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Zoomorphology

, Volume 138, Issue 1, pp 55–71 | Cite as

The organization of musculature and the nervous system in the pygidial region of phyllodocid annelids

  • Viktor V. StarunovEmail author
Original Paper

Abstract

The annelid body can be subdivided into three main regions: the prostomium, the body segments, and the pygidium. The prostomium and pygidium, originating from the episphere and the posterior part of the hyposphere of a trochophore larva, are usually mentioned as non-homologous to body segments. However, recent studies revealed that the pygidium of several annelid species is far more complex than previously mentioned and possesses some segment-like features. To assess the diversity of a pygidial organization, I describe the innervation and muscular system of the pygidium in 19 annelid species belonging to the order Phyllodocida using phalloidin labeling, immunohistochemistry and confocal scanning microscopy. The musculature of the pygidium varies between families and usually consists of the circular and/or horseshoe-shaped hindgut sphincter muscles. In several families it can be accompanied by small additional transversal or dorso-ventral muscles. In contrast to the variable musculature, the pygidial innervation is far more uniform and in general comprises two huge main longitudinal nerves, a terminal commissure between them, and paired circumpigidial nerves. The pygidial epithelium bears numerous receptor cell endings, suggesting that the pygidium may act as an important sensory organ. The obtained results are in accordance with the recent data and indicate that such muscular and nervous organization may be characteristic of the whole order Phyllodocida.

Keywords

Annelida Phyllodocida Nervous system Musculature Confocal microscopy 

Notes

Acknowledgements

The author is grateful to Prof. Dr. Thomas Bartolomaeus and Dr. Andrey (A) Dobrovolsky, Dr. Elena E. Voronezhskaya and Olga (B) Lavrova for help with result interpretation and fruitful discussions. I am also grateful to Alexey Miroliubov for the help with scanning electron microscopy. The work was supported by the research grant RFBR16-34-60134 mol_a_dk and by Zoological Institute Project AAAA-A17-117030110029-3. The scientific research was performed at the Center for molecular and cell technologies, Center for Culturing Collection of Microorganisms, center “CHROMAS” of St. Petersburg State University and “Taxon” Research Resource Center of Zoological Institute RAS (http://www.ckp-rf.ru/ckp/3038/?sphrase_id=8879024).

Compliance with ethical standards

Ethical standards

All applicable international, national, and institutional guidelines for the care and use of animals were followed. I neither used endangered species nor were the investigated animals collected in protected areas.

Supplementary material

Innervation of the pygidium in unidentified atypical Syllid (presumably Syllis fasciata) with single unpaired pygidial cirrus. 3D rotatable reconstruction (AVI 7759 KB)

435_2018_430_MOESM2_ESM.tif (138 mb)
Confocal z-stack showing the musculature of the pygidium in Harmothoe imbricata (TIF 141341 KB)

