The order is Haplosclerida. In total, we obtained 395 combined sequences of the mitochondrial CO1 and ATP6 markers, which resulted in 17 different haplotypes. Description of sponges with illustrations: Sponges - The Simplest Animals. volume 36, pages933–945(2017)Cite this article. In sponges, mitochondrial variation is typically low (Wörheide et al. Taxonomy; Resources Gallery did you know that the Giant Barrel Sponge can live for over 2,000 years. This suggests that distinct species of giant barrel sponges must have existed prior to the most recent physical separation of the tropical Atlantic and the Indo-Pacific. Lines connecting haplotypes represent one base substitution between two haplotypes; additional crossbars indicate an additional base substitution each. PubMed The third objective is to investigate the importance of photosymbionts in the chemical defense and bleaching of the giant barrel sponge Xestospongia muta. The domain is Eukarya. 1999). Bull Mar Sci 58:792–803, Vermeij GJ (2001) Community assembly in the sea: geologic history of the living shore biota. National Geographic article about sponges in the Shape of Life: Was The Humble Sponge Earth's First Animal? Globally intertwined evolutionary history of giant barrel sponges, http://creativecommons.org/licenses/by/4.0/, https://doi.org/10.1007/s00338-017-1585-6. 2016). The PCR protocol consisted of an initial denaturing step (95 °C for 5 min), followed by 35 cycles of denaturing (95 °C for 30 s), annealing (45 °C for 30 s) and extension (72 °C for 45 s), and a final extension step (72 °C for 4 min) executed in a T100 thermal cycler from Bio-Rad. Harvard University Press, Cambridge, MA, USA, McMurray SE, Blum JE, Pawlik JR (2008) Redwood of the reef: growth and age of the giant barrel sponge Xestospongia muta in the Florida Keys. As is common in sponges (Wörheide et al.
A recently published demographic study of the giant barrel sponge on the Florida Keys reefs showed population increases by ~40% between 2000 and 2006. All of them share the same basic body plan: a … The number of bootstrap replications was set at 1000. 2009; Maloof et al. The giant barrel sponge is a large sponge that lives on coral reefs around the Caribbean Sea and adjacent waters. Abbreviations in the legend of the background colors indicate the current species consensus (XT, Xestospongia testudinaria; XM, Xestospongia muta). Values on branches indicate bootstrap support (only shown when >50) and Bayesian support value (only shown when >0.90). We conducted an automated barcoding gap discovery (ABGD) analysis with standard settings to split our sequences into candidate species and compare those to our identified groups based on congruence between mtDNA, nDNA and geography (Puillandre et al. 2016). 2011). Video : Yucatania sphaeroidocladus: Most of them live on barrel sponges of the genus Xestospongia. Google Scholar, Teske PR, Rius M, McQuaid CD, Styan CA, Piggott MP, Benhissoune S, Fuentes-Grünewald C, Walls K, Page M, Attard CRM, Cooke GM, McClusky CF, Banks SC, Barker NP, Cooke GM (2011) “Nested” cryptic diversity in a widespread marine ecosystem engineer: a challenge for detecting biological invasions. Mol Biol Evol 10:512–526, CAS All of the following sponges are found within the coral cap region of the sanctuary (0-130 ft, 0-40m deep). Our second aim was to test whether the giant barrel sponges in the tropical Atlantic and the Indo-Pacific represent two monophyletic lineages. Bioinformatics 23:2947–2948, Levitan DR, Fukami H, Jara J, Kline D, McGovern TM, McGhee KE, Swanson CA, Knowlton N (2004) Mechanisms of reproductive isolation among sympatric broadcast-spawning corals of the Montastraea annularis species complex. et al. Trends Ecol Evol 28:359–366, Bowen BW, Bass AL, Rocha LA, Grant WS, Robertson DR (2001) Phylogeography of the trumpetfishes (Aulostomus): ring species complex on a global scale. PLoS One 7:e35105, van Veghel MLJ, Cleary DFR, Bak RPM (1996) Interspecific interactions and competitive ability of the polymorphic reef-building coral Montastrea annularis. Giant barrel sponge. Development 11. Reproduction 10. Nuclear DNA (nDNA) evolves independently from mitochondrial DNA (mtDNA); thus, congruent patterns across these markers support the existence of biological species (Goetze 2010; Padial et al. This renewal project would investigate the chemical ecology of Caribbean reef sponges, a group whose taxonomy … Three species have been described, with the species delineation mainly based on geographic