Reconstructing early sponge relationships by using the Burgess Shale fossil Eiffelia globosa, Walcott - PubMed (original) (raw)
Reconstructing early sponge relationships by using the Burgess Shale fossil Eiffelia globosa, Walcott
Joseph P Botting et al. Proc Natl Acad Sci U S A. 2005.
Abstract
The relationships of the sponge classes are controversial, particularly between the calcareous and siliceous sponges. Specimens of the putative calcarean Eiffelia globosa Walcott from the Burgess Shale show the presence of diagnostic hexactinellid spicules integrated into the skeletal mesh. The arrangement of these spicules in Eiffelia is shown to be precisely equivalent to that of early protospongioid hexactinellids, and sponge growth occurred through an identical pattern to produce identical skeletal body morphology. The difference in spicule composition of the classes is interpreted through the observation of taphonomic features of Eiffelia that suggest the presence of at least two mineralogically distinct layers within the spicules. These results support molecular analyses that identify the calcarean-silicisponge transition as the earliest major sponge branch and suggest that the heteractinids were paraphyletic with respect to the Hexactinellida.
Figures
Fig. 1.
Morphology of Eiffelia globosa (ROM 57023). (A) Whole specimen. (B-G) Details of A, showing tetraradiate spicules. Note the quadruled arrangement of tetraradiates in E and F, and evidence of a central vertical ray in C and G.(H) Spicule showing evidence of bilayered construction. (Scale bar: A, 3 mm; F, 0.50 mm; D, 0.45 mm; B, E, and G, 0.35 mm; C and H, 0.20 mm.)
Fig. 2.
Morphology of Eiffelia globosa (ROM 57022). (A) Bedding-plane view, reflective patches are fragments of HF-resistant carbonaceous film. Note the slight color/textural difference between the shale matrix and spicules where the film has peeled away (both aluminosilicate). The poorly defined material interspersed between the spicules is also HF-resistant. (B) Detail of spicule ray showing bilayered structure and fragments of carbonaceous film. (C) Perpendicular-to-bedding thin section through spicule ray showing divergence of the carbonaceous film in the cortical layer.
Fig. 3.
Camera lucida drawings from the type material of Eiffelia globosa showing tetraradiate spicules. (A) USNM 200648. (B) USNM 200653. (C and D) USNM 200638. Tetraradiate spicules are shaded in A-D.(E) USNM 200656. (F) Artificial construction obtained by tracing of E with all remaining hexaradiates replaced by tetraradiates, revealing an irregular quadruling habit (see Discussion). (G) Illustration of perfect quadruling as seen in Protospongia. (Scale bar: A, 1 mm; B-F, 2 mm.)
Fig. 4.
Proposed phylogenetic relationships of extant sponge classes, Eumetazoa, and Eiffelia globosa. Eiffelia is shown as a stem hexactinellid (Silicispongea) and a derived member of the “Heteractinida” (stem Calcarea). Eiffelia and early hexactinellids share tetraradial hexactines and a quadruled spicule geometry, but the spicules of the latter are entirely siliceous.
Fig. 5.
Proposed transition from magnesium calcite (Calcarea) to opal (Silicospongea) spicules based on the bilayered structure exhibited by Eiffelia. (A) Calcarean spicule with outer sheath of collagen fibrils. (B) Secondary precipitation of opal onto the collagenous sheath (as represented by Eiffelia).(C) Further increase in opal precipitation, accompanied by reduction of the calcaean sheath to an axial filament and loss of hexaradial symmetry. Mg-Ca, magnesium calcite; ACC, amorphous calcium carbonate; CFS, collagen fibril sheath; Op, opal; Sl/Um, silicalemma/unit membrane or second collagen fibril sheath.
Similar articles
- Carbonaceous preservation of Cambrian hexactinellid sponge spicules.
Harvey TH. Harvey TH. Biol Lett. 2010 Dec 23;6(6):834-7. doi: 10.1098/rsbl.2010.0377. Epub 2010 Jun 16. Biol Lett. 2010. PMID: 20554559 Free PMC article. - Discovery of missing link between demosponges and hexactinellids confirms palaeontological model of sponge evolution.
