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Type: Article
Published: 2017-07-03
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Two new species in the annelid genus Stygocapitella (Orbiniida, Parergodrilidae) with comments on their biogeography

Natural History Museum, University of Oslo, P.O. Box 1172, Blindern, NO-0318 Oslo, Norway. Zoological Research Museum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany.
Zoological Research Museum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany. Zoology and Developmental Biology, Department of Biology and Chemistry, University of Osnabrück, Barbarastr. 11, 49069 Osna-brück, Germany.
Zoological Research Museum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany. Zoology and Developmental Biology, Department of Biology and Chemistry, University of Osnabrück, Barbarastr. 11, 49069 Osna-brück, Germany.
Zoology and Developmental Biology, Department of Biology and Chemistry, University of Osnabrück, Barbarastr. 11, 49069 Osna-brück, Germany.
Zoology and Developmental Biology, Department of Biology and Chemistry, University of Osnabrück, Barbarastr. 11, 49069 Osna-brück, Germany.
Annelida Interstitial species Paleo-Tethys ancient distribution Meiofauna paradox integrative taxonomy multidimensional morphological disparity

Abstract

Many interstitial species with limited dispersal capacity are in fact complexes of cryptic species showing a seemingly cosmopolitan distribution. The interstitial annelid Stygocapitella subterranea (Orbiniida, Parergodrilidae) is such a complex with populations in Northern America, Europe, Australia, and New Zealand and a tropical distribution gap. Herein we present new records of Stygocapitella from South Africa, which is morphologically substantially different from S. subterranea. Additionally, using specimens from both hemispheres and morphological, nuclear and mitochondrial data as well as principal component analyses and a newly developed measurement for morphological disparity we show furthermore that the cryptic species complex of S. subterranea is not as cryptic as assumed as the Australian populations are morphologically and genetically different from the European population. Hence, we herein describe two new species, S. minuta and S. australis, within this complex from the Southern hemisphere. Additionally, we assigned a neotype for S. subterranea. This increases numbers of species known for Stygocapitella from one to three and for Parergodrilidae from two to four. Moreover, our results support an origin of this species complex on the Southern hemisphere and that both the split of S. minuta from the other two and S. subterranea from S. australis was several tens of millions years ago. Hence, the distribution of this complex was not driven by recent events, but rather it represents a strong case of decelerated morphological evolution as only slight differences in the morphology could be observed after all.

 

References

  1. Astrin, J.J. & Stüben, P.E. (2008) Phylogeny in cryptic weevils: molecules, morphology and new genera of western Palaearctic Cryptorhynchinae (Coleoptera : Curculionidae). Invertebrate Systematics, 22, 503–522.

    http://dx.doi.org/10.1071/IS07057

    Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22, 148–155.

    http://dx.doi.org/10.1016/j.tree.2006.11.004

    Boeckner, M., Sharma, J. & Proctor, H. (2009) Revisiting the meiofauna paradox: dispersal and colonization of nematodes and other meiofaunal organisms in low- and high-energy environments. Hydrobiologia, 624, 91–106.

    http://dx.doi.org/10.1007/s10750-008-9669-5

    Damm, S., Schierwater, B. & Hadrys, H. (2010) An integrative approach to species discovery in odonates: from character-based DNA barcoding to ecology. Molecular Ecology, 19, 3881–3893.

    http://dx.doi.org/10.1111/j.1365-294X.2010.04720.x

    Dawson, M.N. & Jacobs, D.K. (2001) Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). Biological Bulletin, 200, 92–96.

    http://dx.doi.org/10.2307/1543089

    de Luna Sales, J.B., Shaw, P.W., Haimovici, M., Markaida, U., Cunha, D.B., Ready, J., Figueiredo-Ready, W.M.B., Schneider, H. & Sampaio, I. (2013) New molecular phylogeny of the squids of the family Loliginidae with emphasis on the genus Doryteuthis Naef, 1912: Mitochondrial and nuclear sequences indicate the presence of cryptic species in the southern Atlantic Ocean. Molecular Phylogenetics and Evolution, 68, 293–299.

    http://dx.doi.org/10.1016/j.ympev.2013.03.027

    Derycke, S., Remerie, T., Backeljau, T., Vierstraete, A., Vanfleteren, J., Vincx, M. & Moens, T. (2008) Phylogeography of the Rhabditis (Pellioditis) marina species complex: evidence for long-distance dispersal, and for range expansions and restricted gene flow in the northeast Atlantic. Molecular Ecology, 17, 3306–3322.

    http://dx.doi.org/10.1111/j.1365-294X.2008.03846.x

    Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973.

