Organisms Diversity & Evolution

, Volume 15, Issue 1, pp 1–21

Description of a new syllid species as a model for evolutionary research of reproduction and regeneration in annelids

  • María Teresa Aguado
  • Conrad Helm
  • Michael Weidhase
  • Christoph Bleidorn
Original Article

Abstract

Syllids are one of the most speciose annelid taxa and characterized by their variety of reproductive modes. We provide the description of a new species of Syllidae (Annelida, Phyllodocida), Typosyllis antoni n. sp., which is characterized by its distinct color pattern consisting of transversal red lines on the dorsum of anterior segments; long antennae and dorsal cirri with strong alternation in length; bidentate chaetae falciger like with long spinulation on edge, one tiny and thin acicula appearing in posterior segments in addition to thicker and pointed one, and a long proventricle. A phylogenetic analysis of Syllinae based on three genes supports that T. antoni n. sp. is sister species to Typosyllis heronislandensis. This sister group relationship may indicate a common ancestor from the Pacific. Moreover, we recommend several steps to unify the taxonomy with phylogenetic knowledge of this group. Using immunocytochemistry coupled with confocal laser scanning microscopy (cLSM), we describe the internal morphology of this species. The body wall is composed of two dorsal and two ventral longitudinal muscle bundles that form a distinct inner layer. The outer or “circular layer” of body wall musculature is represented by prominent transverse muscle fibers that exhibit a semicircular arrangement. The musculature of the uniramous parapodia is characterized by distinct parapodial retractor muscles, acicular protractor muscles, as well as prominent acicular and chaetal flexor muscle bundles. T. antoni n. sp. reproduces by schizogamic scissiparity producing dicerous stolons. This species is able to regenerate the anterior end, including the prostomium, the first chaetae-less segment with all appendages, and some additional chaetigers, depending on the dissection side. Regeneration of the proventricle, ventricle, caeca, or pharyngeal tooth is not detectable. In contrast, regeneration of the posterior end appears to be complete. The available data makes T. antoni n. sp. to be one of the best investigated syllids, emphasizing its potential as model for the whole group. Our analysis establishes a framework for future studies on the evolution of reproductive modes in Syllidae, and we outline research questions how they are related to regeneration and development.

Keywords

Annelida cLSM Development Musculature Polychaetes Regeneration Reproduction Syllidae 

