Abstract
Identifying genetic connectivity and discrete population boundaries is an important objective for management of declining Caribbean reef-building corals. A double digest restriction-associated DNA sequencing protocol was utilized to generate 321 single nucleotide polymorphisms to estimate patterns of horizontal and vertical gene flow in the brooding Caribbean plate coral, Agaricia lamarcki. Individual colonies (n = 59) were sampled from eight locations throughout southwestern Puerto Rico from six shallow (~ 10–20 m) and two mesophotic habitats (~ 30–40 m). Descriptive summary statistics (fixation index, F ST), analysis of molecular variance, and analysis through landscape and ecological associations and discriminant analysis of principal components estimated high population connectivity with subtle subpopulation structure among all sampling localities.
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Appeldoorn RS, Hensley DA, Shapiro DY, Kioroglou S, Sanderson BG (1994) Egg dispersal in a Caribbean coral reef fish, Thalassoma bifasciatum. II. Dispersal off the reef platform. Bull Mar Sci 54:271–280
Appeldoorn RS, Ballantine D, Bejarano I, Carlo M, Nemeth M, Otero E, Pagan F, Ruiz H, Schizas N, Sherman C, Weil E (2016) Mesophotic coral ecosystems under anthropogenic stress: a case study at Ponce, Puerto Rico. Coral Reefs 35:63–75
Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O, Wilson MC, Piel J, Ashoor H, Bougouffa S, Bajic VB, Ryu T, Ravasi T, Bayer T, Micklem G, Kim H, Bhak J, LaJeunesse TC, Voolstra CR (2016) Genomes of coral dinoflagellate symbionts highlight evolutionary adaptions conducive to a symbiotic lifestyle. Sci Rep 6:39734
Aronson R, Bruckner A, Moore J, Precht B, Weil E (2008) Agaricia lamarcki. The IUCN red list of threatened species 2008: e.T132970A3515504
Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Creski WA, Johnson EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3:e3376
Benestan L, Gosselin T, Perrier C, Sainte-Marie B, Rochette R, Bernatchez L (2015) RAD genotyping reveals fine-scale genetic structuring and provides powerful population assignment in a widely distributed marine species, the American lobster (Homarus americanus). Mol Ecol 24:3299–3315
Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the “deep reef refugia” hypothesis: focus on Caribbean reefs. Coral Reefs 29:1–19
Bongaerts P, Riginos C, Brunner R, Englebert N, Smith SR, Hoegh-Guldberg O (2017) Deep reefs are not universal refuges: reseeding potential varies among coral species. Sci Adv 3:e1602373
Bongaerts P, Frade PR, Ogier JJ, Hay KB, van Bleijswijk J, Englebert N, Vermeij MJ, Bak RP, Visser PM, Hoegh-Guldberg O (2013) Sharing the slope: depth partitioning of agariciid corals and associated Symbiodinium across shallow and mesophotic habitats (2–60 m) on a Caribbean reef. BMC Evol Biol 13:205
Brazeau DA, Lesser MP, Slattery M (2013) Genetic structure in the coral, Montastraea cavernosa: assessing genetic differentiation among and within mesophotic reefs. PLoS One 8:e65845
Capella J, Laboy E (2003) Environmental settings. In: Field R (ed) Jobos Bay estuarine profile. Jobos Bay NERR, Puerto Rico, pp 14–39
Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortes J, Delbeek JC, DeVantier L, Edgar GJ, Edwards AJ, Fenner D, Guzman HM, Hoeksema BW, Hodgson G, Johan O, Licuanan WY, Veron JEN, Wallace C, Weil E, Wood E (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 25:560–563
Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140
Davey JL, Blaxter MW (2010) RADseq: Next-generation population genetics. Brief Funct Genomics 9:416–423
Drury C, Dale KE, Panlilio JM, Miller SV, Lirman D, Larson EA, Bartels E, Crawford DL, Oleksiak MF (2016) Genomic variation among populations of threatened coral: Acropora cervicornis. BMC Genomics 17:286