distributions. Joseph Henry Press, Washington, USA, pp 83–108, Reece JS, Bowen BW, Larson A (2011) Long larval duration in moray eels (Muraenidae) ensures ocean-wide connectivity despite differences in adult niche breadth. The nuclear intron ATPsß provided much more genetic variation (157 segregating sites; π = 0.0767) than the mitochondrial genes (13 segregating sites; π = 0.0032). Resolving accurate species boundaries in such groups is important for the conservation of tropical marine ecosystems. A ninth group (group 4) consisted of a single sample from Taiwan. Sponges in the genus Xestospongia exist in many morphotypes and include the two giant barrel sponges Xestospongia muta, which is ubiquitous throughout coral reefs in the Caribbean, and Xestospongia testudinaria, which can be found throughout Indo-Pacific reef environments. 4. Xestospongia muta. However, present-day ocean currents and geographic barriers cannot explain why giant barrel sponges in the tropical Atlantic and the Indo-Pacific do not form monophyletic lineages, and why in each ocean basin multiple genetically isolated lineages exist in sympatry. 2016) using the Tamura–Nei model (Tamura and Nei 1993) with standard settings. Altogether, we identified at least eight potential giant barrel sponge species globally, yet the limitations of the markers make it impossible to exactly determine the number of species with the data presented in this study. Article Barrel shaped, with thick walls. The congruent identification of a phylogenetic lineage by multiple unlinked genetic loci indicates that it is genetically isolated from other such lineages, and thus qualifies as a species, because only in separate species will the coalescent histories of the different markers agree (Avise and Ball 1990; Coyne and Orr 2004; Padial et al. They are considered the oldest multicellular animal lineage (van Soest et al. Pie chart size is relative to the number of individuals with that haplotype. BMC Evol Biol 11:176, van Soest RWM (1980) Marine sponges from Curaçao and other Caribbean localities. The giant barrel sponge has been called the "redwoodof the reef" because of its size and estimated lifespan of hundreds to a thousand or more years. However, if sponges do not form two distinct monophyletic groups in different ocean basins, it suggests that a species complex already existed prior to the ocean basins becoming separated. We found three potential giant barrel sponge species in the central Indo-Pacific (groups 1, 2, 3), three in the tropical Atlantic (groups 7, 8, 9), one in the western Indian Ocean (group 6) and one in the Red Sea (group 5). At present, giant barrel sponges occur in the western Indo-Pacific (including the Red Sea and western Indian Ocean), the central Indo-Pacific and the tropical Atlantic. However, these studies were done at small spatial scales, and, to the best of our knowledge, there has been no global phylogenetic study of any sponge taxon. An ABGD analysis on our nuclear data supported the groups 2, 3, 4, 5, 8 and 9 with recursive partitions at a prior maximal distance of 0.0046, while groups 1, 6 and 7 were not supported as separate groups (ESM S2). Economic Importance. Congruent patterns between mtDNA and nDNA markers of giant barrel sponges around the globe point to the existence of multiple genetically isolated taxa and support our hypothesis of the existence of additional species. Also, heterozygotes were only found with both alleles within the same nuclear group providing further support that different groups are reproductively isolated (ESM Fig. Also, some groups are only partly congruent, for example groups 4 and 5. In: Futuyma D, Antonovics J (eds) Oxford surveys in evolutionary biology, vol 7., Oxford University PressOxford, UK, pp 45–67, Bell JJ, Smith D, Hannan D, Haris A, Jompa J, Thomas L (2014) Resilience to disturbance despite limited dispersal and self-recruitment in tropical barrel sponges: implications for conservation and management. Group 8 represented one network, group 3 represented three networks, and the remaining three networks consisted of the combinations of groups 2 and 9, groups 1, 6 and 7, and groups 4 and 5, respectively (ESM S3, S4). This project will include comparisons of growth and reproductive output of several species in each class. Mol Ecol 19:952–967, Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. 