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Science Journals SCIENCE ADVANCES | RESEARCH ARTICLE PALEONTOLOGY 2016 © The Authors, some rights reserved; Photosymbiosis and the expansion of exclusive licensee American Association shallow-water corals for the Advancement of Science. Distributed 1 2 2 3 under a Creative Katarzyna Frankowiak, Xingchen T. Wang, Daniel M. Sigman, Anne M. Gothmann, Commons Attribution 4 5 6 1 Marcelo V. Kitahara, Maciej Mazur, Anders Meibom, Jarosław Stolarski * NonCommercial License 4.0 (CC BY-NC). Roughly 240 million years ago (Ma), scleractinian corals rapidly expanded and diversified across shallow marine environments. The main driver behind this evolution is uncertain, but the ecological success of modern reef- building corals is attributed to their nutritional symbiosis with photosynthesizing dinoflagellate algae. We show that a suite of exceptionally preserved Late Triassic (ca. 212 Ma) coral skeletons from Antalya (Turkey) have microstructures, carbonate 13C/12C and 18O/16O, and intracrystalline skeletal organic matter 15N/14N all indicat- ing symbiosis. This includes species with growth forms conventionally considered asymbiotic. The nitrogen iso- Downloaded from topes further suggest that their Tethys Sea habitat was a nutrient-poor, low-productivity marine environment in which photosymbiosis would be highly advantageous. Thus, coral-dinoflagellate symbiosis was likely a key driver in the evolution and expansion of shallow-water scleractinians. INTRODUCTION their application requires exceptional preservation of primary skeleton. Symbiosis between scleractinian corals and endocellular dinoflagellate This is rare in the fossil record because the aragonite polymorph is un- algae (known as zooxanthellae) is key to the success of modern reefs stable under ambient conditions and recrystallizes to calcite, with asso- http://advances.sciencemag.org/ in oligotrophic (sub)tropical waters. The coral host benefits from this ciated modifications of original skeletal composition. association through the translocation of photosynthates and an Recently, two key method developments have created new oppor- increased capability to recycle metabolic waste products, such as am- tunities for the investigation of photosymbiosis among fossil corals. monium (1, 2). The physiological mechanisms and the molecular First, microscale skeletal growth bands have been shown to provide background underlying this partnership have been extensively studied a robust diagnostic signature of photosymbiosis in scleractinian corals (2–5). Nevertheless, fundamental questions regarding the coevolution (12). Modern symbiotic corals have, almost without exception, highly of photosynthesizing algae and coralsremain,forexample,withregard regular microscale growth bands, whereas these growth bands in to the role of photosymbiosis during the sudden Triassic expansion asymbiotic corals are irregular and often discontinuous. This dif- of coral reefs (6). Molecular phylogeny indicates that existing clades ference can be quantified with the coefficient of variation (CV) of band- of endosymbiotic dinoflagellates originated in the Early Paleogene widths and thus used as an indicator of photosymbiosis. Skeletons of [that is, only about 60 million years ago (Ma)] (7), and fossil coral modern asymbiotic corals are characterized by CVs >40% (Fig. 1B) versus skeletons do not preserve direct evidence of the presence of these <20% in symbiotic corals. Second, a new “persulfate-denitrifier” method symbionts. Through comparison with modern corals, indirect crite- makes high-precision analysis of nitrogen (N) isotopic compositions of on November 2, 2016 ria, such as macromorphology and isotope geochemistry, have been intracrystalline OM possible with minute skeleton samples, making developed to investigate photosymbiosis in fossil corals (8). For ex- it possible to sample only original, unaltered skeletal aragonite (13). ample, most modern symbiotic corals tend to form highly integrated colonies with small (<5 mm) corallites, whereas asymbiotic corals tend to have solitary growth forms or poorly integrated (phaceloid) RESULTS AND DISCUSSION colonies with larger corallites (9). However, numerous exceptions ex- We applied these new skeleton-based indicators of photosymbiosis to ist in these morphological traits, pointing to the need for additional, a suite of fossil coral skeletons from the lower Norian outcrops (about more definitive indicators. Skeletal isotopic compositions have been 212 Ma) of the Lycian Taurus (near Gödene, Alakir Çay Valley, Antalya used to distinguish symbiotic from asymbiotic corals. Modern asymbio- Province, Turkey), which provide a unique opportunity to investigate tic corals show a wide range of positively correlated 18O/16Oand13C/ the onset of photosymbiosis among