Frichot E, François O (2015) LEA: an R package for landscape and ecological association studies. Methods Ecol Evol 6:925–929
Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960
Goodbody-Gringley G, Woollacott RM, Giribet G (2011) Population structure and connectivity in the Atlantic scleractinian coral Montastraea cavernosa (Linnaeus, 1767). Mar Ecol 33:32–48
Goudet J (2005) Hierfstat, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186
Guinotte JM, Orr J, Cairns S, Freiwald A, Morgan L, George R (2006) Will human-induced changes in seawater chemistry alter the distribution of deep-sea scleractinian corals? Front Ecol Environ 4:141–146
Harvell CD, Altizer S, Cattadori IM, Harrington L, Weil E (2009) Climate change and wildlife diseases: when does the host matter the most? Ecology 90:912–920
Hinderstein LM, Marr JCA, Martinez FA, Dowgiallo MJ, Puglise KA, Pyle RL, Zawada DG, Appeldoorn R (2010) Theme section on “Mesophotic Coral Ecosystems: Characterization, Ecology, and Management”. Coral Reefs 29:247–251
Hohenlohe PA, Amish SJ, Catchen JM, Allendorf FW, Luikart G (2011) Next-generation RAD sequencing identifies thousands of SNPs for assessing hybridization between rainbow and westslope cutthroat trout. Mol Ecol Resour 11:117–122
Jombart T, Ahmed I (2011) Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071
Kahng SE, Copus JM, Wagner D (2014) Recent advances in the ecology of mesophotic coral ecosystems (MCEs). Curr Opin Environ Sustain 7:72–81
Kahng SE, Copus JM, Wagner D (2017) Mesophotic coral ecosystems. In: Rossi S, Bramanti L, Gori A, Orejas C (eds) Marine animal forests: the ecology of benthic biodiversity hotspots. Springer International Publishing, Cham, Switzerland, pp 185–206
Kahng SE, Garcia-Sais JR, Spalding HL, Brokovich E, Wagner D, Weil E (2010) Community ecology of mesophotic coral reef ecosystems. Coral Reefs 29:255–275
Langmead B, Salzberg S (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359
Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Bio Ecol 375:1–8
Lin S, Cheng S, Song B, Zhong X, Lin X, Li W, Li L, Zhang Y, Zhang H, Ji Z, Cai M, Zhuang Y, Shi X, Lin L, Wang L, Wng Z, Liu X, Yu S, Zeng P, Hao H, Zou Q, Chen C, Li Y, Wang Y, Xu C, Meng S, Xu X, Wang J, Yang H, Campbell DA, Sturn NR, Dangenais-Bellefeuille S, Morse D (2015) The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science 350:691–964
Lucas MQ, Stat M, Smith MC, Weil E, Schizas NV (2016) Symbiodinium (internal transcribed spacer 2) diversity in the coral host Agaricia lamarcki (Cnidaria: Scleractinia) between shallow and mesophotic reefs in the northern Caribbean (20–70m). Mar Ecol 37:1079–1087
Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nature Rev Genet 4:981–994
McCook LJ, Almany GR, Berumen ML, Day JC, Green AL, Jones GP, Leis JM, Planes S, Russ GR, Sale PF, Thorrold SR (2009) Management under uncertainty: guidelines for incorporating connectivity into the protection of coral reefs. Coral Reefs 28:353–366
Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: Two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794
Miller M, Dunham J, Amores A, Cresko W, Johnson E (2007) Genotyping using restriction site associated DNA (RAD) markers. Genome Res 17:240–248
Milne H, Haime J (1851) Recherches sur les polypiers. Mémoire 6. Monographie des Fongides. Ann Sci Nat Zool 15:73–144
Morse DE, Hooker N, Morse ANC, Jensen RA (1988) Control of larval metamorphosis and recruitment in sympatric agariciid corals. J Exp Mar Bio Ecol 116:193–217
Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7:e37135
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Reitzel AM, Herrera S, Layden MJ, Martindale MQ, Shank TM (2013) Going where traditional markers have not gone before: utility of and promise for RAD sequencing in marine invertebrate phylogeography and population genomics. Mol Ecol 22:2953–2970