References

  1. Aguado, M. T., & San Martín, G. (2006). Sílidos intersticiales (Syllidae: Polychaeta) del Parque Nacional de Coiba (Pacífico, Panamá). Revista de Biología Tropical, 54(3), 725–743.PubMedGoogle Scholar
  2. Aguado, M. T., & San Martín, G. (2009). Phylogeny of the Syllidae (Polychaeta) based on morphological data. Zoologica Scripta, 38, 379–402.Google Scholar
  3. Aguado, M.T; San Martín, G., & Nishi, E. (2006). Two new species of Syllidae (Annelida: Polychaeta) from Japan. Scientia Marina, 70S3, 9–16.Google Scholar
  4. Aguado, M. T., Nygren, A., & Siddall, M. E. (2007). Phylogeny of Syllidae (Polychaeta) based on combined molecular analysis of nuclear and mitochondrial genes. Cladistics, 23, 552–564.Google Scholar
  5. Aguado, M. T., San Martín, G., & Ten Hove, H. (2008). Syllidae (Annelida: Polychaeta) from Indonesia collected in the Siboga (1899–1900) and Snellius II (1984) expeditions. Zootaxa, 1673, 1–48.Google Scholar
  6. Aguado, M. T., San Martín, G., & Siddall, M. (2012). Systematics and Evolution of syllids (Annelida, Syllidae). Cladistics, 28, 234–250.CrossRefGoogle Scholar
  7. Allen, E. J. (1923). Regeneration and reproduction of the syllid Procerastea. Philosophical Transactions of the Royal Society, London, B., 211, 131–177.CrossRefGoogle Scholar
  8. del Castillo, J., Anderson, M., & Smith, D. S. (1972). Proventriculus of a marine annelid: muscle preparation with the longest recoded sarcomere. Proceedings of the National Academy of Sciences, USA, 69(7), 1669–1672.CrossRefGoogle Scholar
  9. Farris, J., Abert, V., Källersjö, M., Lipscomb, D., & Kluge, A. (1996). Parsimony jackknifing outperforms neighbor-joining. Cladistics, 12, 99–124.CrossRefGoogle Scholar
  10. Fauchald, K., & Jumars, P. A. (1979). The diet of worms: a study of polychaete feeding guilds. Oceanography and Marine Biology, 17, 193–284.Google Scholar
  11. Filippova, A., Purschke, G., Tzetlin, A. B., & Müller, M. C. M. (2010). Musculature in polychaetes: comparison of Myrianida prolifera (Syllidae) and Sphaerodoropsis sp. (Sphaerodoridae). Invertebrates Biology, 129, 184–198.CrossRefGoogle Scholar
  12. Fischer, A., & Dorresteijn, A. (2004). The polychaete Platynereis dumerilii (Annelida): a laboratory animal with spiralian cleavage, lifelong segment proliferation and a mixed benthic/pelagic life cycle. BioEssays, 26, 314–325.CrossRefPubMedGoogle Scholar
  13. Fischer, A., & Fischer, U. (1995). On the life-style and life-cycle of the luminescent polychaete Odontosyllis enopla (Annelida: Polychaeta). Invertebrate Biology, 114, 236–247.CrossRefGoogle Scholar
  14. Franke, H. D. (1983). Endocrine mechanisms mediating light-temperature effects on male reproductive activity in Typosyllis prolifera (Polychaeta, Syllidae). Wilhelm Roux’s Archives of Developmental Biology, 192, 95–102.CrossRefGoogle Scholar
  15. Franke, H. D. (1986). The role of light and endogenous factors in the timing of the reproductive cycle of Typosyllis prolifera and some other polychaetes. American Zoologist, 26, 433–445.Google Scholar
  16. Franke, H. D. (1999). Reproduction of the Syllidae. Hydrobiologia, 402, 39–55.CrossRefGoogle Scholar
  17. Glasby, C. J. (2000). Family Syllidae (In Beesley, P.L., Ross, G.J.B., & Glasby, C.J. (Eds.), Polychaetes and allies: The Southern Synthesis. Fauna of Australia. Vol. 4 Polychaeta, Myzostomida, Pogonophora, Echiura, Sipuncula (pp. 161–167)). Melbourne: CSIRO Publishing.Google Scholar
  18. Glasby, C. J., Schroeder, P. C., & Aguado, M. T. (2012). Branching out: a remarkable new branching syllid (Annelida) living in a Petrosia sponge (Porifera: Demospongiae). Zoological Journal of the Linnean Society, 164, 481–497.CrossRefGoogle Scholar
  19. Goloboff, P. A., Farris, J. S., & Nixon, K. (2008). TNT: a free program for Phylogenetic analysis. Cladistics, 24, 774–786.CrossRefGoogle Scholar
  20. Hartmann-Schröder, G. (1979). Teil 2. Die Polychaeten der tropischen Nordwestküste Australiens (zwischen Port Samson in Norden und Port Hedland in Süden). Zur Kenntnis des Eulitorals der australischen Küsten, unter besonderer Berücksichtigung der Polychaeten und Ostracoden. Mitteilungen aus dem hamburgischen zoologischen Museum und Institut, 76, 75–218.Google Scholar
  21. Hartmann-Schröder, G. (1981). Teil 6. Die Polychaeten der tropisch-subtropischen Westküste Australiens (zwischen Exmouth im Norden und Cervantes im Süden). Mitteilungen aus dem hamburgischen zoologischen Museum und Institut, 78, 19–96.Google Scholar
  22. Hartmann-Schröder, G. (1989). Teil 14. Die Polychaeten der antiborealen und subtropisch-tropischen Küste Südost-Australiens zwischen Lakes Entrance (Victoria) im Süden und Maclean (New South Wales) im Norden. Mitteilungen aus dem hamburgischen zoologischen Museum und Institut, 86, 11–63.Google Scholar
  23. Hartmann-Schröder, G. (1991). Teil 16. Die Polychaeten der subtropisch-tropischen bis tropischen Ostküste Australiens zwischen Maclean (New South Wales) und Gladstone (Queensland) sowie von Heron Island (Grosses Barriere-Riff). Mitteilungen aus dem hamburgischen zoologischen Museum und Institut, 88, 17–71.Google Scholar
  24. Haswell, W. A. (1920). Australian Syllidae, Eusyllidae and Autolytidae. Journal of the Linnean Society of London, 24, 90–112.Google Scholar