References

  1. Anderson DT (1966) The comparative embryology of the Polychaeta. Acta Zool 47:1–42CrossRefGoogle Scholar
  2. Andrade SCS, Novo M, Kawauchi GY et al (2015) Articulating “Archiannelids”: phylogenomics and annelid relationships, with emphasis on Meiofaunal Taxa. Mol Biol Evol 32(11):2860–2875.  https://doi.org/10.1093/molbev/msv157 CrossRefPubMedGoogle Scholar
  3. Bubko OV, Minichev YS (1972) Nervous system in Oweniidae (Polychaeta). Zoologichesky Zhurnal 51:1288–1299Google Scholar
  4. Filippova A, Purschke G, Tzetlin AB et al (2005) Reconstruction of the musculature of Magelona cf. mirabilis (Magelonidae) and Prionospio cirrifera (Spionidae) (Polychaeta, Annelida) by phalloidin labeling and cLSM. Zoomorphology 124:1–8.  https://doi.org/10.1007/s00435-004-0106-7 CrossRefGoogle Scholar
  5. Filippova A, Purschke G, Tzetlin AB, Müller MCM (2006) Three-dimensional reconstruction of the F-actin musculature of Dorvillea kastjani (Dorvilleidae: Polychaeta) by means of phalloidin-labelling and cLSM. Sci Mar 70:293–300.  https://doi.org/10.3989/scimar.2006.70s3293 CrossRefGoogle Scholar
  6. Filippova A, Purschke G, Tzetlin AB, Müller MCM (2010) Musculature in polychaetes: comparison of Myrianida prolifera (Syllidae) and Sphaerodoropsis sp. (Sphaerodoridae). Invertebr Biol 129:184–198.  https://doi.org/10.1111/j.1744-7410.2010.00191.x CrossRefGoogle Scholar
  7. Harrison FW, Gardiner SL (1992) Microscopic anatomy of invertebrates, volume 7, Annelida. Wiley-Liss, New YorkGoogle Scholar
  8. Helm C, Beckers P, Bartolomaeus T et al (2018) Convergent evolution of the ladder-like ventral nerve cord in Annelida. Front Zool 15:36CrossRefPubMedPubMedCentralGoogle Scholar
  9. Hessling R (2002) Metameric organisation of the nervous system in developmental stages of Urechis caupo (Echiura) and its phylogenetic implications. Zoomorphology 121:221–234.  https://doi.org/10.1007/s00435-002-0059-7 CrossRefGoogle Scholar
  10. Hessling R (2003) Novel aspects of the nervous system of Bonellia viridis (Echiura) revealed by the combination of immunohistochemistry, confocal laser-scanning microscopy and three-dimensional reconstruction. Hydrobiologia 496:225–239.  https://doi.org/10.1023/A:1026153016913 CrossRefGoogle Scholar
  11. Hessling R, Westheide W (2002) Are Echiura derived from a segmented ancestor? Immunohistochemical analysis of the nervous system in developmental stages of Bonellia viridis. J Morphol 252:100–113.  https://doi.org/10.1002/jmor.1093 CrossRefPubMedGoogle Scholar
  12. Heuer CM, Müller CH, Todt C, Loesel R (2010) Comparative neuroanatomy suggests repeated reduction of neuroarchitectural complexity in Annelida. Front Zool 7:13.  https://doi.org/10.1186/1742-9994-7-13 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Horton T, Kroh A, Ahyong S et al (2018) World register of marine species (WoRMS). http://www.marinespecies.org. Accessed 27 Dec 2018
  14. Ivanov I, Tzetlin A (1997) Fine structure of body cavity of Phyllodocidae (Annelida, Polychaeta). Morphofunctional analysis. Doklady Akademii Nauk 354:272–277Google Scholar
  15. Jirkov IA (2001) Polychaeta of the Arctic Ocean. Janus-K, MoscowGoogle Scholar
  16. Kerbl A, Bekkouche N, Sterrer W, Worsaae K (2015) Detailed reconstruction of the nervous and muscular system of Lobatocerebridae with an evaluation of its annelid affinity. BMC Evol Biol 15:277.  https://doi.org/10.1186/s12862-015-0531-x CrossRefPubMedPubMedCentralGoogle Scholar
  17. Kerbl A, Fofanova EG, Mayorova TD et al (2016) Comparison of neuromuscular development in two dinophilid species (Annelida) suggests progenetic origin of Dinophilus gyrociliatus. Front Zool 13:49.  https://doi.org/10.1186/s12983-016-0181-x CrossRefPubMedPubMedCentralGoogle Scholar
