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Ediacaran Sponges, Animal Biomineralization, and Skeletal Reefs COMMENTARY Shuhai Xiaoa,1

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Ediacaran Sponges, Animal Biomineralization, and Skeletal Reefs COMMENTARY Shuhai Xiaoa,1 COMMENTARY Ediacaran sponges, animal biomineralization, and skeletal reefs COMMENTARY Shuhai Xiaoa,1 With an estimated 15,000 living species (1), the animal AB phylum Porifera (colloquially known as sponges) is not a biodiversity heavyweight as are arthropods, mol- lusks, and chordates. Unassuming in character, sponges barely move in their adult lifetime of up to several thousand years, and they passively strain food particles from water currents that they generate con- tinuously around the clock. They would be one of the most boring pets to have. However, sponges contrib- ute to the global ecosystem and to our knowledge CD about animal evolution in their own ways. Because Other Crown-group sponges Other Crown-group sponges sponges diverged near the base of the animal family metazoans metazoans Age (Ma) Age tree (2), they hold a special place in understanding 500 520 early animal evolution. Because sponges were among Cambrian the first animals to build mineralized skeletons 540 bilaterian fossils 560 Stem-group through biologically controlled processes (3), they pro- sponge vide key insights into the origins of animal biomineral- 580 600 ization. Also, because many sponges are important reef Ediacaran Aspiculate sponges or non-biomineralizing animals constructors, they play an essential role in modern reef 620 640 Spiculate sponges or ecosystems and may take over the reins from corals as demosponge biomarkers biomineralizing animals Stem-group sponge Stem-group global warming exacerbates (4). Thus, when and how 660 680 Cryogenian sponges evolved, acquired biomineralization, and molecular clocks 700 started contributing to reef construction become crit- ical questions in the early evolution of animals, biomi- Fig. 1. N. rietoogensis (A and B) and sponge evolution (C and D). (A) Outcrop photo. (B) Reflected light photo of polished specimen. (A and B) Republished with neralization, and reefs. In this context, the ca. 550-My- permission of the Royal Society, from ref. 6; permission conveyed through old fossil Namapoikia rietoogensis (Fig. 1 A and B), orig- Copyright Clearance Center, Inc. (C and D) Two alternative scenarios of sponge inally reported by Wood et al. (5) from carbonate rocks of evolution. Molecular clocks marked on the lower left refer to estimated the Omkyk Member in southern Namibia, has been fea- divergence times of the four living sponge classes (12). See text for details. tured prominently because it is considered one of the oldest sponges that built biologically controlled aragonitic Why does it matter whether N. rietoogensis is a skeletons and contributed to the construction of the sponge? We need to understand early sponge evolu- oldest animal reefs (6). Writing in PNAS, however, Mehra tion in order to understand early animal evolution, be- et al. (7) question the sponge interpretation of N. rietoo- cause sponges are either a paraphyletic group at the gensis. Instead, they interpret N. rietoogensis as a micro- base of the animal tree (9) or a monophyletic clade bial construction analogous to stromatolites and constituting a sister group of all other animals (2). Mo- thrombolites, which are microbial buildups particularly lecular fossils or biomarkers indicate that one of the common in Precambrian and early Paleozoic carbon- modern sponge classes, the demosponges, diverged ates (8). The implications are that N. rietoogensis did no later than ca. 650 Ma in the Cryogenian Period (ref. not build its calcareous structures in a biologically con- 10, but see ref. 11). Molecular clock estimates, including trolled fashion as do modern sponges, and it may have those independent of the aforementioned biomarkers as lacked the structural integrity to support reef growth (7). calibrations, place the divergence of sponge classes at aDepartment of Geosciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061 Author contributions: S.X. designed research, performed research, contributed new reagents/analytic tools, analyzed data, and wrote the paper. The author declares no competing interest. Published under the PNAS license. See companion article, “Three-dimensional reconstructions of the putative metazoan Namapoikia show that it was a microbial construction,” 10.1073/pnas.2009129117. 