  25. Heacox, A. E., & Schroeder, P. (1982). The effects of prostomium and proventriculus removal on sex determination and gametogenesis in Typosyllis pulchra (Polychaeta: Syllidae). Wilhelm Roux's Archives of Developmental Biology, 191, 84–90.CrossRefGoogle Scholar
  26. Helm, C., Weigert, A., Mayer, G., & Bleidorn, C. (2013). Myoanatomy of Myzostoma cirriferum (Annelida, Myzostomida): implications for the evolution of the myzostomid body plan. Journal of Morphology, 274, 456–466.CrossRefPubMedGoogle Scholar
  27. Jeuniaux, C. (1969). Nutrition and digestion. In M. Florkin & B. T. Scheer (Eds.), Chemical Zoology (Annelida, Echiura, and Sipuncula, Vol. IV, pp. 69–91). New York: Academic.CrossRefGoogle Scholar
  28. Katoh, K., Misawa, K., Kuma, K., & Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30, 3059–3066.CrossRefPubMedCentralPubMedGoogle Scholar
  29. Lamarck, J. B. P. A. D. (1818). Histoire Naturelle des animaux sans vertèbres, présentant les caractères generaux et particuliers de ces animaux, leur distribution, leur classes, leur familles, leur genres, et la citation synonymique des principales espèces qui s´y rapportent; précedés d′une introduction offrant la détermination des caractères essentiels de l′Animal, sa distinction du végétal et des autres corps naturelles, enfin l′Exposition des Principes fondamentaux de la Zoologie (Vol. 5). Paris: Deterville. 612pp.Google Scholar
  30. Langerhans, P. (1879). Die Würmfauna van Madeira. Zeitschrift für Wissenschaftliche Zoologie, 33, 513–592.Google Scholar
  31. Licher, F. (1999). Revision der Gattung Typosyllis Langerhans, 1879 (Polychaeta: Syllidae). Morphologie, taxonomie und phylogenie. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft, 551, 1–336.Google Scholar
  32. Nygren, A. (1999). Phylogeny and reproduction in Syllidae (Polychaeta). Zoological Journal of the Linnean Society, 126, 365–386.CrossRefGoogle Scholar
  33. Martin, D., Temir, A. B., San Martín, G., & Gil, J. (2003). Inter-population variability and character description in the sponge-associated Haplosyllis spongicola complex (Polychaeta: Syllidae). Hydrobiologia, 496, 145–162.CrossRefGoogle Scholar
  34. Okada, Y. K. (1929). Regeneration and fragmentation in the syllidian polychaetes. Wilhelm Roux′ Archiv für Entwicklungsmechanik der Organismen, 115, 542–600.CrossRefGoogle Scholar
  35. Okada, Y. K. (1938). An internal factor controlling posterior regeneration in syllid polychaetes. Journal of the Marine Biological Association of the United Kingdom, 23, 75–78.CrossRefGoogle Scholar
  36. Pleijel, F. (2001). Syllidae, Grube, 1850 (In Rouse, G.W., & Pleijel, F. (Eds.), Polychaetes (pp. 102–105)). New York: Oxford University Press.Google Scholar
  37. Purschke, G., & Müller, M. C. M. (2006). Evolution of body wall musculature. Integrative and Comparative Biology, 46, 497–507.CrossRefPubMedGoogle Scholar
  38. San Martín, G. (1984). Estudio biogegráfico, faunístico y sistemático de los Poliquetos de la familia Sílidos (Syllidae: Polychaeta) en Baleares. Ediciones de la Universidad Complutense de Madrid, 187, 529.Google Scholar
  39. San Martín, G. (2003). Annelida, Polychaeta II: Syllidae. In Ramos, M.A. et al. (Eds.), Fauna Ibérica, vol. 21. Museo Nacional de Ciencias Naturales. CSIC. Madrid, 554pp.Google Scholar
  40. Simakov, O., Larsson, T. A., & Arendt, D. (2013). Linking micro- and macro-evolution at the cell type level: a view from the lophotrochozoan Platynereis dumerilii. Briefings in Functional Genomics, 12, 430–439.CrossRefPubMedGoogle Scholar
  41. Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.CrossRefPubMedGoogle Scholar
  42. Stamatakis, A., Hoover, P., & Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML Web servers. Systematic Biology, 57, 758–771.CrossRefPubMedGoogle Scholar
  43. Storch, V. (1968). Zur vergleichenden Anatomie der segmentalen Muskelsysteme und zur Verwandtschaft der Polychaeten-Familien. Zeitschrift für Morphologie der Tiere, 63, 251–342.CrossRefGoogle Scholar
  44. Tzetlin, A. B., & Filippova, A. V. (2005). Muscular system in polychaetes (Annelida). Hydrobiologia, 535(536), 113–126.Google Scholar
  45. Viguier, C. (1902). Sur la valeur morphologique de la tête des Annélides. Annales Des Sciences Naturelles (Zoologie), 25, 281–293.Google Scholar
  46. Weigert, A., Helm, C., Meyer, M., Nickel, B., Arendt, D., Hausdorf, B., Santos, S. R., Halanych, K. M., Purschke, G., Bleidorn, C., & Struck, T. H. (2014). Illuminating the base of the annelid tree using transcriptomics. Molecular Biology and Evolution, 31, 1391–1401.CrossRefPubMedGoogle Scholar
  47. Westheide, W. (1974). Interstitielle Fauna von Galapagos. XI. Pisionidae, Pilargidae, Syllidae. Mikrofauna Meeresbodens, 44, 195–338.Google Scholar
  48. Wissocq, J. C. (1966). La sexualisation du stolon chez Syllis spongicola Grübe. Cahiers de Biologie Marine, 7, 337–342.Google Scholar
  49. Zantke, J., Bannister, S., Rajan, V. B. V., Raible, F., & Tessmar-Raible, K. (2014). Genetic and genomic tools for the marine annelid Platynereis dumerilii. Genetics, 197, 19–31.CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2014

Authors and Affiliations

  • María Teresa Aguado
    • 1
  • Conrad Helm
    • 2
  • Michael Weidhase
    • 2
  • Christoph Bleidorn
    • 2
  1. 1.Departamento de Biología, Facultad de CienciasUniversidad Autónoma de Madrid, CantoblancoMadridSpain
  2. 2.Molecular Evolution and Systematics of Animals, Institute of BiologyUniversity of LeipzigLeipzigGermany

Personalised recommendations