    http://dx.doi.org/10.1093/molbev/mss075

    Ermak, T.H. & Eakin, R.M. (1976) Fine structure of the cerebral and pygidial ocelli in Chone ecaudata (Polychaeta: Sabellidae). Journal of Ultrastructure Research, 54, 243–260.

    http://dx.doi.org/10.1016/S0022-5320(76)80154-2

    Escalante, A.A. & Ayala, F.J. (1995) Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes. Proceedings of the National Academy of Sciences, 92, 5793–5797.

    http://dx.doi.org/10.1073/pnas.92.13.5793

    Franchini, P., Slabbert, R., Merwe, M.V.D., Roux, A. & Roodt-Wilding, R. (2010) Karyotype and Genome Size Estimation of Haliotis midae: Estimators to Assist Future Studies on the Evolutionary History of Haliotidae. Journal of Shellfish Research, 29, 945–950.

    http://dx.doi.org/10.2983/035.029.0428

    Gerlach, S.A. (1977) Means of meiofauna dispersal. Mikrofauna Meeresboden, 61, 89–103.

    Gharrett, A.J., Matala, A.P., Peterson, E.L., Gray, A.K., Li, Z.Z. & Heifetz, J. (2005) Two genetically distinct forms of rougheye rockfish are different species. Transactions of the American Fisheries Society, 134, 242–260.

    http://dx.doi.org/10.1577/T04-055.1

    Giere, O. (2009) Meiobenthology - The microscopic motile fauna of aquatic sediments. Springer-Verlag, Berlin/Heidelberg, 527 pp.

    Glasby, C.J. (2005) Polychaete distribution patterns revisited: an historical explanation. Marine Ecology, 26, 235–245.

    http://dx.doi.org/10.1111/j.1439-0485.2005.00059.x

    Hagerman, G.M. & Rieger, R.M. (1981) Dispersal of benthic meiofauna by wave and current action in Bogue Sound, N.C., USA. Pubblicazioni della Stazione Zoologica di Napoli, Section I: Marine Ecology, 2, 245–270.

    http://dx.doi.org/10.1111/j.1439-0485.1981.tb00099.x

    Hartmann-Schröder, G. (1983) Teil 9 - Die Polychaeten der antiborealen Südwestküste Australiens (zwischen Dunsborough im Norden und Denmark im Süden). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut, 80, 123–167.

    Higgins, R.P. & Thiel, H. (1988) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington D.C., 488 pp.

    Hillis, D.M. & Dixon, M.T. (1991) Ribosomal DNA: Molecular Evolution and Phylogenetic Inference. The Quarterly Review of Biology, 66, 411–453.

    http://dx.doi.org/10.1086/417338

    Hutter, C.R. & Guayasamin, J.M. (2012) A new cryptic species of glassfrog (Centrolenidae: Nymphargus) from Reserva Las Gralarias, Ecuador. Zootaxa, 3257, 1–21.

    Jans, W. & Römbke, J. (1989) Funde eines terrestrischen Polychaeten (Annelida) in Wäldern Baden-Württembergs. Carolinea, 47, 158–162.

    Jaume, D. (2007) Global diversity of spelaeogriphaceans & thermosbaenaceans (Crustacea; Spelaeogriphacea & Thermosbaenacea) in freshwater. Hydrobiologia, 595, 219–224.

    http://dx.doi.org/10.1007/s10750-007-9017-1

    Karling, T.G. (1958) Zur Kenntnis von Stygocapitella subterranea Knöllner und Parergodrilus heideri Reisinger. Arkiv för Zoologi, 1, 307–324.

    Katoh, K., Kuma, K.-I., Toh, H. & Miyata, T. (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research, 33, 511–518.

    http://dx.doi.org/10.1093/nar/gki198

    Knöllner, F. (1934) Stypocapitella subterranea nov. gen., nov. spec. Schriften der Naturwissenschaftlichen Vereins für Schleswig-Holstein, 20, 468–472.

    Kück, P., Meusemann, K., Dambach, J., Thormann, B., von Reumont, B.M., Wägele, J.W. & Misof, B. (2010) Parametric and non-parametric masking of randomness in sequence alignments can be improved and leads to better resolved trees. Frontiers in Zoology, 7, 10.

    http://dx.doi.org/10.1186/1742-9994-7-10

    Kück, P. & Struck, T.H. (2014) BaCoCa - A heuristic software tool for the parallel assessment of sequence biases in hundreds of gene and taxon partitions. Molecular Phylogenetics and Evolution, 70, 94–98.

