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A phylogenomic examination of Palmyra Atoll’s corallimorpharian invader

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Abstract

The reefs at Palmyra Atoll, a small outlying atoll in the equatorial Pacific, have been undergoing a phase shift from scleractinian corals to a corallimorph-dominated benthos. It has been unclear whether there has been cryptic speciation or morphological plasticity leading to different ecotypes of Rhodactis howesii. Here, we use mitochondrial genomic analysis to assess species validation and underlying cause of morphological variation across the atoll. We mapped sequenced reads to Rhodactis indosinensis, R. howesii’s closest recorded genomic taxon. In addition to one individual from American Sāmoa, we assessed phylogenetic relationships of published corallimorph genomes with those from Palmyra. There was no identifiable population structure within Palmyra, and available dinoflagellate symbiont communities were consistent among the sequenced individuals. There were noticeable differences in symbiont communities between Palmyra and American Sāmoa individuals, as well as six fixed nucleotide differences. We conclude that the lack of taxonomically validated genetic reference material together with vague species descriptions, morphological plasticity and overlap among morphological characters, combine to raise doubts about the validity of the currently accepted species name, R. howesii. Comparison of our results to all currently available genetic data for corallimorpharians suggests that the species at Palmyra is most closely related to an unidentified species of Rhodactis from Okinawa. However, taxonomically confirmed R. howesii is absent from genetic databases, so no firm conclusions about species identification can yet be drawn. It seems clear that this group is in need of additional taxonomic work and a broad phylogenetic survey of taxa with geographic distribution would further our understanding of marine biodiversity, conservation, and invasion dynamics of this understudied group.

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References

  • 16S Metagenomic Sequencing Library Preparation. (2013) https://www.illumina.com/content/dam/illumina-support/documents/documentation/chemistry_documentation/16s/16s-metagenomic-library-prep-guide-15044223-b.pdf

  • Arif C, Daniels C, Bayer T, Banguera-Hinestroza E, Barbrook A, Howe CJ, LaJeunesse TC, Voolstra CR (2014) Assessing Symbiodinium diversity in scleractinian corals via next-generation sequencing-based genotyping of the ITS2 rDNA region. Mol Ecol 23:4418–4433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andrews, S. (2010) FastQC: A Quality Control Tool for High Throughput Sequence Data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/

  • Baker, A.C. (2004) Symbiont diversity on coral reefs and its relationship to bleaching resistance and resilience. Coral health and disease (pp. 177–194). Springer, Berlin, Heidelberg.

  • Baskett ML, Gaines SD, Nisbet RM (2009) Symbiont diversity may help coral reefs survive moderate climate change. Ecol Appl 19:3–17

    Article  PubMed  Google Scholar 

  • Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc R Soc B Biol Sci 273(1599):2305–2312. https://doi.org/10.1098/rspb.2006.3567

    Article  Google Scholar 

  • Cabral, R.B., Bradley, D., Mayorga, J., Goodell, W., Friedlander, A.M., Sala, E., Costello, C. and Gaines, S.D. (2020) A global network of marine protected areas for food. Proceedings of the National Academy of Sciences.

  • Carter, A. (2014) Invasion Mechanisms of the corallimorph, Rhodactis howesii, at Palmyra Atoll. Ph.D. thesis, University of California San Diego, p53.

  • Carter A, Edwards Clinton B, Fox MD, Amir CG, Eynaud Y, Johnson MD, Lewis LS, Sandin SA, Smith JE (2019) Changes in benthic community composition associated with the outbreak of the corallimorph, Rhodactis howesii at Palmyra Atoll. Coral Reefs 38:1267–1279

    Article  Google Scholar 

  • Cha, Harim. (2001) Systematics of the Order Corallimorpharia (Cnidaria: Anthozoa). [unpublished dissertation]. University of Kansas.

  • Chadwick-Furman NE, Spiegel M (2000) Abundance and clonal replication in the tropical corallimorpharian Rhodactis rhodostoma. Invertebr Biol 119:351–360

    Article  Google Scholar 

  • Chadwick-Furman NE, Spiegel M, Nir I (2000) Sexual reproduction in the tropical corallimorpharian Rhodactis rhodostoma. Invertebr Biol 119:361–369

    Article  Google Scholar 

  • Chen CA, Odorico DM, Lohuis MT, Veron JEN, Miller DJ (1995) Systematic Relationships within the Anthozoa (Cnidaria: Anthozoa) Using the 5’-end of the 28S rDNA. Mol Phylogenet Evol 4:175–183

    Article  CAS  PubMed  Google Scholar 

  • Chen CA, Willis BL, Miller DJ (1996) Systematic relationships between tropical corallimorpharians (cnidarian: anthozoa: corallimorpharia): Utility of the 5.8S and internal transcribed spacer (ITS) regions of the rRNA transcription unit. Bull Mar Sci 59:196–208

