinal stalk muscles; st, stalk; tm, tentacle muscles
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Fig1: Myoanatomy of an adult Loxosomella murmanica specimen. Confocal micrograph with two embryos (arrowheads). Oral (i.e., ventral) facing upwards. Scale bar: 50 μm. Nucleic acid staining (blue), F-actin staining (red). arm, atrial ring muscles; bp, (empty) brood pouch; ca, calyx; ilm, intestinal longitudinal muscles; irm, intestinal ring muscles; lsm, longitudinal stalk muscles; st, stalk; tm, tentacle muscles

Mentions: Adult specimens of Loxosomella murmanica possess a flat, almost circular main body (calyx) with a crown that carries eight tentacles, a short stalk and an attachment disc, which is only slightly broader than the diameter of the stalk. The tentacle crown surrounds mouth and anus and marks the ventral (upper) side of the entoproct body [22]. In addition to the cerebral ganglion, the U-shaped digestive tract and the protonephridia [23], adults were observed to contain up to five embryos in the brood pouches of their calyces (Fig. 1). Early cleavage stages are located in the posterior-most part of the brood pouch. Later embryonic stages, close to hatching, are typically found in the uppermost part of the calyx. Released larvae are of the lecithotrophic creeping-type (Fig. 2).Fig. 1


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)

Myoanatomy of an adult Loxosomella murmanica specimen. Confocal micrograph with two embryos (arrowheads). Oral (i.e., ventral) facing upwards. Scale bar: 50 μm. Nucleic acid staining (blue), F-actin staining (red). arm, atrial ring muscles; bp, (empty) brood pouch; ca, calyx; ilm, intestinal longitudinal muscles; irm, intestinal ring muscles; lsm, longitudinal stalk muscles; st, stalk; tm, tentacle muscles
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig1: Myoanatomy of an adult Loxosomella murmanica specimen. Confocal micrograph with two embryos (arrowheads). Oral (i.e., ventral) facing upwards. Scale bar: 50 μm. Nucleic acid staining (blue), F-actin staining (red). arm, atrial ring muscles; bp, (empty) brood pouch; ca, calyx; ilm, intestinal longitudinal muscles; irm, intestinal ring muscles; lsm, longitudinal stalk muscles; st, stalk; tm, tentacle muscles
Mentions: Adult specimens of Loxosomella murmanica possess a flat, almost circular main body (calyx) with a crown that carries eight tentacles, a short stalk and an attachment disc, which is only slightly broader than the diameter of the stalk. The tentacle crown surrounds mouth and anus and marks the ventral (upper) side of the entoproct body [22]. In addition to the cerebral ganglion, the U-shaped digestive tract and the protonephridia [23], adults were observed to contain up to five embryos in the brood pouches of their calyces (Fig. 1). Early cleavage stages are located in the posterior-most part of the brood pouch. Later embryonic stages, close to hatching, are typically found in the uppermost part of the calyx. Released larvae are of the lecithotrophic creeping-type (Fig. 2).Fig. 1

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