Abstract
A 2013 study revealed that three morphologically distinct antipatharian genera (Dendrobathypathes, Lillipathes, Parantipathes) from the eastern North Pacific (ENP) are genetically indistinguishable using three mitochondrial and four nuclear markers (7,203 bp). To investigate whether this lack of molecular variability extends beyond three mitochondrial genes, we sequenced the complete mitogenome of a single representative within each genus. Dendrobathypathes was the only specimen from the 2013 study containing high molecular weight (HMW) DNA. In terms of geographic proximity to the ENP, the closest Lillipathes and Parantipathes yielding HMW DNA were from the central North Pacific near Hawai'i. Based on cox3-IGR-cox1, Lillipathes and Parantipathes each contained two variable sites and thus were not equivalent substitutes for specimens from the ENP. Nonetheless, variation was extremely low when comparing the mitogenomes, with 32 variable positions across 17,687 bp. Pairwise comparisons revealed 18 (Dendrobathypathes and Parantipathes) and 23 (Lillipathes and Parantipathes; Lillipathes and Dendrobathypathes) variable sites. An ML-based phylogenetic reconstruction using 13 protein-coding genes and two rRNAs revealed that the three North Pacific genera grouped in a clade with Atlantic Dendrobathypathes, while Atlantic Parantipathes spp. formed a sister clade. Previous research hypothesized that hybridization with subsequent introgression was responsible for the lack of variability among genera. Due to uniparental inheritance and lack of recombination, mtDNA cannot identify hybrids; however, finding Pacific Parantipathes grouping with Dendrobathypathes and Lillipathes rather than Atlantic Parantipathes suggests that the trigeneric complex has a unique evolutionary history. If high-resolution nuclear markers support hybridization, it will be important to elucidate the molecular mechanism that maintains three distinct morphological forms occurring in sympatry.
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Availability of data and material
Mitogenomic data are available in GenBank under accession numbers MZ520327 (Parantipathes cf. larix USNM-1404491), MZ520328 (Lillipathes cf. wingi USNM-1457355), and MZ520329 (Dendrobathypathes boutillieri USNM-1070762). The phylogenetic tree is available in TreeBASE under study number S28972.
Code availability
Our MitoFinder code is included under “Materials and methods.”
References
Allio, R., Schomaker-Bastos, A., Romiguier, J., Prosdocimi, F., Nabholz, B., & Delsuc, F. (2020). MitoFinder: Efficient automated large-scale extraction of mitogenomic data in target enrichment phylogenomics. Molecular Ecology Resources, 20(4), 892–905. https://doi.org/10.1111/1755-0998.13160
Baliński, A., Sun, Y., & Dzik, J. (2012). 470-Million-year-old black corals from China. Naturwissenschaften, 99(8), 645–653. https://doi.org/10.1007/s00114-012-0947-8
Barrett, N. J., Hogan, R., Allcock, L., Molodtsova, T. N., Hopkins, K. P., Wheeler, A. J., & Yesson, C. (2020). Phylogenetics and mitogenome organisation in black corals (Anthozoa: Hexacorallia: Antipatharia): An order-wide survey inferred from complete mitochondrial genomes. Frontiers in Marine Science, 7, 440. https://doi.org/10.3389/fmars.2020.00440