    Google Scholar 

  • Collen JD, Garton DW, Gardner JPA (2009) Shoreline changes and sediment redistribution at Palmyra Atoll (Equatorial Pacific Ocean): 1874-present. J Coastal Res 25:711–722

    Article  Google Scholar 

  • Crane NL, Paddack MJ, Nelson PA, Abelson A, Rulmal J, Bernardi G (2016) Corallimorph and Montipora Reefs in Ulithi Atoll, Micronesia: documenting unusual reefs. Journal of the Ocean Science Foundation 21:10–17

    Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fautin, D. G. (2013) World List of Corallimorpharia. Rhodactis howesii Saville-Kent, 1893. Accessed through: World Register of Marine Species

  • Fautin DG (2016) Catalog to families, genera, and species of orders Actiniaria and Corallimorpharia (Cnidaria: Anthozoa). Zootaxa 4145:1–449

    Article  PubMed  Google Scholar 

  • Fukami, H., Chen, C.A., Budd, A.F., Collins, A., Wallace, C., Chuang, Y., Chen, C., Dai, C., Iwao, K., Sheppard, C., and Knowlton, N. (2008) Mitochondrial and Nuclear Genes Suggest that Stony Corals Are Monophyletic but Most Families of Stony Corals Are Not (Order Scleractinia, Class Anthozoa, Phylum Cnidaria). PLoSOne 3:e3222.

  • Gaither MR, Szabo Z, Crepeau MW, Bird CE, Toonen RJ (2011) Preservation of corals in salt-saturated DMSO buffer is superior to ethanol for PCR experiments. Coral Reefs 30:329–333

    Article  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Harrington, B. et al. (2004–2005). Inkscape.

  • Hill MS (1996) Symbiotic zooxanthellae enhance boring and growth rates of the tropical sponge Anthosigmella varians forma varians. Mar Biol 125:649–654

    Article  Google Scholar 

  • Hoadley KD, Pettay DT, Dodge D, Warner ME (2016) Contrasting physiological plasticity in response to environmental stress within different cnidarians and their respective symbionts. Coral Reefs 35:529–542

    Article  Google Scholar 

  • Hsin Y, Qui B (2012) Seasonal fluctuations of the surface North Equatorial Countercurrent (NECC) across the Pacific Basin. Journal of Geophysical Research: Oceans 117:1–17

    Article  Google Scholar 

  • Hume BCC, Smith EG, Ziegler M, Warrington HJM, Burt JA, LaJeunesse TC, Wiedenmann J, Voolstra CR (2019) Symportal: A novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling”. Mol Ecol Resour 19:1063–1080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson, M.D., Fox, M.D., Kelly, E.L.A., Zgliczynski, B.J., Sandin, S.A., and Smith, J.E. (2020) Ecophysiology of coral reef primary producers across an upwelling gradient in the tropical central Pacific. PlosOne 15: e0228448.

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics Applications 28:1647–1649

    Google Scholar 

  • Kelly LW, Barott KL, Dinsdale E, Friedlander AM, Nosrat B, Obura D, Sala E, Sandin SA, Smith JE, Vermeij MJA, Williams GJ, Willner D, Rohwer F (2011) Black Reefs: Iron-induced phase shifts on coral reefs. The International Society for Microbial Ecology Journal 6:638–649

    Google Scholar 

  • Kenyon, J., Maragos, J., and Vroom, P. (2012) Monitoring supports establishment of Pacific Remote Islands Marine National Monument. Proceedings of the 12th International Coral Reef Symposium, Cairns, Australia.

  • Kitahara, M.V., Lin, M., Foret, S., Huttley, G., Miller, D.J., and Chen, C.A. (2014) The “Naked Coral” Hypothesis Revisited – Evidence against Scleractinian Monophyly. PlosOne 9: e94774.

  • Knapp IS, Godwin LS, Smith JE, Williams CJ, Bell JJ (2011) Records of non-indigenous marine species at Palmyra Atoll in the US Line Islands. Marine Biodiversity Records 4:1–7

    Article  Google Scholar 

  • Knapp, I.S., Forsman, Z.H., Williams, G.J., Toonen, R.J. and Bell, J.J. (2015) Cryptic species obscure introduction pathway of the blue Caribbean sponge (Haliclona (Soestella) caerulea),(order: Haplosclerida) to Palmyra Atoll, Central Pacific. PeerJ, 3: e1170.

  • Knapp, I.S.S., Puritz, J., Bird, C., Whitney, J., Sudek, M., Forsman, Z., and Toonen, R. (2016) ezRAD- an accessible next-generation RAD sequencing protocol suitable for non-model organsims_v3.2. https://doi.org/10.17504/protocols.io.e9pbh5n.