  18. Kristof A, Wollesen T, Wanninger A (2008) Segmental mode of neural patterning in sipuncula. Curr Biol 18:1129–1132.  https://doi.org/10.1016/j.cub.2008.06.066 CrossRefPubMedGoogle Scholar
  19. Kvist S, Siddall ME (2013) Phylogenomics of Annelida revisited: a cladistic approach using genome-wide expressed sequence tag data mining and examining the effects of missing data. Cladistics 29:435–448CrossRefGoogle Scholar
  20. Lehmacher C, Fiege D, Purschke G (2013) Immunohistochemical and ultrastructural analysis of the muscular and nervous systems in the interstitial polychaete Polygordius appendiculatus (Annelida). Zoomorphology 133:21–41.  https://doi.org/10.1007/s00435-013-0203-6 CrossRefGoogle Scholar
  21. Mchugh D (2000) Molecular phylogeny of the Annelida. Can J Zool 78:1873–1884.  https://doi.org/10.1139/z00-141 CrossRefGoogle Scholar
  22. McHugh D (2005) Molecular systematics of polychaetes (Annelida). Hydrobiologia 535/536:309–318.  https://doi.org/10.1007/s10750-004-4414-1 CrossRefGoogle Scholar
  23. Müller MCM, Henning L (2004) Ground plan of the polychaete brain—I. Patterns of nerve development during regeneration in Dorvillea bermudensis (Dorvilleidae). J Comp Neurol 471:49–58.  https://doi.org/10.1002/cne.20022 CrossRefPubMedGoogle Scholar
  24. Müller MCM, Westheide W (2002) Comparative analysis of the nervous systems in presumptive progenetic dinophilid and dorvilleid polychaetes (Annelida) by immunohistochemistry and cLSM. Acta Zool 83:33–48.  https://doi.org/10.1046/j.1463-6395.2002.00096.x CrossRefGoogle Scholar
  25. Müller MCM, Worsaae K (2006) CLSM Analysis of the phalloidin-stained muscle system in Nerilla antennata, Nerillidium sp. and Trochonerilla mobilis (Polychaeta; Nerillidae). J Morphol 267:885–896.  https://doi.org/10.1002/jmor CrossRefPubMedGoogle Scholar
  26. Orrhage L, Müller MCM (2005) Morphology of the nervous system of Polychaeta (Annelida). Hydrobiologia 535–536:79–111.  https://doi.org/10.1007/s10750-004-4375-4 CrossRefGoogle Scholar
  27. Purschke G (1997) Ultrastructure of Nuchal organs in polychaetes (Annelida)—new results and review. Acta Zool 78:123–143CrossRefGoogle Scholar
  28. Purschke G (2005) Sense organs in polychaetes (Annelida). Hydrobiologia 535/536:53–78.  https://doi.org/10.1007/s10750-004-4358-5 CrossRefGoogle Scholar
  29. Purschke G, Müller MCM (2006) Evolution of body wall musculature. Integr Comp Biol 46:497–507.  https://doi.org/10.1093/icb/icj053 CrossRefPubMedGoogle Scholar
  30. Purschke G, Bleidorn C, Struck T (2014) Systematics, evolution and phylogeny of Annelida—a morphological perspective. Mem Museum Victoria 71:247–269CrossRefGoogle Scholar
  31. Rimskaya-Korsakova NN, Kristof A, Malakhov VV, Wanninger A (2016) Neural architecture of Galathowenia oculata Zach, 1923 (Oweniidae, Annelida). Front Zool 13:5.  https://doi.org/10.1186/s12983-016-0136-2 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Rota E, Carchini G (1999) A new Polygordius (Annelida: Polychaeta) from Terra Nova Bay, Ross Sea, Antarctica. Polar Biol 21:201–213.  https://doi.org/10.1007/s003000050354 CrossRefGoogle Scholar
  33. Rouse GW, Fauchald K (1997) Cladistics and polychaetes. Zool Scr 26:139–204.  https://doi.org/10.1111/j.1463-6409.1997.tb00412.x CrossRefGoogle Scholar
  34. Rouse GW, Fauchald K (1998) Recent views on the status, delineation and classification of the Annelida. Am Zool 38:953–964.  https://doi.org/10.1093/icb/38.6.953 CrossRefGoogle Scholar