    http://dx.doi.org/10.1016/j.ympev.2013.09.011

    Misof, B. & Misof, K. (2009) A Monte Carlo Approach Successfully Identifies Randomness in Multiple Sequence Alignments : A More Objective Means of Data Exclusion. Systematic Biology, 58, 21–34.

    http://dx.doi.org/10.1093/sysbio/syp006

    Pérez-Losada, M., Høeg, J.T. & Crandall, K.A. (2004) Unraveling the Evolutionary Radiation of the Thoracican Barnacles Using Molecular and Morphological Evidence: A Comparison of Several Divergence Time Estimation Approaches. Systematic Biology, 53, 244–264.

    http://dx.doi.org/10.1080/10635150490423458

    Perna, N.T. & Kocher, T.D. (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. Journal of Molecular Evolution, 41, 353–358.

    http://dx.doi.org/10.1007/BF01215182

    Purschke, G. (1981) Tolerance to freezing and supercooling of interstitial Turbellaria and Polychaeta from a sandy tidal beach of the North Sea Island of Sylt (North Sea). Marine Biology, 63, 257–267.

    http://dx.doi.org/10.1007/BF00395995

    Purschke, G. (1986) Ultrastructure of the nuchal organ in the interstitial polychaete Stygocapitella subterranea (Parergodrilidae). Zoologica Scripta, 15, 13–20.

    http://dx.doi.org/10.1111/j.1463-6409.1986.tb00204.x

    Purschke, G. (1987) Anatomy and ultrastructure of ventral pharyngeal organs and their phylogenetic importance in Polychaeta (Annelida) - III. The pharynx of the Parergodrilidae. Zoologische Jahrbücher Anatomie, 115, 331 - 362.

    Purschke, G. (1999) Terrestrial polychaetes – models for the evolution of the Clitellata (Annelida)? Hydrobiologia, 406, 87–99.

    http://dx.doi.org/10.1023/A:1003780032497

    Purschke, G. (2006) Problematic Annelid Groups. In: Rouse, G.W. & Pleijel, F. (Eds), Reproductive Biology and Phylogeny of Annelida. Science Publisher, Enfield, Jersey, Plymouth, pp. 639–667.

    Purschke, G. & Fursman, M. (2005) Spermatogenesis and spermatozoa in Stygocapitella subterranea (Annelida, Parergodrilidae), an enigmatic supralittoral polychaete. Zoomorphology, 124, 137–148.

    http://dx.doi.org/10.1007/s00435-005-0001-x

    Purschke, G. & Jördens, J. (2007) Male genital organs in the eulittoral meiofaunal polychaete Stygocapitella subterranea (Annelida, Parergodrilidae): ultrastructure, functional and phylogenetic significance. Zoomorphology, 126, 283–297.

    http://dx.doi.org/10.1007/s00435-007-0047-z

    R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Available from: http://www.R-project.org/ (accessed 20 August 2016)

    Rambaut, A. & Drummond, A.J. (2007) Tracer v1.4. Available from: http://beast.bio.ed.ac.uk/Tracer (accessed 14 August 2016)

    Reisinger, E. (1925) Ein landbewohnender Archiannelide. Zugleich ein Beitrag zur Systematik der Archianneliden. Zeitschrift für Morphologie und Ökologie der Tiere, 3, 197–254.

    http://dx.doi.org/10.1007/BF00408145

    Riser, N.W. (1980) The aberrant polychaete Stygocapitella from some American beaches. The Wasmann Journal of Biology, 38, 10–17.

    Riser, N.W. (1984) General observations on the intertidal interstitial fauna of New Zealand. Tane, 30, 239–250.

    Rocha-Olivares, A., Fleeger, J.W. & Foltz, D.W. (2001) Decoupling of molecular and morphological evolution in deep lineages of a meiobenthic harpacticoid copepod. . Molecular Biology and Evolution, 18, 1088–1102.

    http://dx.doi.org/10.1093/oxfordjournals.molbev.a003880

    Rull, J., Abraham, S., Kovaleski, A., Segura, D.F., Mendoza, M., Clara Liendo, M. & Teresa, V.M. (2013) Evolution of pre-zygotic and post-zygotic barriers to gene flow among three cryptic species within the Anastrepha fraterculus complex. Entomologia Experimentalis et Applicata, 148, 213–222.

    http://dx.doi.org/10.1111/eea.12094

    Sáez, A.G., Probert, I., Geisen, M., Quinn, P., Young, J.R. & Medlin, L.K. (2003) Pseudo-cryptic speciation in coccolithophores. Proceedings of the National Academy of Sciences, 100, 7163–7168.