  • Koweek D, Dunbar RB, Rogers JS, Williams GJ, Price N, Mucciarone D, Teneva L (2015) Environmental and ecological controls of coral community metabolism on Palmyra Atoll. Coral Reefs 34(1):339–351. https://doi.org/10.1007/s00338-014-1217-3

    Article  Google Scholar 

  • McCauley DJ, Micheli F, Young HS, Tittensor DP, Brumbaugh DR, Madin EM, Holmes KE, Smith JE, Lotze HK, DeSalles PA, Arnold SN (2010) Acute effects of removing large fish from a near-pristine coral reef. Mar Biol 157:2739–2750

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuguru BL, Mgaya YD, Ohman MC, Wagner GM (2004) The reef environment and competitive success in the Corallimorpharia. Mar Biol 145:875–884

    Article  Google Scholar 

  • Kuguru BL, Chadwick NE, Achituv Y, Zandbank K, Tchernov D (2008) Mechanisms of habitat segregation between corallimorpharians: photosynthetic parameters and Symbiodinium types. Mar Ecol Prog Ser 269:115–129

    Article  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K, Battistuzzi FU (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lafferty KD, Shaw JC, Kuris AM (2008) Reef fishes have higher parasite richness at unfished Palmyra Atoll compared to fished Kiritimati Island. EcoHealth 5:338–345

    Article  PubMed  Google Scholar 

  • LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic Revision of Symbiodiniaceae Highlights the Antiquity and Diversity of Coral Endosymbionts. Curr Biol 28:2570–2580

    Article  CAS  PubMed  Google Scholar 

  • Lin M, Kitahara MV, Luo H, Tracey D, Geller J, Fukami H, Miller DJ, Chen CA (2014) Mitochondrial Genome in the Scleractinia/Corallimorpharia Complex: Implications for Coral Phylogeny. Genome Biol Evol 6:1085–1086

    Article  Google Scholar 

  • Lin M, Moya A, Ying H, Chen CA, Cooke I, Ball EE, Foret S, Miller DJ (2017) Analyses of Corallimorpharian Transcriptomes Provide New Perspectives on the Evolution of Calcification in the Scleractinia (Corals). Genome Biology Evolution 9:150–160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mair M (2008) Oil, fire, and fate: the sinking of the USS Mississinewa (AO-59) in WWII by Japan’s secret weapon. SMJ Publishing, Platteville, Wisconsin, USA, p 642

    Google Scholar 

  • Miller, M.A., Pfeiffer, W., and Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE) 14 Nov. 2010, New Orleans, LA pp 1 - 8.

  • Mooney HA, Mack RN, McNeely JA, Neville LE, Schei PJ, Waage JK (eds) (2005) Invasive alien species: a new synthesis IUCN Scientific Committee on Problems of the Environment. Island Press, Washington DC, p 368

    Google Scholar 

  • Muhando CA, Kuguru BL, Wagner GM, Mbije NE, Ohman MC (2002) Environmental Effects on the Distribution of Corallimorphs in Tanzania. Ambio 31:558–561

    Article  PubMed  Google Scholar 

  • Nilkerd B, Swatdipong A, Salaenoi J, Tunkijjanukij S (2015) Pilot Survey of Corallimorpharian (Cnidaria) Diversity in the Gulf of Thailand. Kasetsart University Fisheries Research Bulletin 39:30–42

    Google Scholar 

  • Norström AV, Nyström M, Lokrantz J, Folke C (2009) Alternative states on coral reefs: beyond coral-macroalgal phase shifts. Mar Ecol Prog Ser 376:295–306

    Article  Google Scholar 

  • Nyström M (2006) Redundancy and response diversity of functional groups: implications for the resilience of coral reefs. AMBIO J Hum Environ 35:30–35

    Article  Google Scholar 

  • Ocaña O, den Hartog JC, Brito A (2017) Restoration of the genus Pseudocorynactis Den Hartog, 1980 and enmended diagnosis of the genera Corynactis Allman, 1846, Pseudocorynactis and Paracorynactis Ocaña, Den Hartog, Brito & Bos, 2010. Rev Acad Canar Cienc 29:9–20

    Google Scholar 

  • Oh RM, Neo ML, Yap NWL, Jain SS, Tan R, Chen CA, Huang D (2019) Citizen science meets integrated taxonomy to uncover the diversity and distribution of Corallimorpharia in Singapore. Raffles Bulletin of Zoology 67:306–321

    Google Scholar 

  • Price MR, Forsman ZH, Knapp IS, Toonen RJ, Hadfield MG (2016) The complete mitochondrial genome of Achatinella sowerbyana (Gastropoda: Pulmonata: Stylommatophora: Achatinellidae). Mitochondrial DNA Part B 1(1):666–668