scleractinians (Fig. 1A). Coral col- 12C ratios, whereas these ratios are uncorrelated and have a tendency for oniesoccurin“cipit blocks” (reef limestone blocks deposited in slope/ higher 13C/12Cinsymbioticcorals(10). In addition, intracrystalline or- basinal sediments) derived from the destruction and redeposition of ganic matter (OM) in asymbiotic corals has higher 15N/14Nratiosthan shallow-water patch reefs that developed during early Norian on the intracrystalline OM in symbiotic corals (11). Although these isotopic southern part of the Apulia-Taurus platform, along the western margin criteria hold strong potential as proxies for symbiosis in fossil corals, of the Tethys Ocean (fig. S1) (14).Thelocalityiswellknownforits excellent preservation of fossil corals (15), which was verified in this 1Institute of Paleobiology, Polish Academy of Sciences, Twarda 51/55, PL-00-818 study with a broad range of complementary analytical techniques (see Warsaw, Poland. 2Department of Geosciences, Princeton University, Princeton, NJ the Supplementary Materials). Ultrastructurally, the skeletons consist of 08544, USA. 3School of Oceanography, University of Washington, 1492 NE Boat “ ” Street, Seattle, WA 98105, USA. 4Marine Sciences Department, Federal University two main components: the rapid accretion deposits (RADs; also known of São Paulo, Santos, São Paulo 11030-400, Brazil. 5Department of Chemistry, Uni- as centers of calcification) which form a narrow, central zone of septa versity of Warsaw, Pasteura 1, PL-02-093 Warsaw, Poland. 6Laboratory for Biological (ca. 5 volume %), and “thickening deposits” (TDs; also known as fibers) Geochemistry, School of Architecture, Civil and Environmental Engineering, Ecole which constitute the main skeletal component (ca. 95 volume %) (16). Polytechnique Fédérale de Lausanne, and Center for Advanced Surface Analysis, In- stitute of Earth Sciences, Université de Lausanne, CH-1015 Lausanne, Switzerland. The RADs are originally nanocrystalline (17, 18) and in comparison to *Corresponding author. Email: [email protected] TDs are easily altered during diagenesis. RADs in Triassic corals often Frankowiak et al. Sci. Adv. 2016; 2 : e1601122 2 November 2016 1of7 SCIENCE ADVANCES | RESEARCH ARTICLE Downloaded from http://advances.sciencemag.org/ on November 2, 2016 Fig. 1. Macrostructural and microstructural characteristics of modern and Triassic corals. (A) Polished slab showing morphological diversity of corals from Antalya (Turkey). (B) CV of growth band thickness in modern asymbiotic (yellow dots) and symbiotic (green squares) scleractinian corals. All Triassic corals (red diamonds), irrespective of growth form, show regular growth banding, that is, low CV values, consistent with a symbiotic lifestyle. Growth increments of TDs (transmitted light images) in the Triassic Coryphyllia sp. (solitary) (C), Volzeia aff. badiotica (phaceloid) (D), Cerioheterastraea cerioidea (cerioid) (E), Meandrovolzeia serialis (meandroid) (F), and Ampakabastraea nodosa (thamnasterioid) (G)indirectcomparisonwithmoderncorals:asymbioticDesmophyllum dianthus (solitary) (H), Lophelia pertusa (phaceloid) (I), symbiotic Goniastraea sp. (cerioid) (J), Symphyllia radians (meandroid) (K), and Pavona cactus (thamnasterioid) (L). Measurements and taxonomic attribution are provided in tables S1 and S2. Scale bars, 10 mm (A) and 50 mm(CtoL). have crystal textures characteristic of diagenetic calcite spar (fig. S2D), the In these samples, transmitted light images of TD revealed the pres- presence of which was independently confirmed by micro-Raman map- ence of centrifugally arranged fibers grouped in bundles (Fig. 1, C to ping (green color; fig. S2, E to H). To avoid these regions during geo- G). Fibers were observed to have doublets of optically light and dark chemical sampling, we characterized their distribution in the skeleton. bands representing growth increments (12), which are also observable In comparison to RADs, TDs are composed of denser aragonite, in scanning electron microscopy (SEM) as layers with positive and which is relatively poor in OM. Therefore, these regions better pre- negative etching relief, respectively (figs. S2D and S3, E and F). These served their original structures in fossil corals (19). We considered TDs were usually preserved as pure aragonite, as demonstrated by a the TDs in the fossil coral skeletons to be well preserved only when lack of cathodoluminescence (CL) signal (figs. S2C, S3D, and S4a to meeting all of the following criteria (19, 20): (i) arrangement of S4i) and by Raman spectral imaging (figs. S2, E to H, and S3C). Oc- crystals and crystal habits identical to those in modern Scleractinia, casionally, small areas (a few micrometers in size) had been altered to (ii) absence of Mn-induced
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