    http://dx.doi.org/10.1073/pnas.1132069100

    Schmidt, H. & Westheide, W. (2000) Are the meiofaunal polychaetes Hesionides arenaria and Stygocapitella subterranea true cosmopolitan species? - results of RAPD-PCR investigations. Zoologica Scripta, 29, 17–27.

    http://dx.doi.org/10.1046/j.1463-6409.2000.00026.x

    Schmidt, P. (1969) Die quantitative Verteilung und Populationsdynamik des Mesopsammons am Gezeiten-Sandstrand der Nordsee-Insel Sylt1). II. Quantitative Verteilung und Populationsdynamik einzelner Arten. Internationale Revue der gesamten Hydrobiologie und Hydrographie, 54, 95–174.

    http://dx.doi.org/10.1002/iroh.19690540104

    Schmidt, P. (1970) Zonation of the interstitial polychaete Stygocapitella subterranea (Stygocapitellidae) in European sandy beaches. Marine Biology, 7, 319–323.

    http://dx.doi.org/10.1007/BF00750824

    Schmidt, P. (1972) Zonierung und jahreszeitliche Fluktuationen des Mesopsammons im Sandstrand von Schilksee (Kieler Bucht). Mikrofauna des Meeresbodens, 10, 1–60.

    Scotese, C.R. (2001) Atlas of Earth History, Volume 1, Paleogeography. PALEOMAP Project, Arlington, Texas, 52 pp.

    Scotese, C.R. (2002) PALEOMAP website. Available from: http://www.scotese.com (accessed 17 Oct. 2016)

    Smith, K.L., Harmon, L.J., Shoo, L.P. & Melville, J. (2011) Evidence of constrained phenotypic evolution in a cryptic species complex of agamid lizards. Evolution, 65, 976–992.

    http://dx.doi.org/10.1111/j.1558-5646.2010.01211.x

    Soisook, P., Bumrungsri, S., Satasook, C., Thong, V.D., Bu, S.S.H., Harrison, D.L. & Bates, P.J.J. (2008) A taxonomic review of Rhinolophus stheno and R. malayanus (Chiroptera: Rhinolophidae) from continental Southeast Asia: an evaluation of echolocation call frequency in discriminating between cryptic species. Acta Chiropterologica, 10, 221–242.

    http://dx.doi.org/10.3161/150811008X414818

    Sterrer, W. (1973) Plate tectonics as a mechanism for dispersal and speciation in interstitial sand fauna. Netherlands Journal of Sea Research, 7, 200–222.

    http://dx.doi.org/10.1016/0077-7579(73)90045-8

    Struck, T.H. (2006) Progenetic species in polychaetes (Annelida) and problems assessing their phylogenetic affiliation. Integrative and Comparative Biology, 46, 558–568.

    http://dx.doi.org/10.1093/icb/icj055

    Struck, T.H., Golombek, A., Weigert, A., Franke, Franziska A., Westheide, W., Purschke, G., Bleidorn, C. & Halanych, K.M. (2015) The Evolution of Annelids Reveals Two Adaptive Routes to the Interstitial Realm. Current Biology, 25, 1993–1999.

    http://dx.doi.org/10.1016/j.cub.2015.06.007

    Struck, T.H., Nesnidal, M.P., Purschke, G. & Halanych, K.M. (2008) Detecting possibly saturated positions in 18S and 28S sequences and their influence on phylogenetic reconstruction of Annelida (Lophotrochozoa). Molecular Phylogenetics and Evolution, 48, 628–645.

    http://dx.doi.org/10.1016/j.ympev.2008.05.015

    Struck, T.H., Westheide, W. & Purschke, G. (2002) Progenesis in Eunicida ("Polychaeta," Annelida) - separate evolutionary events? Evidence from molecular data. Molecular Phylogenetics and Evolution, 25, 190–199.

    http://dx.doi.org/10.1016/S1055-7903(02)00231-2

    Suatoni, E., Vicario, S., Rice, S., Snell, T. & Caccone, A. (2006) An analysis of species boundaries and biogeographic patterns in a cryptic species complex: The rotifer--Brachionus plicatilis. Molecular Phylogenetics and Evolution, 41, 86–98.

    http://dx.doi.org/10.1016/j.ympev.2006.04.025

    Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution, 28, 2731–2739.

    http://dx.doi.org/10.1093/molbev/msr121

    Todaro, M.A., Fleeger, J.W., Hu, Y.P., Hrincevich, A.W. & Foltz, D.W. (1996) Are meiofaunal species cosmopolitan? Morphological and molecular analysis of Xenotrichula intermedia (Gastrotricha: Chaetonotida). Marine Biology, 125, 735–742.