2016). In particular, groups 1, 6 and 7 are ‘mixed’ in the tree, but they do not share any alleles. J Fish Biol 72:1101–1121, Rocha LA, Robertson DR, Roman J, Bowen BW (2005) Ecological speciation in tropical reef fishes. Nature 457:718–721, Maloof AC, Rose CV, Beach R, Samuels BM, Calmet CC, Erwin DH, Poirier GR, Yao N, Simons FJ (2010) Possible animal-body fossils in pre-Marinoan limestones from South Australia. Re-analysis of the sample carrying the C3 haplotype from Lembeh Island showed that the sample was C2, and hence, this haplotype was wrongly identified (Swierts et al. 2005), mitochondrial variation was low (π = 0.0032). Trumpet fish represent a so-called ‘global ring species complex’, in which different lineages have come into contact after three to four million years of isolation and appear to be merging (Bowen et al. 2012). Mol Ecol 21:1864–1877, Reaka-Kudla ML, Wilson DE, Wilson EO (1997) Biodiversity II. It is typically brownish-red to brownish-gray in color, with a hard or stony texture. Red-Orange Encrusting Sponge. 2010). Genetic markers have become increasingly important tools to identify divergent cryptic species and have forced the rejection of the long-believed assumption of cosmopolitan distribution of certain species (Boury-Esnault et al. Certain other groups were statistically supported, which is, particularly in combination with their sympatric occurrence, a strong indication for speciation. Proc R Soc Lond B Biol Sci 280:20131541, Coyne JA, Orr HA (2004) Speciation. Geology 6:630–634, Kerr RG, Kerr SL, Djerassi C (1991) Biosynthetic studies of marine lipids. Mar Biol 155:159–171, McMurray SE, Henkel TP, Pawlik JR (2010) Demographics of increasing populations of the giant barrel sponge Xestospongia muta in the Florida Keys. (2013), but amplification and sequencing were repeated in this study to confirm haplotype assignment. Water is continually being pumped through the interior of the sponge. The genetic differences between the nuclear clades are based on the variation of a single gene and the mitochondrial markers have low variation. We'd like to inform you that we have updated our Privacy Notice to comply Only reconstructed haplotypes with probabilities >0.9 were used for further analysis. Definition of Sponges 3. You are using a version of browser that may not display all the features of this website. Below is the link to the electronic supplementary material. Most global marine species complexes are so-called ‘sibling species complexes’ that developed simultaneously in different ocean basins, potentially followed by cryptic invasions (Schwaninger 2008; Geller et al. Sponges of diverse size, shape, and color. All sequences were submitted to GenBank under accession numbers KY381293–KY381577. Mar Biol 141:377–386, Fromont J, Bergquist PR (1994) Reproductive biology of three sponge species of the genus Xestospongia (Porifera: Demospongiae: Petrosida) from the Great Barrier Reef. Science 235:1156–1167, Harzhauser M, Piller WE (2007) Benchmark data of a changing sea—palaeogeography, palaeobiogeography and events in the Central Paratethys during the Miocene. Google Scholar, Bowen BW, Gaither MR, DiBattista JD, Iacchei M, Andrews KR, Grant WS, Toonen RJ, Briggs JC (2016) Comparative phylogeography of the ocean planet. Previously, the closure of the Isthmus of Panama, approximately 3 million yr ago (Keigwin 1978, was suggested as the final geographic separation between giant barrel sponges from the tropical Atlantic and the Indo-Pacific (Montalvo and Hill 2011; Swierts et al. 2013). The nuclear sequences provided much more information than the mitochondrial markers, but were mostly phylogenetically congruent with the mtDNA. It grows at depths from 10 meters down to 120 metres (390 ft), and can reach a diameter of 1.8 metres (6 feet). Giant barrel sponges are large and long-lived and have therefore been nicknamed ‘the redwoods of the reef’ (McMurray et al. Also, the inconsistencies of the placement of certain groups relative to other groups illustrate that the phylogenetic relationships between the groups cannot be completely resolved with the combination of markers used in this study. 