Bernt, M., Donath, A., Jühling, F., Externbrink, F., Florentz, C., Fritzsch, G., Pütz, J., Middendorf, M., & Stadler, P. F. (2013). MITOS: Improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution, 69(2), 313–319. https://doi.org/10.1016/j.ympev.2012.08.023
Bilewitch, J. P., & Degnan, S. M. (2011). A unique horizontal gene transfer event has provided the octocoral mitochondrial genome with an active mismatch repair gene that has potential for an unusual self-contained function. BMC Evolutionary Biology, 11(1), 1–15. https://doi.org/10.1186/1471-2148-11-228
Bo, M., Barucca, M., Biscotti, M. A., Brugler, M. R., Canapa, A., Canese, S., Iacono, C. L., & Bavestrello, G. (2018). Phylogenetic relationships of Mediterranean black corals (Cnidaria: Anthozoa: Hexacorallia) and implications for classification within the order Antipatharia. Invertebrate Systematics, 32(5), 1102–1110. https://doi.org/10.1071/IS17043
Bo, M., Canese, S., & Bavestrello, G. (2014). Discovering Mediterranean black coral forests: Parantipathes larix (Anthozoa: Hexacorallia) in the Tuscan Archipelago, Italy. Italian Journal of Zoology, 81(1), 112–125. https://doi.org/10.1080/11250003.2013.859750
Boch, C. A., DeVogelaere, A., Burton, E., King, C., Lord, J., Lovera, C., Litvin, S. Y., Kuhnz, L., & Barry, J. P. (2019). Coral translocation as a method to restore impacted deep-sea coral communities. Frontiers in Marine Science, 6, 540. https://doi.org/10.3389/fmars.2019.00540
Brickley, P. J., & Thomas, A. C. (2004). Satellite-measured seasonal and inter-annual chlorophyll variability in the Northeast Pacific and Coastal Gulf of Alaska. Deep Sea Research Part II: Topical Studies in Oceanography, 51(1–3), 229–245. https://doi.org/10.1016/j.dsr2.2003.06.003
Brook, G. (1889). Report on the Antipatharia. Report of the scientific results of the voyage of the H.M.S. ‘Challenger.’ Challenger Reports, Zoology, 32, 1–222.
Brugler, M. R., Opresko, D. M., & France, S. C. (2013). The evolutionary history of the order Antipatharia (Cnidaria: Anthozoa: Hexacorallia) as inferred from mitochondrial and nuclear DNA: Implications for black coral taxonomy and systematics. Zoological Journal of the Linnean Society, 169(2), 312–361. https://doi.org/10.1111/zoj.12060
Cairns, S. D. (2007). Deep-water corals: An overview with special reference to diversity and distribution of deep-water scleractinian corals. Bulletin of Marine Science, 81(3), 311–322.
Chan, P. P., & Lowe, T. M. (2019). tRNAscan-SE: Searching for tRNA genes in genomic sequences. In Gene Prediction (pp. 1–14). Humana, New York, NY. https://doi.org/10.1007/978-1-4939-9173-0_1
Combosch, D. J., Guzman, H. M., Schuhmacher, H., & Vollmer, S. V. (2008). Interspecific hybridization and restricted trans-Pacific gene flow in the Tropical Eastern Pacific Pocillopora. Molecular Ecology, 17(5), 1304–1312. https://doi.org/10.1111/j.1365-294X.2007.03672.x
Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: More models, new heuristics and parallel computing. Nature Methods, 9(8), 772–772. https://doi.org/10.1038/nmeth.2109
Eldredge, L. G., & Evenhuis, N. L. (2003). Hawaii’s biodiversity: A detailed assessment of the numbers of species in the Hawaiian Islands. Records of the Hawaii Biological Survey for 2001–2002. Bishop Museum Occasional Papers, 76, 1–28.
France, S. C., Rosel, P. E., & Ewann, J. (1996). DNA sequence variation of mitochondrial large-subunit rRNA. Molecular Marine Biology and Biotechnology, 5(1), 15–28.