    http://dx.doi.org/10.1007/BF00349256

    Vinuesa, M.D.A., Sanches-Puelles, J.M. & Tibell, L. (2001) Intraspecific variation in Mycocalicium subtile (Mycocaliciaceae) elucidated by morphology and the sequences of the ITS1-5.8S-ITS2 region of rDNA. Mycological Research, 105, 323–330.

    http://dx.doi.org/10.1017/S0953756201003604

    Von Soosten, C., Schmidt, H. & Westheide, W. (1998) Genetic variability and relationships among geographically widely separated populations of Petitia amphophthalma (Polychaeta: Syllidae). Results from RAPD-PCR investigastions. Marine Biology, 131, 659–669.

    http://dx.doi.org/10.1007/s002270050358

    Wada, S., Kameda, Y. & Chiba, S. (2013) Long-term stasis and short-term divergence in the phenotypes of microsnails on oceanic islands. Molecular Ecology, 22, 4801–4810.

    http://dx.doi.org/10.1111/mec.12427

    Westheide, W. (1966) Zur Polychaetenfauna des Eulitorals der Nordseeinsel Sylt. Helgoländer wissenschaftliche Meeresuntersuchungen, 13, 203–209.

    http://dx.doi.org/10.1007/BF01611422

    Westheide, W. (1977) The geographical distribution of interstitial polychaetes. Mikrofauna Meeresboden, 61, 287–302.

    Westheide, W. (1984) The concept of reproduction in polychaetes with small body size: adaptations in interstitial species. In: Pfannenstiel, H.-D. & Fischer, A. (Eds.), Polychaete Reproduction. Fortschritte der Zoologie, Stuttgart, pp. 265–287.

    Westheide, W. (1987) Progenesis as a principle in meiofauna evolution. Journal of Natural History, 21, 843–854.

    http://dx.doi.org/10.1080/00222938700770501

    Westheide, W. (1991) The meiofauna of the Galapagos - A review. In: James, M.J. (Ed.), Galapagos Marine Invertebrates - Taxonomy, Biogeography, and Evolution in Darwin's Islands. Plenum Press, New York & London, pp. 37–73.

    Westheide, W. (2008) Polychaetes: Interstitial families. 2nd Edition. Field Studies Council, Shrewsbury, 169 pp.

    Westheide, W. & Hass, C. (2001) Molecular taxonomy: description of a cryptic Petitia species (Polychaeta: Syllidae) from the island of Mahé (Seychelles, Indian Ocean) using RAPD markers and ITS2 sequences. Journal of Zoological Systematics and Evolutionary Research, 39, 103–111.

    http://dx.doi.org/10.1046/j.1439-0469.2001.00166.x

    Westheide, W. & Purschke, G. (1988) Organism processing. In: Higgins, R.P. & Thiel, H. (Eds.), Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, pp. 146–160.

    Westheide, W. & Rieger, R.M. (1987) Systematics of the amphiatlantic Microphthalmus listensis species-group (Polychaeta: Hesionidae): Facts and concepts for reconstruction of phylogeny and speciation. Zeitschrift für zoologische Systematik and Evolutionsforschung, 25, 12–39.

    http://dx.doi.org/10.1111/j.1439-0469.1987.tb00911.x

    Worsaae, K. & Kristensen, R.M. (2005) Evolution of interstitial Polychaeta (Annelida). Hydrobiologia, 535–536, 319–340.

    http://dx.doi.org/10.1007/s10750-004-4417-y

    Worsfold, T.M. (2006) British records of the interstitial polychaete Stygocapitella subterranea (Annelida: Parergodrilidae). JMBA2 Biodiversity Records, 5429, 1–3.

    Worsfold, T.M. & Dyer, M.F. (1997) UK Marine SACs Project. Monitoring methods workshop at Plymouth (April 1997) and Millport (May 1997). (Contractor: Unicomarine, Letchworth). Joint Nature Conservation Committee, Peterborough, 20 pp.

    Zhong, M., Hansen, B., Nesnidal, M.P., Golombek, A., Halanych, K.M. & Struck, T.H. (2011) Detecting the symplesiomorphy trap: A multigene phylogenetic analysis for terebelliform annelids. BMC Evolutionary Biology, 11, 369.

    http://dx.doi.org/10.1186/1471-2148-11-369

    Zúñiga-Reinoso, Á. & Benítez, H.A. (2015) The overrated use of the morphological cryptic species concept: An example with Nyctelia darkbeetles (Coleoptera: Tenebrionidae) using geometric morphometrics. Zoologischer Anzeiger - A Journal of Comparative Zoology, 255, 47–53.

    http://dx.doi.org/10.1016/j.jcz.2015.01.004