2012), having evolved more than 500 million yr ago (Love et al. 2010) with the GTR model, which was the best fit model according to jModelTest2 (Guindon and Gascuel 2003; Darriba et al. S1). SPONGE SPECIES. Molecular studies on giant barrel sponges using these mtDNA and nDNA markers have revealed some interesting results. The kingdom is Animalia. In contrast, the giant barrel sponge, Xestospongia muta, showed evidence of limited larval exchange or connection between Pulley Ridge and the Dry Tortugas and no connectivity with the Florida Keys. PubMed 1999). Giant barrel sponges are large and long-lived and have therefore been nicknamed ‘the redwoods of the reef’ (McMurray et al. Help pages, FAQs, UniProtKB manual, documents, news archive and Biocuration projects. Haplosclerida. Orange Sieve Encrusting Sponge. Globally intertwined evolutionary history of giant barrel sponges. Reaching sizes of at least 6 feet (1.8 m) across, this is one of the largest sponge species wherever it lives. Table 3 shows the mean genetic distances between these drafted groups. Mar Ecol Prog Ser 437:269–277, Renema W, Bellwood DR, Braga JC, Bromfield K, Hall R, Johnson KG, Lunt P, Meyer CP, McMonagle LB, Morley RJ, O’Dea A, Todd JA, Wesselingh FP, Wilson MEJ, Pandolfi JM (2008) Hopping hotspots: global shifts in marine biodiversity. Eine bekannte Sehenswürdigkeit in der Nähe ist in Obri Sud das Restaurant mit dem Riesenfass. 2013). Box 9517, 2300 RA, Leiden, The Netherlands, Thomas Swierts, Katja T. C. A. Peijnenburg, Christiaan A. de Leeuw & Nicole J. de Voogd, Institute for Biodiversity and Ecosystem Dynamics (IBED), P.O. Three species of giant barrel sponge are currently recognized in two distinct geographic regions, the tropical Atlantic and the Indo-Pacific. For the ATP6 gene, we used the primers ATP6porF (5′-GTAGTCCAGGATAATTTAGG-3′) and ATP6porR (5′-GTTAATAGACAAAATACATAAGCCTG-3′), which amplified a product of 445 bp. DNA was extracted from sponge tissue using the DNeasy Blood and Tissue kit (Qiagen) following the manufacturer’s instructions. (Schmidt, 1870) Description: Persistently a cup- or barrel-shaped sponge with a rough, often jagged, stone-hard exterior. Background colors represent geographic origin of the lineages. Origin 4. A focus on wide-ranging studies within each marine phylum should therefore be a priority for the scientific community. 2013; Bell et al. It is, therefore, important to study and quantify the diversity of these systems and understand the evolutionary processes that have led to this diversity. Mean genetic distance for the nDNA was considerably higher than for the mtDNA. 1991). Also in the tropical Atlantic, McMurray et al. 2). Evolution 58:308–323, López-Legentil S, Pawlik JR (2009) Genetic structure of the Caribbean giant barrel sponge Xestospongia muta using the I3-M11 partition of COI. All PCR products were sequenced in both directions by BaseClear, Leiden, the Netherlands or Macrogen Europe, Amsterdam, the Netherlands. This information provides insight into genetic divergence among tropical reefs before physical barriers impeded gene flow between the Indo-Pacific and tropical Atlantic. 2013; Bell et al. These specimens may be over 100 years old, as the sponges grow only about 1.5 cm a year. 2010). Taken together, these factors were believed to lead to fewer opportunities for allopatric speciation compared to terrestrial ecosystems (Palumbi 1997; Rocha and Bowen 2008). Sinauer Associates, Sunderland, MA, Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. MtDNA diversity of the Indonesian giant barrel sponge Xestospongia testudinaria (Porifera: Haplosclerida) – implications from partial cytochrome oxidase 1 sequences - Volume 96 Special Issue - Edwin Setiawan, Nicole J. de Voogd, Thomas Swierts, John N.A. Therefore, these three groups seem to be distributed across the entire tropical Atlantic. Canal System 8. (2002). Coral Reefs 36, 933–945 (2017). To test for congruent patterns at an independent genetic locus, the ATPsβ nuclear intron was amplified for a subset of 211 samples following Jarman et al. PLoS One 8:e74396, Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Domain, Kingdom, Phylum, Class, Order, Family, Genus, Species. Our own interpretation of nine groups differs from the results from the ABGD and TCS analyses, which both find only seven groups, but with partially different compositions. Aquat Biol 23:1–13, Montalvo NF, Hill RT (2011) Sponge-associated bacteria are strictly maintained in two closely related but geographically distant sponge hosts. Google Scholar, Bentlage B, Wörheide G (2007) Low genetic structuring among Pericharax heteroraphis (Porifera: Calcarea) populations from the Great Barrier Reef (Australia), revealed by analysis of nrDNA and nuclear intron sequences. Some of the previously assumed ‘morphological plasticity’ of giant barrel sponges might actually be morphological differentiation between species. Box 338, 6700 AH, Wageningen, The Netherlands, Departamento de Biologia, CESAM, Centro de Estudos do Ambiente e do Mar, Universidade de Aveiro, Aveiro, Portugal, You can also search for this author in Sponge tissue for DNA extraction was immediately stored in absolute ethanol (98%) in a cool box. Samples that contained many double peaks may have represented mixtures of multiple sequences and were therefore cloned using the pGEM-T Easy kit (Promega Corporation) or the TOPO-TA cloning kit (Thermo Fisher Scientific), following the manufacturers’ protocols. The giant barrel sponge (Xestospongia muta) is the largest species of sponge found growing on Caribbean coral reefs. PubMed While not all branches in the nDNA tree were statistically supported and some mtDNA haplotypes were shared between regions, we could identify multiple groups that potentially operate as reproductively isolated populations. General Organisation 7. Hooper, Gert Wörheide, Dirk Erpenbeck Giant kelp grow at an average rate of 11 inches (28 cm) a day but can grow 24 inches (61 cm) a day in ideal conditions. Giant barrel sponges from the tropical Atlantic and the Indo-Pacific sharing the same CO1 haplotype have both been related to an exterior morphology consisting of digitate structures (López-Legentil and Pawlik 2009; Swierts et al. We obtained a total of 395 combined sequences of partial mitochondrial CO1 and ATP6 genes. Marine Biodiversity, Naturalis Biodiversity Center, P.O. Amplification was performed in a 25 µL total reaction volume with 14.55 µL sterile water, 4.2 Ll dNTPs (2.5 mM), 2.6 µL buffer (Qiagen), 1.6 Ll BSA (Promega) 0.4 µL of each primer (10 µM), 0.25 µL taq polymerase (Qiagen) and 1 µL DNA template (20 ng µL−1). Caribbean reef shark (Carcharhinus perezii) and giant barrel sponge (Xestospongia muta), Roatan, Bay Islands, Honduras Orange elephant ear sponge (Agelas clathrodes) and a gorgonian (Plexaurella nutans). The sponge has primary roles providing ecosystem services and creating unique habitats for diverse microbial communities. 2014; Knapp et al. Sinauer Press, Sunderland, MA, USA, pp 39–60, Wörheide G, Solé-Cava AM, Hooper JN (2005) Biodiversity, molecular ecology and phylogeography of marine sponges: patterns, implications and outlooks. 2013) illustrate the evolutionary potential of tropical marine environments. However, there is an inconsistency in their placement relative to the other groups, since they are most closely related to group 8 in the nDNA phylogenetic tree (Fig. Giant kelp grows faster than bamboo. Individuals were grouped based on a combination of mtDNA, nDNA and the geographic origin of the sample. This rules out the scenario that one species of giant barrel sponge developed into separate species complexes following geographic separation and instead suggests that multiple species of giant barrel sponges already existed prior to the physical separation of the Indo-Pacific and tropical Atlantic. Most studies that have focused on the distribution and evolution of marine species cover small spatial scales and become more useful when they are compared to more wide-ranging studies (Briggs and Bowen 2013; Cowman and Bellwood 2013a). This pattern may, however, be found in other tropical marine species, especially those with a long evolutionary history such as other globally distributed sponge groups. Not only are they the largest sponges on the reef, but they also are very long lived – up tp thousands of years. Classification 6. In the western Indian Ocean, we found five different haplotypes in 21 sponges that were spread over the haplotype network; three of these haplotypes were only present in this region. Giant Barrel Sponge has shades of gray color, brown, red brown or rose purple color. 3); a larger and more detailed rectangular phylogenetic tree is provided in the Electronic supplementary material, ESM, Fig. Sponges (Porifera) are an animal group with a relatively simple morphology and often pronounced morphological plasticity (Knowlton 2000). 2). 2013) due to the combined threat of climate change and anthropogenic stressors including pollution and overfishing (Hughes 1994; Pandolfi et al. The nuclear adenine triphosphate synthesis-β intron (ATPsβ) is very variable in giant barrel sponges, and because it is unlinked to the mtDNA, it serves as a good additional marker to identify potential species (Bentlage and Wörheide 2007; Swierts et al. 2008). PubMed Central Fifty-four sponge samples from Lembeh Island, Indonesia, were previously described in Swierts et al. History of Sponges 2. Mol Ecol 19:4678–4694.