    Article  PubMed  PubMed Central  Google Scholar 

  • Ratnasingham S, Hebert P (2007) Barcoding BOLD: The Barcode of Life Data System. Mol Ecol Notes 7:355–364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rambaut, Andrew. (2018) FigTree. http://tree.bio.ed.ac.uk/software/figtree/

  • Reichelt-Brushett AJ, Harrison PL (1999) The effect of Copper, Zinc, and Cadmium on Fertilization Success of Gametes from Scleractinian Reef Corals”. Mar Pollut Bull 38:182–187

    Article  CAS  Google Scholar 

  • Roff G, Doropoulos C, Zupan M, Rogers A, Steneck RS, Golbuu Y, Mumby PJ (2015) Phase shift facilitation following cyclone disturbance on coral reefs. Oecologia 178:1193–1203

    Article  PubMed  Google Scholar 

  • Sandin SA, Smith JE, De Martini EE, Dinsdale EA, Donner SD, Friedlander AM, Konotchick T, Malay M, Maragos JE, Obura D, Pantos O, Paulay G, Richie M, Rohwer F, Schroder RE, Walsh S, Jackson JB, Knowlton N, Sala E (2008) Baselines and degradation of Coral Reefs in the Northern Line Islands. PlosOne 3:e1548

    Article  CAS  Google Scholar 

  • Saville-Kent, W. (1893) The Great Barrier Reef of Australia: Its products and potentialities. London.

  • Spalding M, Burke L, Wood SA, Ashpole J, Hutchinson J, Ermgassen P (2017) Mapping the global value and distribution of coral reef tourism. Mar Policy 82:104–113

    Article  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toonen RJ, Puritz JB, Forsman ZH, Whitney JL, Fernandez-Silva I, Andrews KR, Bird CE (2013a) ezRAD: a simplified method for genomic genotyping in non-model organisms. PeerJ 1:e203. https://doi.org/10.7717/peerj.203

    Article  PubMed  PubMed Central  Google Scholar 

  • Toonen RJ, Wilhelm TA, Maxwell SM, Wagner D, Bowen BW, Sheppard CR, Taei SM, Teroroko T, Moffitt R, Gaymer CF, Morgan L (2013b) One size does not fit all: the emerging frontier in large-scale marine conservation. Mar Pollut Bull 77:7–10

    Article  CAS  PubMed  Google Scholar 

  • Veron JE, Odorico DM, Chen CA, Miller DJ (1996) Reassessing evolutionary relationships of scleractinian corals. Coral Reefs 15:1–9

    Article  Google Scholar 

  • Williams GJ, Knapp IS, Aeby GS, Davy SK (2011) Spatial and temporal patterns of scleractinian coral, soft coral, and zoanthid disease on a remote, near-pristine coral reef (Palmyra Atoll, central Pacific). Dis Aquat Org 94:89–100

    Article  Google Scholar 

  • Work TM, Aeby GS, Maragos JE (2008) Phase Shift from a Coral to a Corallimorph-Dominated Reef Associated with a Shipwreck on Palmyra Atoll. PLoS ONE 3:e2989

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Work TM, Aeby GS, Neal BP, Price NN, Conklin E, Pollock A (2018) Managing an invasive corallimorph at Palmyra Atoll National Wildlife Refuge, Line Islands, Central Pacific. Biol Invasions 20:2197–2208

    Article  Google Scholar 

  • Ziegler M, Eguíluz VM, Duarte CM, Voolstra CR (2018) Rare symbionts may contribute to the resilience of coral–algal assemblages. ISME J 12:161–172

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank the HIMB EPSCoR core facility and the University of Hawai‘i’s Advanced Studies in Genomics, Proteomics, and Bioinformatics facility for their assistance with DNA sequencing. This project was completed in fulfillment of Kaitlyn Jacobs’ master’s degree at UHM. KJ also gives a large thank you to the United States Fish and Wildlife Palmyra team for collaboration and sample collection, specifically Stefan Kropidlowski, Danielle Cantrell, the amazing volunteers, and Tim Clark for collection from Sāmoa. KJ wants to thank Thierry Work of the United States Geological Survey for background on the Palmyra outbreak and corallimorph tissue samples for practicing DNA extraction. We appreciate the individuals who provided thoughtful comments and suggestions, including the Editors and referees that helped to improve this manuscript. This research was supported by the University of Hawai‘i at Mānoa School of Life Science’s Edmondson Fund, and the Hawai‘i Institiute of Marine Biology’s Lord Scholarship (to KJ). The remaining financial support came from NSF-OA#1416889 and NOAA#NA19NOS4780196 to RJT. The views expressed herein are those of the authors and may not reflect the views of the USFWS or its sub-agencies.

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Jacobs, K.P., Hunter, C.L., Forsman, Z.H. et al. A phylogenomic examination of Palmyra Atoll’s corallimorpharian invader. Coral Reefs 41, 673–685 (2022). https://doi.org/10.1007/s00338-021-02143-5

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