Sammarco PW, Brazeau DA, Sinclair J (2012) Genetic connectivity in scleractinian corals across the northern Gulf of Mexico: oil/gas platforms, and relationship to the Flower Garden Banks. PLoS One 7:25–29
Serrano XM, Baums IB, Smith TB, Jones RJ, Shearer TL, Baker AC (2016) Long distance dispersal and vertical gene flow in the Caribbean brooding coral Porites astreoides. Sci Rep 6:21619
Serrano XM, Baums IB, O’Reilly K, Smith TB, Jones RJ, Shearer TL, Nunes FL, Baker AC (2014) Geographic differences in vertical connectivity in the Caribbean coral Montastraea cavernosa despite high levels of horizontal connectivity at shallow depths. Mol Ecol 23:4226–4240
Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpakdee S, Koyanagi R, Takeuchi T, Hisata K, Tanaka M, Fujiwara M, Hamada M, Seidi A, Fujie M, Usami T, Goto H, Yamasaki S, Arakaki N, Suzuki Y, Sugano S, Toyoda A, Kuroki Y, Fujiyama A, Medina M, Coffroth MA, Bhattacharya D, Satoh N (2013) Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr Biol 23:1399–1408
Slattery M, Lesser MP, Brazeau D, Stokes MD, Leichter JJ (2011) Connectivity and stability of mesophotic coral reefs. J Exp Mar Bio Ecol 408:32–41
Smith TB, Gyory J, Brandt ME, Miller WJ, Jossart J, Nemeth RS (2015) Caribbean mesophotic coral ecosystems are unlikely climate change refugia. Glob Chang Biol 8:2756–2765
Toonen RJ, Puritz JB, Forsman ZH, Whitney JL, Fernandez-Silva I, Andrews KR, Bird CE (2013) ezRAD: a simplified method for genomic genotyping in non-model organisms. PeerJ 1:e203
Toonen RJ, Andrews KR, Baums IB, Bird CE, Concepcion GT, Daly-Engel TS, Eble JA, Faucci A, Gaither MR, Lacchei M, Puritz JB, Schultz JK, Skillings DJ, Timmers MA, Bowen BW (2011) Defining boundaries for ecosystem-based management: a multispecies case study of marine connectivity across the Hawaiian Archipelago. J Mar Biol 2011:460173
Van Moorsel GWNM (1983) Reproductive strategies in two closely related stony corals (Agaricia, Scleractinia). Mar Ecol Prog Ser 13:273–283
Van Oppen MJH, Bongaerts P, Underwood JN, Peplow LM, Cooper TF (2011) The role of deep reefs in shallow reef recovery: an assessment of vertical connectivity in a brooding coral from west and east Australia. Mol Ecol 20:1647–1660
Vollmer SV, Palumbi SR (2007) Restricted gene flow in the Caribbean staghorn coral Acropora cervicornis: implications for the recovery of endangered reefs. J Hered 98:40–50
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
Acknowledgements
We thank Ivonne Bejarano, Milton Carlo, Michael Nemeth, Hector Ruiz, Clark Sherman, Evan Tuohy, Orlando Espinosa and Jaaziel Garcia for assistance in specimen collection. We acknowledge the constructive suggestions by Pim Bongaerts. This work was supported by the National Oceanic and Atmospheric Administration’s Center for Sponsored Coastal Ocean Research (NA06NOS4780190), through the Caribbean Coral Reef Institute and Puerto Rico Sea Grant Project # R-101-1-14 awarded to NVS. We thank the ReFuGe 2020 Consortium, (C. Xin, P. Lundgren, C.R. Voolstra) for sharing unpublished data of Symbiodinium genomes with us. NH was the recipient of Sea Grant Puerto Rico SEED money (PD-313). Research permits were obtained from the Department of Natural and Environmental Resources, Puerto Rico (O-VS-PVS15-MA-00017-29092014).
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Hammerman, N.M., Rivera-Vicens, R.E., Galaska, M.P. et al. Population connectivity of the plating coral Agaricia lamarcki from southwest Puerto Rico. Coral Reefs 37, 183–191 (2018). https://doi.org/10.1007/s00338-017-1646-x
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DOI: https://doi.org/10.1007/s00338-017-1646-x