Abstract
Nemertodermatida is a small taxon of marine worm-like animals; its position in the tree of life is highly contested. The musculature of Nemertoderma westbladi and Meara stichopi is studied here in detail using fluorescent phalloidin and confocal microscopy. In both species, the musculature is composed of an outer layer of circular and an inner layer of longitudinal musculature, diagonal muscles form a distinct layer in N. westbladi, but in M. stichopi these fibres connect to both other layers. The supraterminally opening male pore and antrum are formed by invagination of the whole body-wall in both species, and the seminal vesicle is lined by a thin net of musculature only in full male maturity. Modifications of the ventral body-wall adjacent to the mouth are small and transient in N. westbladi including no extra musculature, whereas it consists of additional strong U-shaped musculature in M. stichopi. Myogenesis in N. westbladi is not finished in hatchlings and will be completed dorsally in juvenile specimens and ventrally in male mature ones, after the loss of the mouth. Musculature between the two species differs considerably and might give insights into the internal relationships of Nemertodermatida and might prove to be useful in studies investigating their phylogenetic position. More data of other species and developmental changes are needed.
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Abbreviations
- bwm:
-
Body-wall musculature
- cl:
-
Cilia
- cm:
-
Circular musculature (blue in sketches)
- cw:
-
Cell web
- db:
-
Dorsal bands of stronger longitudinal fibres in M. stichopi
- dm:
-
Diagonal musculature (green in sketches)
- eg:
-
Epidermal glands
- ef:
-
Epidermal fibres
- ep:
-
Epidermis
- int:
-
Intestine
- lm:
-
Longitudinal musculature (red in sketches)
- m:
-
Mouth
- ma:
-
Male antrum
- mo:
-
Male opening
- mco:
-
Male copulatory organ
- mv:
-
Microvilli
- ov:
-
Ovaries
- pm:
-
Parenchymal musculature
- st:
-
Statocyst with two statoliths
- stm:
-
Statocyst musculature
- sv:
-
Seminal vesicle
- U:
-
U-shaped musculature (orange in sketches)
References
Apelt G (1969) Fortpflanzungsbiologie, Entwicklungszyklen und vergleichende Frühentwicklung acoeler Turbellarien. Mar Biol 3:165–187
Baguñà J, Riutort M (2004) Molecular phylogeny of the Platyhelminthes. Can J Zool 82:168–193
Carranza S, Baguñà J, Ruitort M (1997) Are the Platyhelminthes a monophyletic primitive group? An assessment using 18S rDNA sequences. Mol Bio Evol 14:485–497
Costello HM, Costello DP (1938) Copulation in the acoelous turbellarian Polychoerus carmelensis. Biol Bull 75:85–98
Dyachuka V, Odintsova N (2013) Larval myogenesis in Echinodermata: conserved features and morphological diversity between class-specific larval forms of Echinoidae, Asteroidea, and Holothuroidea. Evo Dev 15:15–17
Egger B, Steinke D, Tarui H et al (2009) To be or not to be a flatworm: the acoel controversy. PLoS ONE 4:e5502
Ehlers U (1985) Das phylogenetische System der Plathelminthes. Gustav Fischer Verlag, Stuttgart
Faubel A (1976) Interstitielle Acoela (Turbellaria) aus dem Litoral der nordfriesischen Inseln Sylt und Amrum (Nordsee). Mitt Hamburg Zool Mus Ins 73:17–56
Faubel A, Dörjes J (1978) Flagellophora apelti gen. n. sp. n.: a remarkable representative of the order Nemertodermatida (Turbellaria: Archoophora). Senckenb Marit 10:1–13
Hejnol A, Obst M, Stamatakis A et al (2009) Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc R Soc B 276:4261–4270
Hooge MD (2001) Evolution of the body-wall musculature in the Platyhelminthes (Acoelomorpha, Catenulida, Rhabditophora). J Morph 249:171–194
Hyman LH (1937) Reproducive system and copulation in Amphiscolops langerhansi (Turbellaria Acoela)
Jimenez-Guri E, Paps J, Garcia-Fernandez J, Salo E (2006) Hox and ParaHox genes in Nemertodermatida, a basal bilaterian clade. Intern J Dev Biol 50:675–679
Jondelius U, Ruiz-Trillo I, Baguñà J, Ruitort M (2002) The Nemertodermatida are basal bilaterians and not members of the Platyhelminthes. Zool Scr 31:201–215
Jondelius U, Larsson K, Raikova OI (2004) Cleavage in Nemertoderma westbladi (Nemertodermatida) and its phylogenetic significance. Zoomorphology 123:221–225
Jondelius U, Wallberg A, Hooge M, Raikova OI (2011) How the worm got its pharynx: phylogeny, classification and Bayesian assessment of character evolution in Acoela. Syst Biol 60:845–871
Karling TG (1940) Zur Morphologie und Systematik der Alloeocoela Cumulata und Rhabdocoela Lecithophora (Turbellaria). Acta Zool Fenn 26:1–45
Ladurner P, Rieger R (2000) Embryonic muscle development of Convoluta pulchra (Turbellaria–Acoelomorpha, Platyhelminthes). Dev Biol 222:359–375
