Systematic revision and phylogeny of the Polygordiidae Czerniavsky, 1881 (Annelida: Polychaeta) based on morphological and molecular methods
Final Report Abstract
The research conducted during this project resulted in a systematic revision based on various morphological (LM, SEM, cLSM) and molecular (sequencing of mitochondrial and nuclear genes) methods. Morphological characters were reassessed using LM and SEM, status of known species clarified, and new species identified. 14 species and 2 subspecies are currently considered valid, 3 additional ones are junior synonyms of other valid species and 2 more are considered doubtful. 4 new species need to be described. An up-to-date identification key to the valid species and barcodes for species investigated are provided. Studies on the musculature and the nervous system based on TEM and cLSM confirmed the anterior appendages as being immobile palps unlike those found in the Protodrilida (Protodrilus, Protodriloides, and Saccocirrus), currently considered the sister group to Polygordiidae. Using TEM regularly arranged minute circular muscle fibers were found in the body wall of Polygordius appendiculatus increasing the evidence that circular fibres belong to the annelid ground pattern. The basiepithelial and non-ganglionic organization of the ventral nerve cord as well as an orthogonal nervous system appear to represent a common feature of the genus Polygordius and might be more common in polychaetes than previously thought, thus representing plesiomorphic characters. The same applies for the predominance of longitudinal muscle fibers. During the project the organization, the distribution pattern, the gross morphology and the ultrastructure of photoreceptor-like sense organs was studied in detail in Polygordius erythrophthalmus and Polygordius lacteus. Several of these organs occur in a single individual and are rather complex being composed of different combinations of up to three different sensory cells, one rhabdomeric and two ciliary. Whereas structural differences are negligible between these two species, major differences can be observed between P. lacteus and P. appendiculatus. These results confirm our other morphological and molecular observations indicating that P. erythrophthalmus represents a junior synonym of P. lacteus. Thus ultrastructural investigations of photoreceptor-like sense organs provide additional characters of taxonomic value. Regarding the function of the pygidial glands it could be confirmed by life observations that they are used to anchor the worm to the substrate by the secretion of an adhesive substance; detachment is performed by a sudden brisk movement of the worm. This mechanism differs from the duo-gland system reported for some other interstitial annelids. The presence of a single type of gland cell producing the adhesive substance as found by our studies of the cellular structure of the pygidial glands using cLSM, LM and TEM supports our observations. Phylogenetic, phylogeographic and population genetics analyses were conducted based on molecular results. These analyses support the distinctness of species investigated which was previously based only on subtle morphological differences. Species distinction is likewise supported by haplotype networks based on COI data and by population genetics indices. Haplotype networks likewise do not indicate a clear separation of Mediterranean and Northeast Atlantic populations. In the Mediterranean Sea populations of three species are present and it appears that they independently colonized the Mediterranean Sea after the Messinian salinity crisis in the late Miocene (about 5.5 myrs ago). Our results support the hypothesis, that the colonization and establishing of stable populations took place much earlier in the Mediterranean Sea than in the North Sea. The colonizaton of the North Sea was probably initiated by only few individuals, representing a genetic bottleneck effect. Both Poygordius species present in the North Sea are characterized by fast growing populations indicating that both were capable to successfully colonize the respective habitat simultaneously. Specimens and DNA-extracts have been stored in the Senckenberg collections and are researchable online via SeSam (sesam.senckenberg.de) and the DNA Bank Network (www.dnabanknetwork.org). Barcoding sequences will be submitted to GenBank after publication of results. A review combining our results from the project together with information from the pertinent literature was contributed to the new edition of the „Handbook of Zoology“.
Publications
- (2010): Spatial and seasonal patterns in distribution and abundance of Polygordius larvae along the east coast of the United States. Abstract (Talk). 10th International Polychaete Conference, 20.-26.06.2010, Lecce, Italy
Ramey-Balci, P.A., Ambler, J. W. & Fiege, D.
- (2010): Three new species of Polygordius (Polygordiidae) from North America. Abstract (Poster). 10th International Polychaete Conference, 20.-26.06.2010, Lecce, Italy
Ramey-Balci, P.A. & Fiege, D.
- (2011): Global and local distribution patterns and diversity of an ecologically important group of marine worms. Abstract (Poster). 46th European marine Biology Symposium, 12.-16.11.2011, Rovinj, Croatia
Ramey-Balci, P. A. & Fiege, D.
- (2011): Polygordiidae – small enigmatic polychaetes of phylogenetic and ecological importance. Abstract (Talk). Senckenberg institutional seminar, 16.02.2011
Fiege, D. & Ramey-Balci, P.A.
- (2012): Polygordiida: Polygordiidae Czerniavsky, 1881 Zoology Online. De Gruyter, Berlin
Ramey-Balci, P. A., Fiege, D. & Purschke, G.
- (2012): Ultrastructure of photoreceptor-like sense organs in Polygordius (Annelida: Polychaeta): a possible character for species distinction? Abstract (Poster). 13th Annual Meeting of the Gesellschaft für Biologische Systematik (GfBS), 23.-25.02.2012, Bonn, Germany. Selected as the 2nd best poster
Wolff, L. I., Wilkens, V., Lehmacher, C., Purschke, G., Ramey-Balci, P. A. & Fiege, D.
- (2013): Nervous system and musculature in Polygordius appendiculatus (Annelida, Polygordiidae) – A model for the annelid ground pattern? Abstract (Talk). 11th International Polychaete Conference, 04.-09.08.2013, Sydney, Australia
Lehmacher, C., Fiege, D. & Purschke, G.
- (2013): Phylogeography and population genetics of Polygordius species and the colonization of the Mediterranean Sea. Abstract (Talk). 106th Annual Meeting of the German Zoological Society (DZG), 13.-16.09.2013, Münich, Germany
Ramey-Balci, P. A., Fiege, D. & Struck, T.
- (2013): Species distinction in Polygordius (Annelida): Ultrastructure of photoreceptor-like sense organs as an additional character? Abstract (Poster). 11th International Polychaete Conference, 04.- 09.08.2013, Sydney, Australia
Lehmacher, C., Wolff, L. I., Wilkens, V., Purschke, G., Ramey-Balci, P. A. & Fiege, D.
- (2014): Immunohistochemical and ultrastructural analysis of the muscular and nervous systems in the interstitial polychaete Polygordius appendiculatus (Annelida). Zoomorphology 133(1): 21-41
Lehmacher, C., Fiege, D. & Purschke, G.
(See online at https://doi.org/10.1007/s00435-013-0203-6) - (2016) Ultrastructural differences in presumed photoreceptive organs and molecular data as a means for species discrimination in Polygordius (Annelida, Protodriliformia, Polygordiidae). Organisms Diversity & Evolution 16 (3): 559-576.
Lehmacher, C., Ramey-Balci, P. A., Wolff, L. I., Fiege, D. & Purschke, G.
(See online at https://doi.org/10.1007/s13127-016-0272-8) - (2018): Molecular phylogeny, morphology, and distribution of Polygordius (Polychaeta: Polygordiidae) in the Atlantic and Mediterranean. Molecular Phylogenetics and Evolution, 127: 919-930.
Ramey-Balci, P. A., Fiege, D., Struck, T.
(See online at https://doi.org/10.1016/j.ympev.2018.06.039)
