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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Integrative systematics of clathrinid sponges: morphological, reproductive and phylogenetic characterisation of a new species of Leucetta from Antarctica (Porifera, Calcarea, Calcinea) with notes on the occurrence of flagellated sperm

Ana Riesgo A D , Fernanda F. Cavalcanti B , Nathan J. Kenny A , Pilar Ríos C , Javier Cristobo C and Emilio Lanna B
+ Author Affiliations
- Author Affiliations

A Department of Life Sciences, The Natural History Museum of London, Cromwell Road, London SW7 5BD, UK.

B Universidade Federal da Bahia, Instituto de Biologia, Rua Barão de Jeremoabo s/n, Ondina, Salvador/Bahia, 40170-115, Brazil.

C Instituto Español de Oceanografía, Avenuenida Príncipe de Asturias, 70 bis, 33212, Gijón, Asturias, Spain.

D Corresponding author. Email: A.Riesgo@nhm.ac.uk

Invertebrate Systematics 32(4) 827-841 https://doi.org/10.1071/IS17033
Submitted: 29 March 2017  Accepted: 1 December 2017   Published: 16 August 2018

Abstract

Our study reports on the occurrence of a new species of Leucetta (Calcinea, Calcarea) from the Southern Ocean, Leucetta giribeti, sp. nov., collected in the shallow waters (15 m depth) of Deception Island, South Shetland Islands. This new taxon is described based on a combination of morphological and molecular data, including the description of oocytes, embryos, larvae and sperm found in the choanosome. While female reproductive elements showed great similarities with those of other calcineans, sperm is reported here for the first time in the whole Calcinea subclass. Sperm cells are flagellated and possess a typical spermatic mid-piece, which is usually observed in cnidarians. In our phylogenetic analyses, we recovered Leucetta giribeti, sp. nov. as sister species of a clade formed by species of the genera Leucetta, Pericharax and Leucettusa. Although the clade in which Leucetta giribeti, sp. nov. is placed is supported by molecular and morphological features, we cannot propose a new genus due to uncertainties regarding the type species of the genus, Leucetta primigenia Haeckel, 1872. Our study reinforces the relevance of integrative approaches in the description of new taxa and contributes to resolving the poorly known reproductive patterns of Antarctic sponge species.

Additional keywords: phylogeny, reproductive biology, sperm morphology.


References

Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.Crossref | GoogleScholarGoogle Scholar |

Amano, S., and Hori, I. (2001). Metamorphosis of coeloblastula performed by multipotential larval flagellated cells in the calcareous sponge Leucosolenia laxa. The Biological Bulletin 200, 20–32.
Metamorphosis of coeloblastula performed by multipotential larval flagellated cells in the calcareous sponge Leucosolenia laxa.Crossref | GoogleScholarGoogle Scholar |

Anakina, R. P., and Drozdov, A. L. (2001). Gamete structure and fertilization in the Barents Sea sponge Leucosolenia complicata. Russian Journal of Marine Biology 27, 143–150.
Gamete structure and fertilization in the Barents Sea sponge Leucosolenia complicata.Crossref | GoogleScholarGoogle Scholar |

Bolger, A. M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120.

Borchiellini, C., Manuel, M., Alivon, E., Boury‐Esnault, N., Vacelet, J., and Le Parco, Y. (2001). Sponge paraphyly and the origin of Metazoa. Journal of Evolutionary Biology 14, 171–179.

Borojevic, R. (1966). Étude expérimentale de la différenciation des cellules de l’éponge au cours de son développement. Developmental Biology 14, 130–153.
Étude expérimentale de la différenciation des cellules de l’éponge au cours de son développement.Crossref | GoogleScholarGoogle Scholar |

Borojevic, R. (1969). Étude du développement et de la différenciation cellulaire d’éponges calcaires calcinèennes (genres Clathrina et Ascandra). Annales d’Embryologie et Morphologie de France 2, 15–36.

Borojevic, R., Boury-Esnault, N., Manuel, M., and Vacelet, J. (2002). Order Clathrinida Hartman, 1958. In ‘Systema Porifera’. (Eds J. Hooper and R. W. M. van Soest.) pp. 1141–1152. (Springer: New York, NY).

Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.
Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar |

Cavalcanti, F. F., Rapp, H. T., and Klautau, M. (2013). Taxonomic revision of Leucascus Dendy, 1892 (Porifera: Calcarea) with revalidation of Ascoleucetta Dendy & Frederick, 1924 and description of three new species. Zootaxa 3619, 275–314.
Taxonomic revision of Leucascus Dendy, 1892 (Porifera: Calcarea) with revalidation of Ascoleucetta Dendy & Frederick, 1924 and description of three new species.Crossref | GoogleScholarGoogle Scholar |

Dendy, A. (1918). ‘Calcareous Sponges.’ Australian Antarctic Expedition, 1911–14, series C VI(I), pp. 1–17. (Government Printer: Sydney.)

Dendy, A., and Frederick, L. M. (1924). On a collection of sponges from the Abrolhos Islands, Western Australia. Zoological Journal of the Linnean Society of London 35, 477–519.
On a collection of sponges from the Abrolhos Islands, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Dendy, A., and Row, R. W. H. (1913). The classification and phylogeny of the calcareous sponges, with a reference list of all the described species, systematically arranged. Proceedings of the Zoological Society 47, 704–813.

Dohrmann, M., Voigt, O., Erpenbeck, D., and Wörheide, G. (2006). Non-monophyly of most supraspecific taxa of calcareous sponges (Porifera, Calcarea) revealed by increased taxon sampling and partitioned Bayesian analysis of ribosomal DNA. Molecular Phylogenetics and Evolution 40, 830–843.

Downey, R. V., Griffiths, H. J., Linse, K., and Janussen, D. (2012). Diversity and distribution patterns in high southern latitude sponges. PLoS One 7, e41672.
Diversity and distribution patterns in high southern latitude sponges.Crossref | GoogleScholarGoogle Scholar |

Eddy, E. M. (1974). Fine structural observations on the form and distribution of nuage in germ cells of the rat. The Anatomical Record 178, 731–757.
Fine structural observations on the form and distribution of nuage in germ cells of the rat.Crossref | GoogleScholarGoogle Scholar |

Ereskovsky, A. V. (2010). The comparative embryology of sponges. (Springer Science & Business Media: Berlin, Germany.)

Ereskovsky, A. V., and Willenz, P. (2008). Larval development in Guancha arnesenae (Porifera, Calcispongiae, Calcinea). Zoomorphology 127, 175–187.
Larval development in Guancha arnesenae (Porifera, Calcispongiae, Calcinea).Crossref | GoogleScholarGoogle Scholar |

Giribet, G., Okusu, A., Lindgren, A. R., Huff, S. W., Schrödl, M., and Nishiguchi, M. K. (2006). Evidence for a clade composed of molluscs with serially repeated structures: monoplacophorans are related to chitons. Proceedings of the National Academy of Sciences of the United States of America 103, 7723–7728.
Evidence for a clade composed of molluscs with serially repeated structures: monoplacophorans are related to chitons.Crossref | GoogleScholarGoogle Scholar |

Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.Crossref | GoogleScholarGoogle Scholar |

Haeckel, E. (1872). ‘Die Kalkschwämme, Eine Monographie, Vols 1–3.’ (Verlag von Georg Reimer: Berlin, Germany.)

Haas, B.J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P.D., Bowden, J., Couger, M.B., Eccles, D., Li, B., Lieber, M., and MacManes, M.D. (2013). De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature protocols 8, 1494.

Hinsch, G. W. (1974). Comparative ultrastructure of cnidarian sperm. American Zoologist 14, 457–465.
Comparative ultrastructure of cnidarian sperm.Crossref | GoogleScholarGoogle Scholar |

Imešek, M., Pleše, B., Pfannkuchen, M., Godrijan, J., Pfannkuchen, D.M., Klautau, M., and Ćetković, H. (2014). Integrative taxonomy of four Clathrina species of the Adriatic Sea, with the first formal description of Clathrina rubra Sarà, 1958. Organisms diversity & evolution 14, 21–29.

Jenkin, C. F. (1908). The Calcarea of the National Antarctic Expedition 1901–1904. Natural History Reports 4, 1–52.

Johnson, M. F. (1978). Studies on the reproductive cycles of the calcareous sponges Clathrina coriacea and C. blanca. Marine Biology 50, 73–79.
Studies on the reproductive cycles of the calcareous sponges Clathrina coriacea and C. blanca.Crossref | GoogleScholarGoogle Scholar |

Johnson, M. F. (1979). Recruitment, growth, mortality and seasonal variations in the calcareous sponges Clathrina coriacea (Montagu) and C. blanca (Miklucho-Maclay) from Santa Catalina Island, California. Biologie des spongiaires. Colloques Internationaux. Centre National de la Recherche Scientifique (France) 291, 325–334.

Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.
MAFFT multiple sequence alignment software version 7: improvements in performance and usability.Crossref | GoogleScholarGoogle Scholar |

Klautau, M., Azevedo, F., Cóndor-Luján, B., Rapp, H. T., Collins, A., and de Moraes Russo, C. A. (2013). A molecular phylogeny for the order Clathrinida rekindles and refines Haeckel’s taxonomic proposal for calcareous sponges. Integrative and Comparative Biology 53, 447–461.
A molecular phylogeny for the order Clathrinida rekindles and refines Haeckel’s taxonomic proposal for calcareous sponges.Crossref | GoogleScholarGoogle Scholar |

Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar |

Lanna, E., and Klautau, M. (2010). Oogenesis and spermatogenesis in Paraleucilla magna (Porifera, Calcarea). Zoomorphology 129, 249–261.
Oogenesis and spermatogenesis in Paraleucilla magna (Porifera, Calcarea).Crossref | GoogleScholarGoogle Scholar |

Lanna, E., and Klautau, M. (2016). Some aspects of the oogenesis of three species of clathrinid sponges (Calcarea, Porifera). Journal of the Marine Biological Association of the United Kingdom 96, 529–539.
Some aspects of the oogenesis of three species of clathrinid sponges (Calcarea, Porifera).Crossref | GoogleScholarGoogle Scholar |

Leocorny, P., Alencar, A., Fromont, J., and Klautau, M. (2016). New Leucettidae de Laubenfels, 1936 (Porifera, Calcarea) from Western Australia. Zootaxa 4175, 319–334.
New Leucettidae de Laubenfels, 1936 (Porifera, Calcarea) from Western Australia.Crossref | GoogleScholarGoogle Scholar |

Maldonado, M., and Riesgo, A. (2008). Reproduction in Porifera: a synoptic overview. Treballs de la Societat Catalana de Biologia 59, 29–49.

Medina, M., Collins, A. G., Silberman, J. D., and Sogin, M. L. (2001). Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA. Proceedings of the National Academy of Sciences of the United States of America 98, 9707–9712.
Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA.Crossref | GoogleScholarGoogle Scholar |

Metschnikoff, E. (1879). Spongiologische Studien. Zeitschrift fur Wissenschartliche Zoologie 32, 349–387.

Minchin, E. A. (1896). Note on the larva and the postlarval development of Leucosolenia variabilis, H. sp., with remarks on the development of other Asconidae. Proceedings of the Royal Society of London 60, 42–52.
Note on the larva and the postlarval development of Leucosolenia variabilis, H. sp., with remarks on the development of other Asconidae.Crossref | GoogleScholarGoogle Scholar |

Minchin, E. A. (1900). Sponges – phylum Porifera. In ‘Treatise on Zoology, vol. 2. The Porifera and Coelenterata’. (Ed. E. R. Lankaster.) pp. 1–180. (Adam & Charles Black: London, UK.)

Poléjaeff, M. A. (1883). Reports on the Calcarea dredged by H.M.S. Challenger during the years 1873–1876. Reports of the scientific results of the voyage of H.M.S. Challenger. Zoology (Jena, Germany) 11, 1–88.

Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
jModelTest: phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar |

Posada, D., and Buckley, T. R. (2004). Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53, 793–808.
Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests.Crossref | GoogleScholarGoogle Scholar |

Rambaut, A., and Drummond, A. J. (2007). Tracer v1.5. Available at http://beast.bio.ed.ac.uk/Tracer. [Accessed 21 October 2016]

Rapp, H. T. (2006). Calcareous sponges of the genera Clathrina and Guancha (Calcinea, Calcarea, Porifera) of Norway (north‐east Atlantic) with the description of five new species. Zoological Journal of the Linnean Society 147, 331–365.
Calcareous sponges of the genera Clathrina and Guancha (Calcinea, Calcarea, Porifera) of Norway (north‐east Atlantic) with the description of five new species.Crossref | GoogleScholarGoogle Scholar |

