Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2024-05-03
Page range: 1-28
Abstract views: 9
PDF downloaded: 0

Taxonomy and phylogeny of the family Suberitidae (Porifera: Demospongiae) in California

Ecology; Evolution; and Marine Biology Department; University of California; Santa Barbara
Scripps Oceanography; University of California San Diego; 9500 Gilman Drive; La Jolla; CA; 92093 USA
Committee on Evolutionary Biology; University of Chicago; Chicago; IL; USA; Current affiliation: Western Washington University; Bellingham; WA; USA
Hakai Institute; Campbell River; British Columbia
Hakai Institute; Campbell River; British Columbia
Department of Ecology and Evolution; Stony Brook University; Stony Brook; NY; USA; and Smithsonian Tropical Research Institute; PO Box 0843-03092; Balboa; Republic of Panama
Porifera sponges integrative taxonomy molecular systematics

Abstract

This study presents a comprehensive taxonomic revision of the family Suberitidae (Porifera: Demospongiae) for California, USA. We include the three species previously known from the region, document two additional species previously known from other regions, and formally describe four new species as Pseudosuberites latke sp. nov., Suberites californiana sp. nov., Suberites kumeyaay sp. nov., and Suberites agaricus sp. nov. Multi-locus DNA sequence data is presented for seven of the nine species, and was combined with all publicly available data to produce the most comprehensive global phylogeny for the family to date. By integrating morphological and genetic data, we show that morphological characters may be sufficient for regional species identification but are likely inadequate for global classification into genera that reflect the evolutionary history of the family. We therefore propose that DNA sequencing is a critical component to support future taxonomic revisions.

References

  1. Abe, T., Sahin, F.P., Akiyama, K., Naito, T., KISHIGAMI, M., Miyamoto, K., Sakakibara, Y. & Uemura, D. (2012) Construction of a metagenomic library for the marine sponge Halichondria okadai. Bioscience, Biotechnology, and Biochemistry, 76, 633–639. https://doi.org/10.1271/bbb.110533
  2. Agne, S., Ekins, M., Galitz, A., Hofreiter, M., Preick, M., Straube, N., Wörheide, G. & Erpenbeck, D. (2022) Keratose sponge MuseOMICS: setting reference points in dictyoceratid demosponge phylogeny. Zootaxa, 5195, 296–300. https://doi.org/10.11646/zootaxa.5195.3.9
  3. Austin, W.C., Ott, B.S., Reiswig, H.M., Romagosa, P. & McDaniel, N.G. (2014) Taxonomic review of Hadromerida (Porifera, Demospongiae) from British Columbia, Canada, and adjacent waters, with the description of nine new species. Zootaxa, 3823 (1), 1–84. https://doi.org/10.11646/zootaxa.3823.1.1
  4. Bakus, G.J. & Green, K.D. (1987) The distribution of marine sponges collected from the 1976–1978 Bureau of Land Management Southern California Bight program. Bulletin of the Southern California Academy of Sciences, 86, 57–88.
  5. Becking, L.E., Erpenbeck, D., Peijnenburg, K.T.C.A. & Voogd, N.J. de (2013) Phylogeography of the sponge Suberites diversicolor in Indonesia: insights into the evolution of marine lake populations. PLOS ONE 8, e75996. https://doi.org/10.1371/journal.pone.0075996
  6. Bowerbank, J.S. (1866) A Monograph of the British Spongiadae. Vol. 2. Ray Society, London, 388 pp. [https://biodiversitylibrary.org/page/1905089]
  7. Brøndsted, H.V. (1933) The Godthaab Expedition 1928. Porifera. Meddelelser om Grønland, 79, 1–25.
  8. Carballo, J.L., Cruz-Barraza, J.A., Vega, C., Nava, H. & del Carmen Chávez-Fuentes, M. (2019) Sponge diversity in eastern tropical Pacific coral reefs: an interoceanic comparison. Scientific Reports, 9, 9409. https://doi.org/10.1038/s41598-019-45834-4
  9. Cóndor-Luján, B., Arteaga, A., Polo, C., Arroyo, Y., Willenz, P. & Hajdu, E. (2023) Shallow Suberitida (Porifera, Demospongiae) from Peru. Zootaxa, 5264 (4), 451–489. https://doi.org/10.11646/zootaxa.5264.4.1
  10. de Voogd, N.J., Alvarez, B., Boury-Esnault, N., Cárdenas, P., Díaz, M.-C., Dohrmann, M., Downey, R., Goodwin, C., Hajdu, E., Hooper, J.N.A., Kelly, M., Klautau, M., Lim, S.C., Manconi, R., Morrow, C.C. Pisera, A.B., Pinheiro, U., Pisera, A.B., Ríos, P., Rützler, K., Schönberg, C., Turner, T.L., Vacelet, J., van Soest, R.W.M. & Xavier, J. (2023) World Porifera Database. Available from: https://www.marinespecies.org/porifera (accessed 3 January 2023) https://doi.org/10.14284/359
  11. Delle Chiaje, S. (1828) Memorie sulla storia e notomia degli animali senza vertebre del regno di Napoli / di Stefano delle Chiaje. Vol. 3. Stamperia della societa tipografica, Napoli, 232 pp.
