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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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3D reconstructions of the myoanatomy of a creeping-type larva of Loxosomella murmanica. Reconstructions are based on the confocal microscopy dataset shown in Fig. 4f. Dorso-ventral muscle sets and enrolling muscle are highlighted. a: Fronto-lateral view. b: Ventral view
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Fig6: 3D reconstructions of the myoanatomy of a creeping-type larva of Loxosomella murmanica. Reconstructions are based on the confocal microscopy dataset shown in Fig. 4f. Dorso-ventral muscle sets and enrolling muscle are highlighted. a: Fronto-lateral view. b: Ventral view

Mentions: The musculature of the released entoproct creeping-type larva is very complex. A broad band of outer ring muscles runs in parallel to the prominent ring muscles of the prototroch and the apical organ (am, pm; Fig. 4a, c). Ventrally to the prototroch muscles is a horseshoe-shaped, posteriorly open muscle fiber, the enrolling muscle (em; Figs. 4b, f; 5e, f; 6a, b). Approximately 28 prototroch longitudinal muscles connect to the enrolling muscle (plm; Figs. 4; 5a, e). When contracted, the prototroch longitudinal muscles pull the enrolling muscle through the other prototroch ring muscles so that these ring muscles come to lie ventrally to the enrolling muscle (compare Fig. 4e and f). On each side of the larva, five to six lateral prototroch longitudinal muscles are connected to fine, rib-shaped dorso-ventral muscle fibers, which run close to the body wall (Figs. 5a, c, d, e; 6a, b). Six to eight abfrontal prototroch longitudinal muscles are attached to the abfrontally branched paired lateral longitudinal muscle, which curves ventrally in direction of the body wall between apical and frontal organ (Fig. 5a, d, e). A pair of pedal muscles, shaped like an inverted U and herein termed “pedal dorso-ventral muscles”, is surrounded by the prototroch muscles and the enrolling muscle and emerges close to the prototroch longitudinal muscles (Figs. 5a, d; 6a, b). The frontal part of each muscle resembles a trident (Figs. 5f; 6b). The abfrontal part is unbranched and intercrosses with the abfrontal part of the other muscle ventral to the prototroch in the posterior third of the foot (pdvm; Figs. 4b, f; 5f; 6b). Two pairs of muscles emerge from the dorsal tip of the pedal dorso-ventral muscles, the dorsal and lateral fronto-pedal muscles (Fig. 5a, d). Both pairs project towards the frontal organ ring muscle, whereas the dorsal fronto-pedal muscle is surrounded by the frontal organ ring muscles (Fig. 5a, b, d). The frontal dorso-ventral muscles are framed by the trident end of the pedal dorso-ventral muscles and seem to run towards the ring muscle system of the apical organ (Figs. 5a, d, 6a). The abfrontal dorso-ventral muscles run from both sides of the gut/anus straight towards the dorsal body wall (Figs. 5e; 6a, b). Another pair of muscles originates from the hindgut, orthogonally and in half of the length of the dorso-ventral muscles. It continues towards the lateral body wall (Fig. 5e). Muscles originating from the middle part of the gut seem to be attached to the dorsal body wall (Fig. 5a). Both muscle types originating from the gut are classified as “gut strap muscles”.Fig. 4


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)

3D reconstructions of the myoanatomy of a creeping-type larva of Loxosomella murmanica. Reconstructions are based on the confocal microscopy dataset shown in Fig. 4f. Dorso-ventral muscle sets and enrolling muscle are highlighted. a: Fronto-lateral view. b: Ventral view
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig6: 3D reconstructions of the myoanatomy of a creeping-type larva of Loxosomella murmanica. Reconstructions are based on the confocal microscopy dataset shown in Fig. 4f. Dorso-ventral muscle sets and enrolling muscle are highlighted. a: Fronto-lateral view. b: Ventral view
Mentions: The musculature of the released entoproct creeping-type larva is very complex. A broad band of outer ring muscles runs in parallel to the prominent ring muscles of the prototroch and the apical organ (am, pm; Fig. 4a, c). Ventrally to the prototroch muscles is a horseshoe-shaped, posteriorly open muscle fiber, the enrolling muscle (em; Figs. 4b, f; 5e, f; 6a, b). Approximately 28 prototroch longitudinal muscles connect to the enrolling muscle (plm; Figs. 4; 5a, e). When contracted, the prototroch longitudinal muscles pull the enrolling muscle through the other prototroch ring muscles so that these ring muscles come to lie ventrally to the enrolling muscle (compare Fig. 4e and f). On each side of the larva, five to six lateral prototroch longitudinal muscles are connected to fine, rib-shaped dorso-ventral muscle fibers, which run close to the body wall (Figs. 5a, c, d, e; 6a, b). Six to eight abfrontal prototroch longitudinal muscles are attached to the abfrontally branched paired lateral longitudinal muscle, which curves ventrally in direction of the body wall between apical and frontal organ (Fig. 5a, d, e). A pair of pedal muscles, shaped like an inverted U and herein termed “pedal dorso-ventral muscles”, is surrounded by the prototroch muscles and the enrolling muscle and emerges close to the prototroch longitudinal muscles (Figs. 5a, d; 6a, b). The frontal part of each muscle resembles a trident (Figs. 5f; 6b). The abfrontal part is unbranched and intercrosses with the abfrontal part of the other muscle ventral to the prototroch in the posterior third of the foot (pdvm; Figs. 4b, f; 5f; 6b). Two pairs of muscles emerge from the dorsal tip of the pedal dorso-ventral muscles, the dorsal and lateral fronto-pedal muscles (Fig. 5a, d). Both pairs project towards the frontal organ ring muscle, whereas the dorsal fronto-pedal muscle is surrounded by the frontal organ ring muscles (Fig. 5a, b, d). The frontal dorso-ventral muscles are framed by the trident end of the pedal dorso-ventral muscles and seem to run towards the ring muscle system of the apical organ (Figs. 5a, d, 6a). The abfrontal dorso-ventral muscles run from both sides of the gut/anus straight towards the dorsal body wall (Figs. 5e; 6a, b). Another pair of muscles originates from the hindgut, orthogonally and in half of the length of the dorso-ventral muscles. It continues towards the lateral body wall (Fig. 5e). Muscles originating from the middle part of the gut seem to be attached to the dorsal body wall (Fig. 5a). Both muscle types originating from the gut are classified as “gut strap muscles”.Fig. 4

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