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Phylogeny and Evolution of Glass Sponges (Porifera, Hexactinellida)
Abstract
Reconstructing the phylogeny of sponges (Porifera) is one of the remaining challenges to resolve the metazoan Tree of Life and is a prerequisite for understanding early animal evolution. Molecular phylogenetic analyses for two of the three extant classes of the phylum, Demospongiae and Calcarea, are largely incongruent with traditional classifications, most likely because of a paucity of informative morphological characters and high levels of homoplasy. For the third class, Hexactinellida (glass sponges)--predominantly deep-sea inhabitants with unusual morphology and biology--we present the first molecular phylogeny, along with a cladistic analysis of morphological characters. We collected 18S, 28S, and mitochondrial 16S ribosomal DNA sequences of 34 glass sponge species from 27 genera, 9 families, and 3 orders and conducted partitioned Bayesian analyses using RNA secondary structure-specific substitution models (paired-sites models) for stem regions. Bayes factor comparisons of different paired-sites models against each other and conventional (independent-sites) models revealed a significantly better fit of the former but, contrary to previous predictions, the least parameter-rich of the tested paired-sites models provided the best fit to our data. In contrast to Demospongiae and Calcarea, our rDNA phylogeny agrees well with the traditional classification and a previously proposed phylogenetic system, which we ascribe to a more informative morphology in Hexactinellida. We find high support for a close relationship of glass sponges and Demospongiae sensu stricto, though the latter may be paraphyletic with respect to Hexactinellida. Homoscleromorpha appears to be the sister group of Calcarea. Contrary to most previous findings from rDNA, we recover Porifera as monophyletic, although support for this clade is low under paired-sites models.
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“Inferred relationships among major sponge lineages (i.e., Demospongiae + Hexactinellida sister to Calcarea + Homoscleromorpha) were consistent with morphology (27,28) and most other molecular analyses that have recovered monophyletic sponges (datasets 1-27 in Figs. 2 and 3 and Figs.S1-S5) (4, 5, 8, 9, 28-30).”
From Error, signal, and the placement of Ctenophora sister to all other animals (2015) · cites this paper as [29]
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Tsagkogeorga, G., Turón, X., Hopcroft, R. R., Tilak, M., Feldstein, T., Shenkar, N., Loya, Y., Huchon, D., Douzery, E., & Delsuc, F. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-187 · Cited by 168
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Self-citationDeep Phylogeny and Evolution of Sponges (Phylum Porifera)
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ResultSelf-citationEarly sponge evolution: A review and phylogenetic framework
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“Cladistics is one of the main methods of phylogenetic reconstruction used in biology (e.g. Mallegni, 2007; Cap et al., 2008; Christiansen, 2008; Dohrmann et al., 2008; O'Leary and Gatesy, 2008; Smith and Grine, 2008; Wills et al., 2008) and has become used in a number of other disciplines in which phylogenetic relatio…”
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“for 18S and 28S, a denaturation step at 95 ◦C for 2 min, [35 cycles denaturation step at 95 ◦C for 1 min, annealing step at 52 ◦C (18S1/18S2; [48]), 55 ◦C (18S-AF/18S-BR, NL4F/NL4R; [49,50]), 57 ◦C (C2/D2; [51]), for 1 min and 72 ◦C of primer extension for 2 min], a final extension step at 72 ◦C for 10 min; ii.”
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A Metataxonomic Approach Reveals Diversified Bacterial Communities in Antarctic Sponges
Ruocco, N., Esposito, R., Bertolino, M., Zazo, G., Sonnessa, M., Andreani, F., Coppola, D., Giordano, D., Nuzzo, G., Lauritano, C., et al. (2021) · Marine Drugs · doi:10.3390/md19030173 · Cited by 22
“PCR reactions were performed on the C1000 Touch Thermal Cycler (BioRad) in a 30 µL reaction mixture final volume including about 50–100 ng of genomic DNA, 6 µL of 5X Buffer GL (GeneSpin Srl, Milan, Italy), 3 µL of dNTPs (2 mM each), 2 µL of each forward and reverse primer (25 pmol/µL, Table 1), 0.2 µL of Xtra Taq Poly…”
MethodInfluentialDohrmann, M., Göcke, C., Reed, J. K., & Janussen, D. (2012) · Zootaxa · doi:10.11646/zootaxa.3383.1.1 · Cited by 21
“2012), sponges of the class Hexactinellida have a higher number of informative morphological characters, especially spicule types and their combinations, and consequently there is a better correspondence between molecular-based phylogenetic hypotheses and traditional taxonomy of this group (Dohrmann et al. 2008).”