  12. Dickinson, M.G. (1945) Sponges of the Gulf of California. In: Reports on the collections obtained by Allan Hancock Pacific Expeditions of Velero III off the coast of Mexico, Central America, South America, and Galapagos Islands in 1932, in 1933, in 1934, in 1935, in 1936, in 1937, in 1939, and 1940. The University of Southern California Press, Los Angeles, California, pp. 1–55.
  13. Ereskovsky, A., Kovtun, O.A., Pronin, K.K., Apostolov, A., Erpenbeck, D. & Ivanenko, V. (2018) Sponge community of the western Black Sea shallow water caves: diversity and spatial distribution. PeerJ, 6, e4596. https://doi.org/10.7717/peerj.4596
  14. Erpenbeck, D., Duran, S., Rützler, K., Paul, V., Hooper, J. & Wörheide, G. (2007) Towards a DNA taxonomy of Caribbean demosponges: a gene tree reconstructed from partial mitochondrial CO1 gene sequences supports previous rDNA phylogenies and provides a new perspective on the systematics of Demospongiae. Journal of the Marine Biological Association of the United Kingdom, 87, 1563–1570. https://doi.org/10.1017/S0025315407058195
  15. Erpenbeck, D., Hall, K., Alvarez, B., Büttner, G., Sacher, K., Schätzle, S., Schuster, A., Vargas, S., Hooper, J. & Wörheide, G. (2012) The phylogeny of halichondrid demosponges: past and present re-visited with DNA-barcoding data. Organisms Diversity & Evolution, 12, 57–70. https://doi.org/10.1007/s13127-011-0068-9
  16. Folmer, O., Black, M., Wr, H. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial Cytochrome C oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.
  17. Fortunato, H.F.M., Pérez, T. & Lôbo-Hajdu, G. (2020) Morphological description of six species of Suberitida (Porifera: Demospongiae) from the unexplored north-eastern coast of Brazil, with emphasis on two new species. Journal of the Marine Biological Association of the United Kingdom, 100, 389–400. https://doi.org/10.1017/S0025315420000296
  18. Geller, J., Meyer, C., Parker, M. & Hawk, H. (2013) Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Molecular Ecology Resources, 13, 851–861. https://doi.org/10.1111/1755-0998.12138
  19. Hartman, W.D. (1975) Phylum Porifera. In: Smith, R.I. & Carlton, J.T. (Eds.), Light’s Manual: Intertidal Invertebrates of the Central California Coast. 3rd Edition. University of California Press, Berkeley, California, pp. 32–64.
  20. Hoang, D., Chernomor, O., von Haeseler, A., Minh, B. & Vinh, L. (2018) UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35, 518–522. https://doi.org/10.1093/molbev/msx281
  21. Huang, D., Meier, R., Todd, P.A. & Chou, L.M. (2008) Slow mitochondrial COI sequence evolution at the base of the Metazoan tree and its implications for DNA barcoding. Journal of Molecular Evolution, 66, 167–174. https://doi.org/10.1007/s00239-008-9069-5
  22. Idan, T., Shefer, S., Feldstein, T., Yahel, R., Huchon, D. & Ilan, M. (2018) Shedding light on an East-Mediterranean mesophotic sponge ground community and the regional sponge fauna. Mediterranean Marine Science, 19, 84–106. https://doi.org/10.12681/mms.13853
  23. Johnson, G. (1842) A history of British sponges and lithophytes. W.H. Lizars, Edinburgh, ii + 264 pp. https://doi.org/10.5962/bhl.title.51495
  24. Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. https://doi.org/10.1038/nmeth.4285
  25. Katoh, K., Rozewicki, J. & Yamada, K.D. (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20, 1160–1166. https://doi.org/10.1093/bib/bbx108
  26. Lambe, L.M. (1893) On some sponges from the Pacific Coast of Canada and Behring Sea. Transactions of the Royal Society of Canada, 10, 67–78.