Rapp, H. T., Janussen, D., and Tendal, O. S. (2011). Calcareous sponges from abyssal and bathyal depths in the Weddell Sea, Antarctica. Deep-sea Research. Part II, Topical Studies in Oceanography 58, 58–67.
Calcareous sponges from abyssal and bathyal depths in the Weddell Sea, Antarctica.Crossref | GoogleScholarGoogle Scholar |

Rapp, H. T., Goecke, C., Tendal, O. S., and Janussen, D. (2013). Two new species of calcareous sponges (Porifera: Calcarea) from the deep Antarctic Eckström Shelf and a revised list of species found in Antarctic waters. Zootaxa 3692, 149–159.
Two new species of calcareous sponges (Porifera: Calcarea) from the deep Antarctic Eckström Shelf and a revised list of species found in Antarctic waters.Crossref | GoogleScholarGoogle Scholar |

Richelle-Maurer, E., Van de Vyver, G., Vissers, S., and Coutinho, C.C. (1998). Homeobox-containing genes in freshwater sponges: characterization, expression, and phylogeny. In Molecular evolution: Evidence for monophyly of Metazoa (pp. 157–175). Springer, Berlin, Heidelberg.

Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar |

Sarà, M. (1955). Sulle cellule nutrici nell’ovogenesi delle Calcispongie Omoceli. Italian Journal of Zoology 22, 323–327.

Schmidt, O. (1877). Das Larvenstadium von Ascetta primordialis und Ascetta clathrus. Archiv für mikroskopische Anatomie 14, 249–263.
Das Larvenstadium von Ascetta primordialis und Ascetta clathrus.Crossref | GoogleScholarGoogle Scholar |

Tavaré, S. (1986). Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences 17, 57–86.

Thacker, R.W., Hill, A.L., Hill, M.S., Redmond, N.E., Collins, A.G., Morrow, C.C., Spicer, L., Carmack, C.A., Zappe, M.E., Pohlmann, D., and Hall, C. (2013). Nearly complete 28S rRNA gene sequences confirm new hypotheses of sponge evolution. Integrative and Comparative Biology 53, 373–387.

Tuzet, O. (1947). L’ovogenèse et la fécondation de l’éponge calcaire Leucosolenia (Clathrina) coriacea Mont. et de l’éponge siliceuse Reniera elegans Bow. Archives de Zoologie Expérimentale et Générale 85, 127–148.

Van Soest, R. W. M., Boury-Esnault, N., Hooper, J. N. A., Rützler, K. D., De Voogd, N. J., Alvarez de Glasby, B., Hajdu, E., Pisera, A. B., Manconi, R., Schoenberg, C., Janussen, D., Tabachnick, K. R., Klautau, M., Picton, B., Kelly, M., Vacelet, J., Dohrmann, M., Díaz, M.C., and Cárdenas, P. (2015). World Porifera database. Available at http://www.marinespecies.org/porifera, [Accessed 16 August 2017]

Voigt, O., and Wörheide, G. (2016). A short LSU rRNA fragment as a standard marker for integrative taxonomy in calcareous sponges (Porifera: Calcarea). Organisms, Diversity & Evolution 16, 53–64.
A short LSU rRNA fragment as a standard marker for integrative taxonomy in calcareous sponges (Porifera: Calcarea).Crossref | GoogleScholarGoogle Scholar |

Voigt, O., Wülfing, E., and Wörheide, G. (2012). Molecular phylogenetic evaluation of classification and scenarios of character evolution in calcareous sponges (Porifera, class Calcarea). PLoS One 7, e33417.
Molecular phylogenetic evaluation of classification and scenarios of character evolution in calcareous sponges (Porifera, class Calcarea).Crossref | GoogleScholarGoogle Scholar |

Wörheide, G., Nichols, S. A., and Goldberg, J. (2004). Intragenomic variation of the rDNA internal transcribed spacers in sponges (phylum Porifera): implications for phylogenetic studies. Molecular Phylogenetics and Evolution 33, 816–830.
Intragenomic variation of the rDNA internal transcribed spacers in sponges (phylum Porifera): implications for phylogenetic studies.Crossref | GoogleScholarGoogle Scholar |

Yang, Z. (1996). Maximum-likelihood models for combined analyses of multiple sequence data. Journal of Molecular Evolution 42, 587–596.
Maximum-likelihood models for combined analyses of multiple sequence data.Crossref | GoogleScholarGoogle Scholar |