Lundin K (2000) Phylogeny of the Nemertodermatida (Acoelomorpha, Platyhelminthes). A cladistic analysis. Zool Scr 29:65–74
Mwinyi A, Bailly X, Bourlat SJ et al (2010) The phylogenetic position of Acoela as revealed by the complete mitochondrial genome of Symsagittifera roscoffensis. BMC Evol Biol 10:309
Paps J, Baguna J, Riutort M (2009) Bilaterian phylogeny: a broad sampling of 13 nuclear genes provides a new Lophotrochozoa phylogeny and supports a paraphyletic basal Acoelomorpha. Mol Biol Evol 26:2397–2406
Pfistermueller R, Tyler S (2001) Correlation of fluorescence and electron microscopy of F-actin-containing sensory cells in the epidermis of Convoluta pulchra (Platyhelminthes: Acoela). Acta Zool 83:15–24
Philippe H, Brinkmann H, Martinez P, Riutort M, Baguñà J (2007) Acoel flatworms are not platyhelminthes: evidence from Phylogenomics (J-N Volff, Ed,). PLoS ONE 2:e717
Philippe H, Brinkmann H, Copley RR et al (2011) Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470:255–258
Ruiz-Trillo I, Riutort M, Littlewood DTJ et al (1999) Acoel flatworms: earliest extant bilaterian metazoans, not members of Platyhelminthes. Science 283:1919–1923
Ruiz-Trillo I, Riutort M, Fourcade HM, Baguñà J, Boore JL (2004) Mitochondrial genome data support the basal position of Acoelomorpha and the polyphyly of the Platyhelminthes. Mol Phyl Evol 33:321–332
Semmler H, Bailly X, Wanninger A (2008) Myogenesis in the basal bilaterian Symsagittifera roscoffensis (Acoela). Front Zool 5:14
Sempere LF, Martinez P, Cole C, Baguñà J, Peterson KJ (2007) Phylogenetic distribution of microRNAs supports the basal position of acoel flatworms and the polyphyly of Platyhelminthes. Evol Dev 9:409–415
Smith JPS, Tyler S (1986) Frontal organs in the Acoelomorpha (Turbellaria): ultrastructure and phylogenetic significance. Hydrobiologia 132:71–78
Steinböck O (1930) Ergebnisse einer von E. Reisinger & O. Steinböck mit Hilfe des Rask-Örsted Fonds durchgefuehrten Reise in Grönland 1926. Vidensk Medd fra Dan Naturhist Fören
Steinmetz PRH, Kraus JEM, Larroux C et al (2012) Independent evolution of striated muscles in cnidarians and bilaterians. Nature 487:231–236
Sterrer W (1998) New and known Nemertodermatida-a revision. Belg J Zool 128:55–92
Telford MJ, Lockyer AE, Cartwright-Finch C, Littlewood DTJ (2003) Combined large and small subunit ribosomal RNA phylogenies support a basal position of the acoelomorph flatworms. Proc R Soc B 270:1077–1083
Todt C (2009) Structure and evolution of the pharynx simplex in acoel flatworms (Acoela). J Morph 270:271–290
Tyler S (1986) Ultrastructure of a remarkable food-gathering organ (?) in Flagellophora (Turbellaria, Nemertodermatida). Abstract. T Am Microsc Soc 105:90
Tyler S, Hooge M (2004) Comparative morphology of the body-wall in flatworms (Platyhelminthes). Can J Zool 82:194–210
Tyler S, Rieger RM (1999) Functional morphology of musculature in the acoelomate worm, Convoluta pulchra (Plathelminthes). Zoomorphology 119:127–141
Wahlberg MH (1998) The distribution of F-actin during the development of Diphyllobothrium dendriticum (Cestoda). Cell Tissue Res 291:561–570
Wallberg A, Curini-Galetti M, Ahmadzadeh A, Jondelius U (2007) Dismissal of Acoelomorpha: Acoela and Nemertodermatida are separate early bilaterian clades. Zool Scr 36:509–523
Westblad E (1937) Die Turbellariengattung Nemertoderma Steinböck. Acta Soc pro Fauna et Flora Fenn 60:45–89
Westblad E (1949) On Meara stichopi (Bock) Westblad, a new representative of Turbellaria Archoophora. Ark Zool 1:1–19
Westheide W, Rieger R (2004) Spezielle Zoologie Teil 1: Einzeller und Wirbellose Tiere. Spektrum Akademischer Verlag, Heidelberg
Acknowledgments
We wish to thank the crew at the Sven Lovén Centre for Marine Sciences (Kristineberg), Sweden, and the marine station in Espegrend, Norway. The work was funded by the Swedish Research Council. OR received financial support from the Royal Swedish Academy of Sciences and Russian Basic Research Foundation grants 09-04-01309 and 13-04.02002. We are also grateful for constructive critique and advice from the two anonymous reviewers.
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Communicated by A. Schmidt-Rhaesa.
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Meyer-Wachsmuth, I., Raikova, O.I. & Jondelius, U. The muscular system of Nemertoderma westbladi and Meara stichopi (Nemertodermatida, Acoelomorpha). Zoomorphology 132, 239–252 (2013). https://doi.org/10.1007/s00435-013-0191-6
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DOI: https://doi.org/10.1007/s00435-013-0191-6