  27. Lambe, L.M. (1895) Sponges from the Western Coast of North America. Transactions of the Royal Society of Canada, 12, 113–138.
  28. de Laubenfels, M.W. (1926) New sponges from California. Annals and Magazine of Natural History, 9, 567–573. https://doi.org/10.1080/00222932608633444
  29. de Laubenfels, M.W. (1930) The Sponges of California. Stanford University Bulletin, 5, 24–29.
  30. de Laubenfels, M.W. (1932) The marine and fresh-water sponges of California. Proceedings of the United States National Museum, 81, 1–140. https://doi.org/10.5479/si.00963801.81-2927.1
  31. de Laubenfels, M.W. (1935) Some sponges of Lower California (Mexico). American Museum Novitates, 779, 1–14.
  32. de Laubenfels, M.W. (1961) Porifera of Friday Harbor and vicinity. Pacific Science, 15, 192–202.
  33. Lawley, J.W., Gamero-Mora, E., Maronna, M.M., Chiaverano, L.M., Stampar, S.N., Hopcroft, R.R., Collins, A.G. & Morandini, A.C. (2021) The importance of molecular characters when morphological variability hinders diagnosability: systematics of the moon jellyfish genus Aurelia (Cnidaria: Scyphozoa). PeerJ, 9, e11954. https://doi.org/10.7717/peerj.11954
  34. Lee, W., Elvin, D. & Reiswig, H. (2007) The sponges of California: A guide and key to the marine sponges of California. Monterey Bay Sanctuary Foundation, Monterey, California, 395 pp.
  35. Lee, W.L., Reiswig, H.M., Austin, W.C. & Lundsten, L. (2012) An extraordinary new carnivorous sponge, Chondrocladia lyra, in the new subgenus Symmetrocladia (Demospongiae, Cladorhizidae), from off of northern California, USA. Invertebrate Biology, 131, 259–284. https://doi.org/10.1111/ivb.12001
  36. Letunic, I. & Bork, P. (2019) Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Research, 47, W256–W259. https://doi.org/10.1093/nar/gkz239
  37. López-Legentil, S., Erwin, P.M., Henkel, T.P., Loh, T.L. & Pawlik, J.R. (2010) Phenotypic plasticity in the Caribbean sponge Callyspongia vaginalis (Porifera: Haplosclerida). Scientia Marina, 74, 445–453. https://doi.org/10.3989/scimar.2010.74n3445
  38. Lukić-Bilela, L., Brandt, D., Pojskić, N., Wiens, M., Gamulin, V. & Müller, W.E.G. (2008) Mitochondrial genome of Suberites domuncula: Palindromes and inverted repeats are abundant in non-coding regions. Gene, 412, 1–11. https://doi.org/10.1016/j.gene.2008.01.001
  39. Lundsten, L., Reiswig, H.M. & Austin, W.C. (2014) Four new species of Cladorhizidae (Porifera, Demospongiae, Poecilosclerida) from the Northeast Pacific. Zootaxa, 3786, 101–123. https://doi.org/10.11646/zootaxa.3786.2.1
  40. Melis, P., Riesgo, A., Taboada, S. & Manconi, R. (2016) Coping with brackish water: A new species of cave-dwelling Protosuberites Porifera: Demospongiae: Suberitidae) from the Western Mediterranean and a first contribution to the phylogenetic relationships within the genus. Zootaxa, 4208 (4), 349–364. https://doi.org/10.11646/zootaxa.4208.4.3
  41. Morozov, G., Sabirov, R. & Zimina, O. (2018) Sponge fauna of the New Siberian Shoal: biodiversity and some features of formation. Journal of Natural History, 52, 2961–2992. https://doi.org/10.1080/00222933.2018.1554166
  42. Morrow, C. & Cárdenas, P. (2015) Proposal for a revised classification of the Demospongiae (Porifera). Frontiers in Zoology, 12, 1–27. https://doi.org/10.1186/s12983-015-0099-8
  43. Morrow, C., Cárdenas, P., Boury-Esnault, N., Picton, B., McCormack, G., van Soest, R., Collins, A., Redmond, N., Maggs, C., Sigwart, J. & Allcock, L.A. (2019) Integrating morphological and molecular taxonomy with the revised concept of Stelligeridae (Porifera: Demospongiae). Zoological Journal of the Linnean Society, 187, 31–81. https://doi.org/10.1093/zoolinnean/zlz017