  35. Rouse GW, Pleijel F (2003) Problems in polychaete systematics. Hydrobiologia 496:175–189.  https://doi.org/10.1023/A:1026188630116 CrossRefGoogle Scholar
  36. Schindelin J, Arganda-Carreras I, Frise E et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682.  https://doi.org/10.1038/nmeth.2019 CrossRefGoogle Scholar
  37. Schlawny A, Hamann T, Müller MA, Pfannenstiel H (1991) The catecholaminergie system of an annelid (Ophryotrocha puerilis, Polychaeta). 265:175–184Google Scholar
  38. Siddall ME (2006) A molecular phylogeny of annelids. Cladistics 22:1–23CrossRefGoogle Scholar
  39. Starunov VV, Lavrova OB (2013) The structure of the nervous system and muscles of the pygidium in the polychaete Alitta virens (Nereididae). Dokl Biol Sci 451:235–237.  https://doi.org/10.1134/S0012496613040078 CrossRefPubMedGoogle Scholar
  40. Starunov VV, Zaitseva OV (2018) Comparative study of pygidial organization in polychaetes of the families nephtyidae and syllidae. Dokl Biol Sci 478:12–15.  https://doi.org/10.1134/S0012496618010039 CrossRefPubMedGoogle Scholar
  41. Starunov VV, Dray N, Belikova EV et al (2015) A metameric origin for the annelid pygidium? BMC Evol Biol 15:25.  https://doi.org/10.1186/s12862-015-0299-z CrossRefPubMedPubMedCentralGoogle Scholar
  42. Storch V (1968) Zur vergleichenden Anatomie der segmentalen Muskelsysteme und zur Verwandtschaft der Polychaeten Familien. Zeitschrift für Morphologie Ökologie der Tiere 63:251–342CrossRefGoogle Scholar
  43. Struck TH, Schult N, Kusen T et al (2007) Annelid phylogeny and the status of Sipuncula and Echiura. BMC Evol Biol 7:57.  https://doi.org/10.1186/1471-2148-7-57 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Struck TH, Paul C, Hill N et al (2011) Phylogenomic analyses unravel annelid evolution. Nature 471:95–98.  https://doi.org/10.1038/nature09864 CrossRefPubMedGoogle Scholar
  45. Struck TH, Golombek A, Weigert A et al (2015) The evolution of annelids reveals two adaptive routes to the interstitial realm. Curr Biol 25:1993–1999.  https://doi.org/10.1016/j.cub.2015.06.007 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Tzetlin AB, Filippova AV (2005) Muscular system in polychaetes (Annelida). Hydrobiologia 535:113–126.  https://doi.org/10.1007/s10750-004-1409-x CrossRefGoogle Scholar
  47. Weidhase M, Helm C, Bleidorn C (2015) Morphological investigations of posttraumatic regeneration in Timarete cf. punctata (Annelida: Cirratulidae). Zool Lett.  https://doi.org/10.1186/s40851-015-0023-2 CrossRefGoogle Scholar
  48. Weidhase M, Bleidorn C, Beckers P, Helm C (2016) Myoanatomy and anterior muscle regeneration of the fireworm Eurythoe cf. complanata (Annelida: Amphinomidae). J Morphol 277:306–315.  https://doi.org/10.1002/jmor.20496 CrossRefPubMedGoogle Scholar
  49. Weigert A, Bleidorn C (2016) Current status of annelid phylogeny. Org Divers Evol 16(2):345–362.  https://doi.org/10.1007/s13127-016-0265-7 CrossRefGoogle Scholar
  50. Weigert A, Helm C, Meyer M et al (2014) Illuminating the base of the annelid tree using transcriptomics. Mol Biol Evol 31:1391–1401.  https://doi.org/10.1093/molbev/msu080 CrossRefPubMedGoogle Scholar
  51. Zhadan A, Vortsepneva E, Tzetlin A (2014) Three-dimensional reconstruction of the musculature of Cossura pygodactylata Jones, 1956 (Annelida: Cossuridae). Zool Anz 253:181–191.  https://doi.org/10.1007/s00435-015-0282-7 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Invertebrate ZoologySaint Petersburg State UniversitySaint PetersburgRussia
  2. 2.Zoological Institute RASSaint PetersburgRussia

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