InfluentialSelf-citationReitner, J., Luo, C., Suárez-González, P., & Duda, J. (2021) · Geological Magazine · doi:10.1017/s001675682100087x · Cited by 20
“For this reason, we integrate findings from the most recent phylogenetic models (e.g. Erpenbeck & Wörheide 2007; Dohrmann et al. 2008; Wörheide et al. 2012; Redmond et al. 2013) into the taxonomic frame of Hooper & van Soest (2002).”
Carrera, M. G., & Maletz, J. (2014) · Journal of Systematic Palaeontology · doi:10.1080/14772019.2013.846946 · Cited by 19
“Sceptrules are a constituent characteristic of the Sceptrulophora (see Dohrmann et al. 2008, 2011), Hexasterophora. In sceptrules, the axial cross of the central axial canal is located within the inflated or expanded terminal end (see Mehl 1998). These spicules can be considered as true monactins. In the case of amphi…”
BackgroundLuo, C., & Joachim Reitner, A. (2019) · Paläontologische Zeitschrift · doi:10.1007/s12542-018-00441-y · Cited by 18
Brown, R., Davis, C. S., & Leys, S. P. (2016) · Molecular Ecology · doi:10.1111/mec.13982 · Cited by 17
“The phylogeny of the family Aphrocallistidae is uncertain; recent molecular analyses have © 2016 John Wiley & Sons Ltd placed H. calyx and A. vastus as sister species with a recent divergence (Dohrmann et al. 2008, 2011) consistent with the above date.”
Microbial diversity in Mediterranean sponges as revealed by metataxonomic analysis
Ruocco, N., Esposito, R., Zagami, G., Bertolino, M., Matteo, S. D., Sonnessa, M., Andreani, F., Crispi, S., Zupo, V., & Costantini, M. (2021) · Scientific Reports · doi:10.1038/s41598-021-00713-9 · Cited by 16
Reiswig, H. M., & Dohrmann, M. (2014) · Zoological Journal of the Linnean Society · doi:10.1111/zoj.12138 · Cited by 16
“…from the holotypes of Conorete pourtalesi sp. nov., Verrucocoeloidea liberatorii sp. nov., and a specimen of Lefroyella decora (HBOI 11-VII-10-1-1; collected on 11 July 2010 at Pourtales Terrace, FL, USA) were amplified using established protocols and primers (Dohrmann et al., 2008, 2009, 2012).”
MethodSelf-citationNew hexactinellid sponges from deep Mediterranean canyons
Boury‐Esnault, N., Vacelet, J., Dubois, M., Goujard, A., Fourt, M., Pérez, T., & Chevaldonné, P. (2017) · Zootaxa · doi:10.11646/zootaxa.4236.1.6 · Cited by 16
Improvement of molecular phylogenetic inference and the phylogeny of Bilateria
Lartillot, N., & Philippe, H. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0012 · Cited by 15
Vargas, S., Dohrmann, M., Göcke, C., Janussen, D., & Wörheide, G. (2017) · Polar Biology · doi:10.1007/s00300-017-2155-7 · Cited by 14
“3.1 Total evidence phylogenetic analysis We recovered a phylogenetic tree congruent with published analyses of the class Hexactinellida (Dohrmann et al., 2008, 2009, 2012a,b).”
BackgroundMethodInfluentialSelf-citationKersken, D., Kocot, K. M., Janussen, D., Schell, T., Pfenninger, M., & Arbizu, P. M. (2018) · Hydrobiologia · doi:10.1007/s10750-017-3498-3 · Cited by 14
“…Hyalonematidae, previously sequenced individuals of Hyalonema are distantly related to individuals sequenced within this study because they were sampled in the northwestern Atlantic (Dohrmann et al., 2008, 2009), while all Hyalonematidae of this study were sampled in the northeastern Pacific.”
BackgroundMethodResultInfluentialSelf-citationMacrofauna abundance and diversity patterns of deep sea southwestern Gulf of Mexico
Quintanar-Retama, O., Vázquez-Bader, A. R., & Gracía, A. (2023) · Frontiers in Marine Science · doi:10.3389/fmars.2022.1033596 · Cited by 13
“Frontiers in Marine Science 14 of the class Hexactinellida are a well-represented and wide distributed taxon in the deep sea (Dohrmann et al., 2008).”