Fukami, H., Budd, A. F., Paulay, G., Solé-Cava, A., Chen, C. A., Iwao, K., & Knowlton, N. (2004). Conventional taxonomy obscures deep divergence between Pacific and Atlantic corals. Nature, 427(6977), 832–835. https://doi.org/10.1038/nature02339
Fukami, H., & Knowlton, N. (2005). Analysis of complete mitochondrial DNA sequences of three members of the Montastraea annularis coral species complex (Cnidaria, Anthozoa, Scleractinia). Coral Reefs, 24(3), 410–417. https://doi.org/10.1007/s00338-005-0023-3
Gress, E., Opresko, D. M., Brugler, M. R., Wagner, D., Eeckhaut, I., & Terrana, L. (2020). Widest geographic distribution of a shallow and mesophotic antipatharian coral (Anthozoa: Hexacorallia): Antipathes grandis VERRILL, 1928 – confirmed by morphometric and molecular analyses. Marine Biodiversity Records, 13(1), 1–7. https://doi.org/10.1186/s41200-020-00195-0
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Systematic Biology, 59(3), 307–321. https://doi.org/10.1093/sysbio/syq010
Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52(5), 696–704. https://doi.org/10.1080/10635150390235520
Heim, P. K., Johnson, M. A., & O’Brien, J. J. (1992). The influence of the Alaskan Gyre on the coastal circulation in the Gulf of Alaska. Journal of Geophysical Research: Oceans, 97(C11), 17765–17775. https://doi.org/10.1029/92JC01260
Hellberg, M. E. (2006). No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evolutionary Biology, 6(1), 1–8. https://doi.org/10.1186/1471-2148-6-24
Hellberg, M. E., Prada, C., Tan, M. H., Forsman, Z. H., & Baums, I. B. (2016). Getting a grip at the edge: Recolonization and introgression in eastern Pacific Porites corals. Journal of Biogeography, 43(11), 2147–2159. https://doi.org/10.1111/jbi.12792
Herrera, S., & Shank, T. M. (2016). RAD sequencing enables unprecedented phylogenetic resolution and objective species delimitation in recalcitrant divergent taxa. Molecular Phylogenetics and Evolution, 100, 70–79. https://doi.org/10.1016/j.ympev.2016.03.010
Hitt, N. T., Sinclair, D. J., Fallon, S. J., Neil, H. L., Tracey, D. M., Komugabe-Dixson, A., & Marriott, P. (2020). Growth and longevity of New Zealand black corals. Deep Sea Research Part I: Oceanographic Research Papers, 162, 103298. https://doi.org/10.1016/j.dsr.2020.103298
Horowitz, J., Brugler, M. R., Bridge, T. C., & Cowman, P. F. (2020). Morphological and molecular description of a new genus and species of black coral (Cnidaria: Anthozoa: Hexacorallia: Antipatharia: Antipathidae: Blastopathes) from Papua New Guinea. Zootaxa, 4821(3):553–569. https://doi.org/10.11646/zootaxa.4821.3.7
Kane, C., Kosaki, R. K., & Wagner, D. (2014). High levels of mesophotic reef fish endemism in the Northwestern Hawaiian Islands. Bulletin of Marine Science, 90(2), 693–703.
Kitahara, M. V., Fukami, H., Benzoni, F., & Huang, D. (2016). The new systematics of Scleractinia: Integrating molecular and morphological evidence. In The Cnidaria, past, present and future (pp. 41–59). Springer, Cham. https://doi.org/10.1007/978-3-319-31305-4_4
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/molbev/msy096
Lauretta, D., & Penchaszadeh, P. E. (2017). Gigantic oocytes in the deep sea black coral Dendrobathypathes grandis (Antipatharia) from the Mar del Plata submarine canyon area (southwestern Atlantic). Deep Sea Research Part I: Oceanographic Research Papers, 128, 109–114. https://doi.org/10.1016/j.dsr.2017.08.011
Li, D., Liu, C. M., Luo, R., Sadakane, K., & Lam, T. W. (2015). MEGAHIT: An ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics, 31(10), 1674–1676. https://doi.org/10.1093/bioinformatics/btv033
MacIsaac, K. G., Best, M., Brugler, M. R., Kenchington, E. L. R., Anstey, L. J., & Jordan, T. (2013). Telopathes magna gen. nov., spec. nov.(Cnidaria: Anthozoa: Antipatharia: Schizopathidae) from deep waters off Atlantic Canada and the first molecular phylogeny of the deep-sea family Schizopathidae. Zootaxa, 3700(2):237–258. https://doi.org/10.11646/zootaxa.3700.2.3
McFadden, C. S., Quattrini, A. M., Brugler, M. R., Cowman, P. F., Dueñas, L. F., Kitahara, M. V., Paz-García, D. A., Reimer, J. D., & Rodríguez, E. (2021). Phylogenomics, origin and diversification of anthozoans (Phylum Cnidaria). Systematic Biology. https://doi.org/10.1093/sysbio/syaa103
Molodtsova, T. N. (2006). Black corals (Antipatharia: Anthozoa: Cnidaria) of the north-eastern Atlantic. Biogeography of the Atlantic seamounts, edited by: Mironov, AN, Gebruk, AV, and Southward, AJ, KMK Scientific Press, Moscow, pp.141–151.