  44. Morrow, C.C., Picton, B.E., Erpenbeck, D., Boury-Esnault, N., Maggs, C.A. & Allcock, A.L. (2012) Congruence between nuclear and mitochondrial genes in Demospongiae: A new hypothesis for relationships within the G4 clade (Porifera: Demospongiae). Molecular Phylogenetics and Evolution, 62, 174–190. https://doi.org/10.1016/j.ympev.2011.09.016
  45. Morrow, C.C., Redmond, N.E., Picton, B.E., Thacker, R.W., Collins, A.G., Maggs, C.A., Sigwart, J.D. & Allcock, A.L. (2013) Molecular phylogenies support homoplasy of multiple morphological characters used in the taxonomy of Heteroscleromorpha (Porifera: Demospongiae). Integrative and Comparative Biology, 53, 428–446. https://doi.org/10.1093/icb/ict065
  46. Najafi, A., Moradinasab, M. & Nabipour, I. (2018) First record of microbiomes of sponges collected from the Persian Gulf, using tag pyrosequencing. Frontiers in Microbiology, 9, 1500. [https://www.frontiersin.org/articles/10.3389/fmicb.2018.01500]
  47. Nguyen, L.-T., Schmidt, H., von Haeseler, A. & Minh, B. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274. https://doi.org/10.1093/molbev/msu300
  48. Nichols, S. (2005) An evaluation of support for order-level monophyly and interrelationships within the class Demospongiae using partial data from the large subunit rDNA and cytochrome oxidase subunit I. Molecular Phylogenetics and Evolution, 34, 81–96. https://doi.org/10.1016/j.ympev.2004.08.019
  49. Núñez Pons, L., Calcinai, B. & Gates, R.D. (2017) Who’s there?—First morphological and DNA barcoding catalogue of the shallow Hawai’ian sponge fauna. PLoS ONE, 12, e0189357. https://doi.org/10.1371/journal.pone.0189357
  50. Olivi, G. (1792) Zoologia Adriatica, ossia catalogo ragionato degli animali del golfo e della lagune di Venezia. Bassano, Venice, 334 pp. https://doi.org/10.5962/bhl.title.60887
  51. Öztürk, E., Temiz, B. & Karahan, A. (2024) Species delimitation analysis indicates cryptic speciation for Terpios gelatinosus (Porifera, Demospongiae) from coastal regions of the northeastern Mediterranean Sea. bioRxiv, 2024.01.12.575186, 1–26. https://doi.org/10.1101/2024.01.12.575186
  52. Pankey, M.S., Plachetzki, D.C., Macartney, K.J., Gastaldi, M., Slattery, M., Gochfeld, D.J. & Lesser, M.P. (2022) Cophylogeny and convergence shape holobiont evolution in sponge-microbe symbioses. Nature Ecology and Evolution, 6, 750–762. https://doi.org/10.1038/s41559-022-01712-3
  53. Perovic-Ottstadt, S., Cetkovic, H., Gamulin, V., Schroder, H.C., Kropf, K., Moss, C., Korzhev, M., Diehl-Seifert, B., Muller, I.M. & Muller, W.E.G. (2004) Molecular markers for germ cell differentiation in the demosponge Suberites domuncula. The International Journal of Developmental Biology, 48, 293–305. https://doi.org/10.1387/ijdb.041813sp
  54. Pöppe, J., Sutcliffe, P., Hooper, J.N., Wörheide, G. & Erpenbeck, D. (2010) CO1 barcoding reveals new clades and radiation patterns of Indo-Pacific sponges of the family Irciniidae. PLoS ONE, 5, e9950. https://doi.org/10.1371/journal.pone.0009950
  55. Reiswig, H. (2018) Four new species of Hexactinellida (Porifera) and a name replacement from the NE Pacific. Zootaxa, 4466 (1), 124. https://doi.org/10.11646/zootaxa.4466.1.11
  56. Ridley, S.O. & Dendy, A. (1887) Report on the Monaxonida collected by H.M.S. “Challenger” during the years 1873–76. Report on the Scientific Results of the Voyage of H.M.S. Challenger during the years 1873–7, Zoology, 1887, 59.
  57. Ristau, D.A. (1978) Six new species of shallow-water marine demosponges from California. Proceedings of the Biological Society of Washington, 91, 569–589.