BackgroundDohrmann, M., Reiswig, H. M., Kelly, M., Mills, S., Schätzle, S., Reverter, M., Niesse, N., Rohde, S., Schupp, P. J., & Wörheide, G. (2023) · PeerJ · doi:10.7717/peerj.15017 · Cited by 13
Self-citationTwo new species of Hexactinellida (Porifera) from the South China Sea
Gong, L., Li, X., & Qiu, J. (2015) · Zootaxa · doi:10.11646/zootaxa.4034.1.9 · Cited by 13
Biomineralization in Marine Organisms
Gebeshuber, I. (2015) · Springer eBooks · doi:10.1007/978-3-642-53971-8_58 · Cited by 8
Tabachnick, K. R., & Menshenina, L. L. (2013) · Marine Biology Research · doi:10.1080/17451000.2012.749996 · Cited by 12
“…spinosus Schulze, 1886: 50; 1887: 153; 1897: 534; Ijima 1898: 48; Topsent 1901: 36; Koltun 1976: 165; Barthel & Tendal 1994: 109 (B. levis is mentioned as a lower synonym); Hooper & Wiedenmayer 1994: 525; Janussen et al. 2004: 1867; Dohrmann et al. 2008: 391; Janussen & Reiswig 2009: 15.”
Leys, S. P., Zaman, A. K., & Boury‐Esnault, N. (2016) · Invertebrate Biology · doi:10.1111/ivb.12142 · Cited by 12
Kise, H., Montenegro, J., Santos, M. E. A., Hoeksema, B. W., Ekins, M., Ise, Y., Higashiji, T., Fernández-Silva, I., & Reimer, J. D. (2021) · Zoological Journal of the Linnean Society · doi:10.1093/zoolinnean/zlab068 · Cited by 12
Deciphering deuterostome phylogeny: molecular, morphological, and palaeontological perspectives
Smith, A. B., & Swalla, B. J. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0009 · Cited by 13
The evolution of nervous system centralization
Arendt, D., Denes, A. S., Jékely, G., & Tessmar‐Raible, K. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0007 · Cited by 12
Quintanar-Retama, O., Armenteros, M., & Gracía, A. (2022) · Deep Sea Research Part I Oceanographic Research Papers · doi:10.1016/j.dsr.2022.103699 · Cited by 11
Peterson, K. J., Cotton, J. A., Gehlîng, J. G., & Pisani, D. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0002 · Cited by 12
A new Silurian (Llandovery, Telychian) sponge assemblage from Gotland, Sweden
Rhebergen, F., & Botting, J. P. (2014) · Fossils and strata · doi:10.1002/9781118906651.ch1 · Cited by 11
Progress in glass sponge phylogenetics: a comment on Kersken et al. (2018)
Dohrmann, M. (2018) · Hydrobiologia · doi:10.1007/s10750-018-3708-7 · Cited by 11
Self-citationKou, Q., Gong, L., & Li, X. (2018) · Deep Sea Research Part I Oceanographic Research Papers · doi:10.1016/j.dsr.2018.03.006 · Cited by 10
No longer Demospongiae: Homoscleromorpha formal nomination as a fourth class of Porifera
Gazave, E., Lapébie, P., Ereskovsky, A. V., Vacelet, J., Renard, E., Cárdenas, P., & Borchiellini, C. (2011) · Springer eBooks · doi:10.1007/978-94-007-4688-6_2 · Cited by 10
Martins, E., Rocha, M. S., Silva, T. H., & Reis, R. L. (2019) · Springer series in biomaterials science and engineering · doi:10.1007/978-981-13-8855-2_2 · Cited by 9
First certain record of Demospongiae class (Porifera) alien species from the Mediterranean Sea
Bertolino, M., Costa, G., Ruocco, N., Esposito, R., Matteo, S. D., Zagami, G., & Costantini, M. (2022) · Marine Genomics · doi:10.1016/j.margen.2022.100951 · Cited by 10
Invertebrate Problematica: kinds, causes, and solutions
Jenner, R. A., Timothy, D. J., & Littlewood, D. T. J. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0011 · Cited by 7
Reiswig, H. M., Dohrmann, M., Pomponi, S. A., & Wörheide, G. (2008) · Zootaxa · doi:10.11646/zootaxa.1721.1.4 · Cited by 8
Self-citationReiswig, H. M. (2010) · Proceedings of the Biological Society of Washington · doi:10.2988/10-02.1 · Cited by 7
Shen, C., Cheng, H., Zhang, D., Lu, B., & Wang, C. (2021) · Acta Oceanologica Sinica · doi:10.1007/s13131-021-1939-3 · Cited by 7
Reiswig, H. M., Dohrmann, M., Kelly, M., Mills, S., Schupp, P. J., & Wörheide, G. (2021) · ZooKeys · doi:10.3897/zookeys.1060.63307 · Cited by 6
“…together with a much larger collection, the remainder of which will be reported on elsewhere, were first subjected to a molecular phylogenetic study (results not shown) based on a mitochondrial 16S ribosomal DNA fragment (cf. Dohrmann et al. 2008) for initial assessment of their relationships.”