Molodtsova, T. N., & Opresko, D. M. (2017). Black corals (Anthozoa: Antipatharia) of the clarion-clipperton fracture zone. Marine Biodiversity, 47(2), 349–365. https://doi.org/10.1007/s12526-017-0659-6
Opresko, D. M. (2002). Revision of the Antipatharia (Cnidaria: Anthozoa). Part II. Schizopathidae. Zoologische Mededelingen, 76, 411–442.
Opresko, D. M. (2005). New genera and species of antipatharian corals (Cnidaria: Anthozoa) from the North Pacific. Zoologische Mededelingen, 79, 129–165.
Opresko, D. M. (2015). New species of black corals (Cnidaria: Anthozoa: Antipatharia) from New Zealand and adjacent regions. New Zealand Journal of Zoology, 42(3), 145–164. https://doi.org/10.1080/03014223.2015.1051550
Opresko, D. M., Goldman, S. L., Johnson, R., Parra, K., Nuttall, M., Schmahl, G. P., & Brugler, M. R. (2020). Morphological and molecular characterization of a new species of black coral from Elvers Bank, north-western Gulf of Mexico (Cnidaria: Anthozoa: Hexacorallia: Antipatharia: Aphanipathidae: Distichopathes). Journal of the Marine Biological Association of the United Kingdom, 100(4), 559–566. https://doi.org/10.1017/S002531542000051X
Opresko, D. M., & Wagner, D. (2020). New species of black corals (Cnidaria: Anthozoa: Antipatharia) from deep-sea seamounts and ridges in the North Pacific. Zootaxa, 4868(4):543–559. https://doi.org/10.11646/zootaxa.4868.4.5
Pinzón, J. H., & LaJeunesse, T. C. (2011). Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology. Molecular Ecology, 20(2), 311–325. https://doi.org/10.1111/j.1365-294X.2010.04939.x
Pinzón, J. H., Sampayo, E., Cox, E., Chauka, L. J., Chen, C. A., Voolstra, C. R., & LaJeunesse, T. C. (2013). Blind to morphology: Genetics identifies several widespread ecologically common species and few endemics among Indo‐Pacific cauliflower corals (Pocillopora, Scleractinia). Journal of Biogeography, 40(8), 1595–1608.
Quattrini, A. M., Wu, T., Soong, K., Jeng, M. S., Benayahu, Y., & McFadden, C. S. (2019). A next generation approach to species delimitation reveals the role of hybridization in a cryptic species complex of corals. BMC Evolutionary Biology, 19(1), 1–19. https://doi.org/10.1186/s12862-019-1427-y
Rakka, M., Orejas, C., Maier, S. R., Van Oevelen, D., Godinho, A., Bilan, M., & Carreiro-Silva, M. (2020). Feeding biology of a habitat-forming antipatharian in the Azores Archipelago. Coral Reefs, 39(5), 1469–1482. https://doi.org/10.1007/s00338-020-01980-0
Ruiz-Ramos, D. V., Saunders, M., Fisher, C. R., & Baums, I. B. (2015). Home bodies and wanderers: Sympatric lineages of the deep-sea black coral Leiopathes glaberrima. PLoS One, 10(10), e0138989. https://doi.org/10.1371/journal.pone.0138989
Shearer, T. L., Van Oppen, M. J. H., Romano, S. L., & 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.x
Stampar, S. N., Maronna, M. M., Kitahara, M. V., Reimer, J. D., & Morandini, A. C. (2014). Fast-evolving mitochondrial DNA in Ceriantharia: A reflection of Hexacorallia paraphyly? PLoS One, 9(1), e86612. https://doi.org/10.1371/journal.pone.0086612
Stecher, G., Tamura, K., & Kumar, S. (2020). Molecular evolutionary genetics analysis (MEGA) for macOS. Molecular Biology and Evolution, 37(4), 1237–1239. https://doi.org/10.1093/molbev/msz312
Tapia-Guerra, J. M., Asorey, C. M., Easton, E. E., Wagner, D., Gorny, M., & Sellanes, J. (2021). First ecological characterization of whip black coral assemblages (Hexacorallia: Antipatharia) in the Easter Island Ecoregion. Southeastern Pacific. Frontiers in Marine Science, 8, 755898. https://doi.org/10.3389/fmars.2021.755898
Tazioli, S., Bo, M., Boyer, M., Rotinsulu, H., & Bavestrello, G. (2007). Ecological observations of some common antipatharian corals in the marine park of Bunaken (North Sulawesi, Indonesia). Zoological Studies, 46(2), 227–241.
Terrana, L., Flot, J. F., & Eeckhaut, I. (2021). ITS1 variation among Stichopathes cf. maldivensis (Hexacorallia: Antipatharia) whip black corals unveils conspecificity and population connectivity at local and global scales across the Indo-Pacific. Coral Reefs, 40(2), 521–533. https://doi.org/10.1007/s00338-020-02049-8
Wagner, D., Luck, D. G., & Toonen, R. J. (2012). The biology and ecology of black corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia). Advances in Marine Biology, 63, 67–132. https://doi.org/10.1016/B978-0-12-394282-1.00002-8
Wagner, D., Waller, R. G., & Toonen, R. J. (2011). Sexual reproduction of Hawai’ian black corals, with a review of the reproduction of antipatharians (Cnidaria: Anthozoa: Hexacorallia). Invertebrate Biology, 130(3), 211–225. https://doi.org/10.1111/j.1744-7410.2011.00233.x
Acknowledgements
The data in this paper were analyzed as part of a Molecular Ecology Techniques course (BIOL B499) at the University of South Carolina Beaufort. Sequencing was conducted at the New York Genome Center using funds provided to MRB through a Cycle 47 PSC-CUNY Research Award (#69191-00-47). Financial support was provided to MRB by the Port Royal Sound Foundation and to the Ocean Genome Legacy Center of Northeastern University by a grant from the National Fish and Wildlife Foundation. Resources purchased with funds from the NSF FSML program (DBI 1722553, to Northeastern University) were used to generate data for this manuscript. MRB is a Research Associate at the American Museum of Natural History and the Smithsonian Institution’s National Museum of Natural History and gratefully acknowledges these affiliations.
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- Cycle 47 PSC-CUNY Research Award (#69191–00-47) for DNA sequencing to MRB. - Port Royal Sound Foundation to MRB. - National Fish and Wildlife Foundation to the Ocean Genome Legacy Center of Northeastern University. - NSF FSML program (DBI 1722553) to Northeastern University.
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Conceived of study: MRB. DNA extraction, DNA quantification, and shipping samples: HJAM, DLD. Data analysis: YMBB, IW, KMN, JJR, KM, KMC, SS, SNM, MSB, JAF, ANW, KEM, TN, HP, MRB. Data interpretation: YMBB, IW, JH, DTP, MRB. Submitted data to GenBank: YMBB, IW, JJR, KM, KMC, MRB. Significant intellectual contributions: JH, DTP. Wrote original draft of manuscript: YMBB, IW, JH, HJAM, MRB. Revised manuscript: all authors.
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Yessenia M. Bledsoe-Becerra, Iesha S. Whittaker, Katherine Medina Naranjo, Jicayla Johnson-Rosemond, Kristen H. Mullins, Karena M. Cunningham, Suchir Shetty, Samuel N. Messinides, Melinda S. Behney, Jessica A. Fehsal, Ashley N. Watson, Kaitlyn E. McKnight, and Teresa W. Nasiadka are undergraduates.
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Bledsoe-Becerra, Y.M., Whittaker, I.S., Horowitz, J. et al. Mitogenomics reveals low variation within a trigeneric complex of black corals from the North Pacific Ocean. Org Divers Evol 22, 343–353 (2022). https://doi.org/10.1007/s13127-021-00537-5
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DOI: https://doi.org/10.1007/s13127-021-00537-5