Botting JP, Zhang Y, Muir LA. Botting JP, et al. Sci Rep. 2017 Jul 13;7(1):5286. doi: 10.1038/s41598-017-05604-6. Sci Rep. 2017. PMID: 28706211 Free PMC article. - Giving the early fossil record of sponges a squeeze.
Antcliffe JB, Callow RH, Brasier MD. Antcliffe JB, et al. Biol Rev Camb Philos Soc. 2014 Nov;89(4):972-1004. doi: 10.1111/brv.12090. Epub 2014 Apr 29. Biol Rev Camb Philos Soc. 2014. PMID: 24779547 - Siliceous spicules and skeleton frameworks in sponges: origin, diversity, ultrastructural patterns, and biological functions.
Uriz MJ, Turon X, Becerro MA, Agell G. Uriz MJ, et al. Microsc Res Tech. 2003 Nov 1;62(4):279-99. doi: 10.1002/jemt.10395. Microsc Res Tech. 2003. PMID: 14534903 Review. - Deep phylogeny and evolution of sponges (phylum Porifera).
Wörheide G, Dohrmann M, Erpenbeck D, Larroux C, Maldonado M, Voigt O, Borchiellini C, Lavrov DV. Wörheide G, et al. Adv Mar Biol. 2012;61:1-78. doi: 10.1016/B978-0-12-387787-1.00007-6. Adv Mar Biol. 2012. PMID: 22560777 Review.
Cited by
- Deep resilience: An evolutionary perspective on calcification in an age of ocean acidification.
Gold DA, Vermeij GJ. Gold DA, et al. Front Physiol. 2023 Feb 3;14:1092321. doi: 10.3389/fphys.2023.1092321. eCollection 2023. Front Physiol. 2023. PMID: 36818444 Free PMC article. - Seventeen new complete mtDNA sequences reveal extensive mitochondrial genome evolution within the Demospongiae.
Wang X, Lavrov DV. Wang X, et al. PLoS One. 2008 Jul 16;3(7):e2723. doi: 10.1371/journal.pone.0002723. PLoS One. 2008. PMID: 18628961 Free PMC article. - The earliest fossil record of the animals and its significance.
Budd GE. Budd GE. Philos Trans R Soc Lond B Biol Sci. 2008 Apr 27;363(1496):1425-34. doi: 10.1098/rstb.2007.2232. Philos Trans R Soc Lond B Biol Sci. 2008. PMID: 18192192 Free PMC article. Review. - Three-dimensionally preserved soft tissues and calcareous hexactins in a Silurian sponge: implications for early sponge evolution.
Nadhira A, Sutton MD, Botting JP, Muir LA, Gueriau P, King A, Briggs DEG, Siveter DJ, Siveter DJ. Nadhira A, et al. R Soc Open Sci. 2019 Jul 31;6(7):190911. doi: 10.1098/rsos.190911. eCollection 2019 Jul. R Soc Open Sci. 2019. PMID: 31417767 Free PMC article. - Naked chancelloriids from the lower Cambrian of China show evidence for sponge-type growth.
Cong PY, Harvey THP, Williams M, Siveter DJ, Siveter DJ, Gabbott SE, Li YJ, Wei F, Hou XG. Cong PY, et al. Proc Biol Sci. 2018 Jun 27;285(1881):20180296. doi: 10.1098/rspb.2018.0296. Proc Biol Sci. 2018. PMID: 29925613 Free PMC article.
References
- Brasier, M. D., Green, O. & Shields, G. (1997) Geology 25, 303-306.
- Gehling, J. G. & Rigby, J. K. (1996) J. Paleontol. 70, 185-195.
- Debrenne, F. & Reitner, J. (2001) in The Ecology of the Cambrian Radiation, eds. Zhuravlev, A. Y. & Riding, R. (Columbia Univ. Press, New York), pp. 301-325.
- Zrzavy, J., Mihulka, S., Kepka, P., Bezdek, A. & Tietz, D. (1998) Cladistics 14, 149-185. - PubMed
- Adams, C. L., McInerney, J. O. & Kelly, M. (1999) Mem. Queensl. Mus. 44, 33-43.
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources