DNA barcodes are ineffective for species identification of Acropora corals from the aquarium trade
Authors/Creators
- 1. Department of Biological Sciences, National University of Singapore, Singapore, Singapore|Yale-NUS College, National University of Singapore, Singapore, Singapore
- 2. Department of Biological Sciences, National University of Singapore, Singapore, Singapore
- 3. NUS High School of Math and Science, Singapore, Singapore
- 4. Lee Kong Chian Natural History Museum, National University of Singapore, Singapore, Singapore|Department of Biological Sciences, National University of Singapore, Singapore, Singapore
Description
Species identification of stony corals (Scleractinia), which are regulated under the Convention on International Trade in Endangered Species of Wild Fauna and Flora, is critical for effective control of harvest quotas, enforcement of trade regulations and species conservation in general. DNA barcoding has the potential to enhance species identification success, depending on the specific taxon concerned and genetic markers used. For Acropora, DNA barcoding, based on the mitochondrial putative control region (mtCR) and the nuclear PaxC intron (PaxC), has been commonly used for species identification and delimitation, but the reliability and robustness of these loci remain contentious. Therefore, we sought to verify the applicability of this approach. In this study, we obtained 127 Acropora colonies from the aquarium trade to test the effectiveness of barcoding mtCR and PaxC for species identification. We were able to recover sequences for both loci in over half of the samples (n = 68), while gene amplification and sequencing of mtCR (n = 125) outperformed PaxC (n = 70). Amongst the 68 samples with both loci recovered, just a single sample could be unambiguously identified to species. Preliminary identities, based on only one gene, were assigned for 40 and 65 samples with mtCR and PaxC, respectively. Further analyses of 110 complete mitochondrial genomes obtained from GenBank showed that, despite the full length of the sequences, only eight species were delimited, of which only three species were correspondingly monophyletic. Therefore, we conclude that the commonly used DNA barcoding markers for Acropora are ineffective for accurate species assignments due to limited variability in both markers and even across the entire mitochondrial genome. Therefore, we propose that barcoding markers should generally not be the only means for identifying corals.
Files
BDJ_article_125914.pdf
Files
(297.9 kB)
| Name | Size | Download all |
|---|---|---|
|
md5:b2df2898565f7e098cbaa5fc0e211d1b
|
297.9 kB | Preview Download |
System files
(115.3 kB)
| Name | Size | Download all |
|---|---|---|
|
md5:37c8dbe88a7b52cefe8df23a0061b369
|
115.3 kB | Download |
Linked records
Additional details
References
- Ayad LA, Pissis SP (2017) MARS: improving multiple circular sequence alignment using refined sequences. BMC Genomics 18: 86. https://doi.org/10.1186/s12864-016-3477-5
- Bridge TC, Cowman PF, Quattrini AM, Bonito VE, Sinniger F, Head CE, Hung JY, Halafihi T, Rongo T, Baird AH (2023) Acropora tenuis relationship: traditional taxonomy obscures systematics and biogeography of the 'Acropora tenuis' (Scleractinia: Acroporidae) species complex. Zoological Journal of the Linnean Societyzlad062. https://doi.org/10.1093/zoolinnean/zlad062
- But GW, Wu HY, Shao KT, Shaw PC (2020) Rapid detection of CITES-listed shark fin species by loop-mediated isothermal amplification assay with potential for field use. Scientific Reports 10: 4455. https://doi.org/10.1038/s41598-020-61150-8
- CITES (2000) Identification and reporting requirements for trade in specimens of hard coral. CITES. Doc. 11.37.
- CITES (2013) Trade in stony corals: List of coral taxa where identification to genus level is acceptable. CITES. Notification number 2013/035. URL: https://cites.org/eng/node/1274
- CITES (2023) Consultation on trade in stony corals. CITES. Notification number 2023/081. URL: https://cites.org/eng/node/137000
- Cohen FPA, Valenti WC, Calado R (2013) Traceability issues in the trade of marine ornamental species. Reviews in Fisheries Science 21 (2): 98‑111. https://doi.org/10.1080/10641262.2012.760522
- Colin L, Abed-Navandi D, Conde DA, Craggs J, Silva Rd, Janse M, Källström B, Pearce-Kelly A, Yesson C (2022) What's left in the tank? Identification of non-ascribed aquarium's coral collections with DNA barcodes as part of an integrated diagnostic approach. Conservation Genetics Resources 14: 167‑182. https://doi.org/10.1007/s12686-021-01250-3
- Cowman PF, Quattrini AM, Bridge TC, Watkins-Colwell GJ, Fadli N, Grinblat M, Roberts TE, McFadden CS, Miller DJ, Baird AH (2020) An enhanced target-enrichment bait set for Hexacorallia provides phylogenomic resolution of the staghorn corals (Acroporidae) and close relatives. Molecular Phylogenetics and Evolution 153: 106944. https://doi.org/10.1016/j.ympev.2020.106944
- Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T (2020) ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Molecular Biology and Evolution 37 (1): 291‑294. https://doi.org/10.1093/molbev/msz189
- Dee L, Horii S, Thornhill D (2014) Conservation and management of ornamental coral reef wildlife: Successes, shortcomings, and future directions. Biological Conservation 169: 225‑237. https://doi.org/10.1016/j.biocon.2013.11.025
- Foster AB (1979) Phenotypic plasticity in the reef corals Montastraea annularis (Ellis & Solander) and Siderastrea siderea (Ellis & Solander). Journal of Experimental Marine Biology and Ecology 39 (1): 25‑54. https://doi.org/10.1016/0022-0981(79)90003-0
- Fukami H, Iwao K, Kumagai NH, Morita M, Isomura N (2019) Maternal inheritance of F1 hybrid morphology and colony shape in the coral genus Acropora. PeerJ 7: e6429. https://doi.org/10.7717/peerj.6429
- Fukami H, Niimura A, Nakamori T, Iryu Y (2021) Species composition and mitochondrial molecular phylogeny of Acropora corals in Funakoshi, Amami-Oshima Island, Japan: A proposal for its new taxonomic grouping. Galaxea, Journal of Coral Reef Studies 23: 17‑35. https://doi.org/10.3755/galaxea.G23-5
- Green E, Shirley F (1999) The global trade in coral. WCMC – World Conservation Press, Cambridge, UK.
- Groenenberg DJ, Neubert E, Gittenberger E (2011) Reappraisal of the "Molecular phylogeny of Western Palaearctic Helicidae s.l. (Gastropoda: Stylommatophora)": When poor science meets GenBank. Molecular Phylogenetics and Evolution 61 (3): 914‑923. https://doi.org/10.1016/j.ympev.2011.08.024
- Hellberg ME (2006) No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evolutionary Biology 6: 24. https://doi.org/10.1186/1471-2148-6-24
- Hoeksema B, Arrigoni R (2020) DNA barcoding of a stowaway reef coral in the international aquarium trade results in a new distribution record. Marine Biodiversity 50 (3): 41. https://doi.org/10.1007/s12526-020-01075-7
- Huang D, Meier R, Todd PA, Chou LM (2008) Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. Journal of Molecular Evolution 66: 167‑174. https://doi.org/10.1007/s00239-008-9069-5
- Katoh K, Standley DM (2013) MAFFT Multiple Sequence Alignment Software Version 7: improvements in performance and usability. Molecular Biology and Evolution 30 (4): 772‑780. https://doi.org/10.1093/molbev/mst010
- Kitahara M, Fukami H, Benzoni F, Huang D (2016) The New Systematics of Scleractinia: Integrating Molecular and Morphological Evidence. The Cnidaria, Past, Present and Future41‑59. https://doi.org/10.1007/978-3-319-31305-4_4
- Knop D, Moorhead J (2012) Ornamentals. In: Lucas JS, Southgate PC (Eds) Aquaculture: Farming aquatic animals and plants. 2. Blackwell Publishing, 583-605 pp. https://doi.org/10.1002/9781118687932
- Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35 (21): 4453‑4455. https://doi.org/10.1093/bioinformatics/btz305
- Naaum AM, Cusa M, Singh M, Bleicher Z, Elliott C, Goodhead IB, Sanchez JA, et al. (2021) Validation of FASTFISH-ID: A new commercial platform for rapid fish species authentication via universal closed-tube barcoding. Food Research International 141: 110035. https://doi.org/10.1016/j.foodres.2020.110035
- Pavitt A, Malsch K, King E, Kachelriess D, Vannuccini S, Friedman K (2021) CITES and the sea: Trade in commercially exploited CITES-listed marine species. FAO. FAO Fisheries and Aquaculture technical Paper No. 666. https://doi.org/10.4060/cb2971en
- Pratlong M, Rancurel C, Pontarotti P, Aurelle D (2017) Monophyly of Anthozoa (Cnidaria): why do nuclear and mitochondrial phylogenies disagree?. Zoologica Scripta 46 (3): 363‑371. https://doi.org/10.1111/zsc.12208
- Quek ZBR, Huang D (2021) Application of phylogenomic tools to unravel anthozoan evolution. Coral Reefs 41: 475‑495. https://doi.org/10.1007/s00338-021-02072-3
- Quek ZBR, Jain SS, Richards ZT, Arrigoni R, Benzoni F, Hoeksema BW, Carvajal JI, Wilson NG, Baird AH, Kitahara MV, Seiblitz IG, Vaga CF, Huang D (2023) A hybrid-capture approach to reconstruct the phylogeny of Scleractinia (Cnidaria: Hexacorallia). Molecular Phylogenetics and Evolution 186: 107867. https://doi.org/10.1016/j.ympev.2023.107867
- Ramírez-Portilla C, Baird AH, Cowman PF, Quattrini AM, Harii S, Sinniger F, Flot JF (2022) Solving the coral species delimitation conundrum. Systematic Biology 71 (2): 461‑475. https://doi.org/10.1093/sysbio/syab077
- Rosser NL (2015) Asynchronous spawning in sympatric populations of a hard coral reveals cryptic species and ancient genetic lineages. Molecular Ecology 24 (19): 5006‑5019. https://doi.org/10.1111/mec.13372
- Rosser NL, Thomas L, Stankowski S, Richards ZT, Kennington WJ, Johnson MS (2017) Phylogenomics provides new insight into evolutionary relationships and genealogical discordance in the reef-building coral genus Acropora. Proceedings of the Royal Society B: Biological Sciences 284 (1846): 20162182. https://doi.org/10.1098/rspb.2016.2182
- Shearer TL, Van Oppen MJH, Romano SL, Wörheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Molecular Ecology 11 (12): 2475‑2487. https://doi.org/10.1046/j.1365-294x.2002.01652.xAbstract
- Suzuki G, Hayashibara T, Shirayama Y, Fukami H (2008) Evidence of species-specific habitat selectivity of Acropora corals based on identification of new recruits by two molecular markers. Marine Ecology Progress Series 355: 149‑159. https://doi.org/10.3354/meps07253
- Tlusty M, Cawthorn D, Goodman OB, Rhyne A, Roberts D (2023) Real-time automated species level detection of trade document systems to reduce illegal wildlife trade and improve data quality. Biological Conservation 281: 110022. https://doi.org/10.1016/j.biocon.2023.110022
- Todd P (2008) Morphological plasticity in scleractinian corals. Biological Reviews 83 (3): 315‑337. https://doi.org/10.1111/j.1469-185x.2008.00045.x
- Todd PA (2008) Morphological plasticity in scleractinian corals. Biological Reviews 83 (3): 315‑337. https://doi.org/10.1111/j.1469-185X.2008.00045.x
- Van Oppen MJH, B JM, Willis B, Miller DJ (2001) The evolutionary history of the coral genus Acropora (Scleractinia, Cnidaria) based on a mitochondrial and a nuclear marker: reticulation, incomplete lineage sorting, or morphological convergence? Molecular Biology and Evolution 18 (7): 1315‑1329. https://doi.org/10.1093/oxfordjournals.molbev.a003916
- Van Oppen MJH, Willis BL, Van Vugt HWJ, Miller DJ (2003) Examination of species boundaries in the Acropora cervicornis group (Scleractinia, Cnidaria) using nuclear DNA sequence analyses. Molecular Ecology 9 (9): 1363‑1373. https://doi.org/10.1046/j.1365-294x.2000.01010.x
- Wallace CC (1999) Staghorn corals of the World: A revision of the genus Acropora. CSIRO Publishing, Australia. https://doi.org/10.1071/9780643101388
- Wallace CC, Done BJ, Muir PR (2012) Revision and catalogue of worldwide staghorn corals Acropora and Isopora (Scleractinia: Acroporidae) in the Museum of Tropical Queensland. Memoirs of the Queensland Museum 57: 1‑255. https://doi.org/10.17082/j:2204-1478-56-2.2013-42
- Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29 (22): 2869‑2876. https://doi.org/10.1093/bioinformatics/btt499