  58. Rot, C., Goldfarb, I., Ilan, M. & Huchon, D. (2006) Putative cross-kingdom horizontal gene transfer in sponge (Porifera) mitochondria. BMC Evolutionary Biology, 6, 1–11. https://doi.org/10.1186/1471-2148-6-71
  59. Samaai, T., Maduray, S., Janson, L., Gibbons, M.J., Ngwakum, B. & Teske, P.R. (2017) A new species of habitat-forming Suberites (Porifera, Demospongiae, Suberitida) in the Benguela upwelling region (South Africa). Zootaxa, 4254 (1), 49–81. https://doi.org/10.11646/zootaxa.4254.1.3
  60. Sim, C.J. & Bakus, G.J. (1986) Marine sponges of Santa Catalina Island, California. Occasional Papers of the Allan Hancock Foundation, 5, 1–23.
  61. van Soest, R.W.M. (2002) Family Suberitidae Schmidt, 1870. In: Hooper, J.N.A. & van Soest, R.W.M. (Eds.), Systema Porifera: A Guide to the Classification of Sponges. Springer, Boston, Massachusetts, pp. 227–244. https://doi.org/10.1007/978-1-4615-0747-5_25
  62. van Soest, R.W.M. & De Kluijver, M.J. (2003) Protosuberites denhartogi spec. nov., a new name for European “Prosuberites epiphytum” (Demospongiae, Hadromerida). Zoologische Verhandelingen Leiden, 345, 401–407.
  63. Solé-Cava, A., M. & Thorpe, J.P. (1986) Genetic differentiation between morphotypes of the marine sponge Suberites ficus. Marine Biology, 93, 247–253. https://doi.org/10.1007/BF00508262
  64. Thacker, R., Hill, A., Hill, M., Redmond, N., Collins, A., Morrow, C., Spicer, L., Carmack, C., Zappe, M., Pohlmann, D., Hall, C., Diaz, M. & Bangalore, P. (2013) Nearly complete 28S rRNA gene sequences confirm new hypotheses of sponge evolution. Integrative and Comparative Biology, 53, 373–387. https://doi.org/10.1093/icb/ict071
  65. Topsent, E. (1900) Étude monographique des Spongiaires de France. III.Monaxonida (Hadromerina). Archives de Zoologie expérimentale et générale, 3, 1–331.
  66. Trifinopoulos, J., Nguyen, L.-T., von Haeseler, A. & Minh, B. (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research, 44, W232–W235. https://doi.org/10.1093/nar/gkw256
  67. Turner, T.L. (2020) The order Tethyida (Porifera) in California: taxonomy, systematics, and the first member of the family Hemiasterellidae in the Eastern Pacific. Zootaxa, 4861 (2), 211–231. https://doi.org/10.11646/zootaxa.4861.2.3
  68. Turner, T.L. (2021) Four new Scopalina from Southern California: the first Scopalinida (Porifera: Demospongiae) from the temperate Eastern Pacific. Zootaxa, 4970 (2), 353–371. https://doi.org/10.11646/zootaxa.4970.2.8
  69. Turner, T.L. & Lonhart, S.I. (2023) The sponges of the Carmel pinnacles marine protected area. Zootaxa, 5230 (2), 151–194. https://doi.org/10.11646/zootaxa.5318.2.1
  70. Turner, T.L. & Pankey, M.S. (2023) The order Axinellida (Porifera: Demospongiae) in California. Zootaxa, 5230 (5), 501–539. https://doi.org/10.11646/zootaxa.5230.5.1
  71. Vargas, S., Kelly, M., Schnabel, K., Mills, S., Bowden, D. & Wörheide, G. (2015) Diversity in a cold hot-spot: DNA-barcoding reveals patterns of evolution among Antarctic Demosponges (Class Demospongiae, Phylum Porifera). PLoS ONE, 10, e0127573. https://doi.org/10.1371/journal.pone.0127573
  72. Vargas, S., Schuster, A., Sacher, K., Büttner, G., Schätzle, S., Läuchli, B., Hall, K., Hooper, J.N.A., Erpenbeck, D. & Wörheide, G. (2012) Barcoding sponges: An overview based on comprehensive sampling. PLoS ONE, 7, e39345. https://doi.org/10.1371/journal.pone.0039345
  73. Vicente, J., Webb, M.K., Paulay, G., Rakchai, W., Timmers, M.A., Jury, C.P., Bahr, K. & Toonen, R.J. (2022) Unveiling hidden sponge biodiversity within the Hawaiian reef cryptofauna. Coral Reefs, 41, 727–742. https://doi.org/10.1007/s00338-021-02109-7