BackgroundSelf-citationHayami, Y., Ambalavanan, L., Zainathan, S. C., Danish‐Daniel, M., Emilia, S. N., & Iehata, S. (2023) · Regional Studies in Marine Science · doi:10.1016/j.rsma.2023.102967 · Cited by 6
A new species of Lophophysema (Porifera, Hexactinellida, Hyalonematidae) from the South China Sea
Gong, L., Li, X., & Qiu, J. (2014) · Zootaxa · doi:10.11646/zootaxa.3884.6.3 · Cited by 6
“However, the phylogenetic relationships between Lophophysema and the 4 other genera of Hyalonematidae remain unexplored due to absence of comparable sequence data from any but three Hyalonema species so far (Dohrmann et al 2008, 2009).”
Background(2009) · doi:10.1093/acprof:oso/9780199549429.001.0001 · Cited by 7
The earliest fossil record of the animals and its significance
Budd, G. E. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0001 · Cited by 6
Yun, H., Janussen, D., Zhang, X., & Joachim Reitner, A. (2023) · Lethaia · doi:10.18261/let.56.3.5 · Cited by 5
Self-citationStratmann, T., Busch, K., de Kluijver, A., Kelly, M., Mills, S., Rossel, S., & Schupp, P. J. (2024) · Deep Sea Research Part I Oceanographic Research Papers · doi:10.1016/j.dsr.2024.104416 · Cited by 5
Shen, C., Cheng, H., Zhang, D., & Wang, C. (2022) · Frontiers in Marine Science · doi:10.3389/fmars.2022.852498 · Cited by 4
Peel, A. (2009) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199549429.003.0016 · Cited by 4
Botting, J. P., Janussen, D., Dohrmann, M., Muir, L. A., Zhang, Y., & Ma, J. (2025) · Papers in Palaeontology · doi:10.1002/spp2.70000 · Cited by 4
Self-citation
Metadata
- Authors
- Dohrmann, M., Janussen, D., Reitner, J., Collins, A. G., & Wörheide, G.
- Affiliations
- University of Göttingen (DE)
- Senckenberg Research Institute and Natural History Museum Frankfurt/M (DE)
- Georg-August-Universität Göttingen Geowissenschaftliches Zentrum Göttingen (GZG), Abteilung Geobiologie, Goldschmidtstrasse 3, 37077 Göttingen, Germany; E-mail: gert.woerheide@geo.uni-goettingen.de (G.W.)
- Smithsonian Institution (US)
- Corresponding author
- Wörheide, Gert
- Venue
- Systematic Biology
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-06-01
- Volume
- 57
- Issue
- 3
- Pages
- 388-405
- ISSN
- 1063-5157 (ISSN-L)
- 1076-836X
- OpenAlex
- W2163478051
- Semantic Scholar
- 6d8dcf741eb7fa9e5bb5f037f2b557ca8a8b1a00
- Cited by
- 143
- References
- 125
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 2 · 2023: 6 · 2022: 4 · 2021: 10 · 2019: 3 · 2018: 6 · 2017: 5 · 2016: 3 · 2015: 8 · 2014: 9 · 2013: 11 · 2012: 7
- FWCI
- 15.22
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Systematic Biology (publishedVersion)
- PubMed (publishedVersion)
- Smithsonian Digital Repository (Smithsonian Institution) (submittedVersion)
- Funders
- Society of Systematic Biologists
- Boehringer Ingelheim Fonds
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Marine Sponges and Natural Products
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
- Keywords
- Hexactinellida, sponge phylogeny, early animal evolution, Demospongiae, calcareous sponges, Homoscleromorpha, rDNA phylogeny, ribosomal RNA secondary structure, deep-sea sponges, homoplasy
- MeSH terms
- Animals, Base Sequence, Bayes Theorem, DNA, Ribosomal, Biological Evolution, Microscopy, Electron, Scanning, Models, Genetic, Phylogeny, Porifera, Sequence Alignment, Sequence Analysis, DNA, Sequence Analysis, RNA
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