1Email: [email protected]. First published August 12, 2020. www.pnas.org/cgi/doi/10.1073/pnas.2014393117 PNAS | September 1, 2020 | vol. 117 | no. 35 | 20997–20999 Downloaded by guest on September 28, 2021 700 to 800 Ma in the Tonian and Cryogenian Periods (12). The abun- the Ediacaran Period, but their sponge affinity has been disputed dant evidence of Ediacaran eumetazoans and even bilaterian animals (15, 21). Certainly, none of the purported Ediacaran sponges (e.g., refs. 13 and 14), which diverged after the sponges, also dictates have unambiguous spicules (21, 22), in sharp contrast to Cam- the presence of at least total-group sponges in the Ediacaran Period brian sponges that are mostly identified on the basis of their bio- or earlier. However, the first unequivocal sponge fossils do not ap- mineralized spicules. In one scenario, assuming sponge spicules pear until in the Cambrian Period, with disarticulated sponge spicules have a single origin and a good preservation potential (21), the around ca. 535 Ma (15) and fully articulated sponge bodies shortly last common ancestor of extant sponges must have had spicules, after (16). Thus, there is a prominent gap in the sponge fossil record, and the lack of Precambrian spicules means the divergence of and any bona fide sponge fossils from the Ediacaran Period (635 to crown-group sponges at the Ediacaran–Cambrian boundary 539 Ma) would help to fill this gap. (21); hence, any Precambrian sponges must be stem lineages According to Wood et al. (5), N. rietoogensis (Fig. 1 A and B)is and aspiculate (Fig. 1C). Alternatively, considering the docu- an Ediacaran sponge that encrusted fissure walls in microbial– mented cases of multiple origins of biomineralization in animals metazoan reefs constructed by thrombolites and Cloudina (ref. (3) and the possibility of independent evolution of spicules 17, but see ref. 18), the latter of which is also regarded as a bio- among sponge classes (23), it is conceivable that modern mineralizing animal (ref. 19, but see ref. 20). It consists of irregu- sponge classes may have diverged in the Precambrian but in- larly tessellated tubules that are separated by poorly defined dependently evolved biomineralized spicules at the Ediacaran– partitioning walls. Thus, it looks like palisades in longitudinal sec- Cambrian boundary (24) (Fig. 1D). Both scenarios are consistent tion but appears spongy and labyrinthine in transverse section with the absence of Precambrian spicules, but the latter sce- (Fig. 1B). It also has structures interpreted as tabulae and dissep- nario is also consistent with the molecular clocks and bio- iments, features that are present in some demosponges (1). Over- markers and predicts the existence of aspiculate crown-group all, N. rietoogensis shares some morphological similarities with sponges in the Ediacaran Period. In this context, it is worth extant demosponges such as Vaceletia cryptica and as Acantho- noting Muscente et al.’s (22) report of Ediacaran organic fila- chaetetes wellsi, and it is phylogenetically placed within the total ments with a rectangular prismatic shape that are interpreted as group Porifera (6). possible precursors of axial filaments later recruited to template spicule formation, as well as Tang et al.’s (24) documentation Mehra et al. question the sponge interpretation that early Cambrian hexactine sponge spicules are only weakly of N. rietoogensis. Instead, they interpret N. biomineralized, with a large axial filament but proportionally rietoogensis as a microbial construction analogous less biomineral when compared with younger sponge spicules. These new data lend some support to the hypothesis that to stromatolites and thrombolites, which are sponge classes diverged in the Precambrian but independently microbial buildups particularly common in evolved spiculogenesis in the Cambrian. This hypothesis im- Precambrian and early Paleozoic carbonates. plies that the search for Precambrian sponges should be shifted away from the search for spicules (24), and further adds to the Mehra et al.’s (7) objection to a sponge interpretation for N. remarkable number of animal lineages that independently ac- rietoogensis is based on three-dimensional morphological recon- quired biomineralization in the early Cambrian (3). structions of two specimens using a serial grinding technique. It should be pointed out that whether N. rietoogensis is a sponge, They found that the tubules and partitions of N. rietoogensis are whether it had biomineralized skeletons, and whether it contributed much larger and morphologically more variable than correspond- to reef construction are three separate questions. Even if N. rietoo- ing features in extant and extinct demosponges. Mehra et al. (7) gensis is not a sponge, it seems to have constructed biomineralized did not observe tabulae and dissepiments in the two specimens skeletons with some regularity and it may have used an organic they analyzed, and they argue that N. rietoogensis lacks sponge template for biomineralization (6). Regardless of the degree of bio- synapomorphies (or characters uniquely evolved in sponges) such logical control in mineralization, N. rietoogensis was definitely part of as ostia and oscula, although this could be related to the small the Ediacaran reef
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