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Population genetic structure of the broadcast spawning coral, Montastraea cavernosa, demonstrates refugia potential of upper mesophotic populations in the Florida Keys

Abstract

In the Florida Keys, coral cover on shallow reef systems (0–30 m) has declined over the past several decades, punctuated by severe losses during coral disease outbreaks and bleaching events. However, certain areas within the Florida Keys, especially the Dry Tortugas and many upper mesophotic habitats (30–60 m), have maintained relatively healthy coral communities, even in the face of recent severe and widespread coral disease outbreaks. Relatively little is known about the genetic connectivity of corals among these sites or the potential for mesophotic sites to act as refugia by contributing to metapopulation recovery and persistence. Using a paired shallow and upper mesophotic sampling design, we assessed the genetic connectivity of a dominant, broadcast spawning coral species, Montastraea cavernosa, across the Northern and Southern Dry Tortugas, Lower Florida Keys, and Upper Florida Keys. A genetic dataset based on a suite of > 9000 single-nucleotide polymorphism loci indicated that the level of vertical genetic connectivity between paired shallow and upper mesophotic populations varied significantly based on location. Shallow and upper mesophotic M. cavernosa populations in the Northern Dry Tortugas and the Upper Keys were genetically similar. In contrast, populations were significantly differentiated across depth in the Lower Keys and Southern Dry Tortugas. While upper mesophotic populations in the Lower Keys and Southern Dry Tortugas were distinct from their shallow counterparts, there was evidence of relatively high levels of genetic connectivity to both the shallow and upper mesophotic populations downstream in the Upper Keys. These results suggest that while vertical connectivity between paired shallow and mesophotic populations can vary, certain upper mesophotic populations may fill an important role in maintaining coral metapopulations throughout the Florida Keys and should be considered in future management strategies.

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References

  1. 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 adaptations conducive to a symbiotic lifestyle. Sci Rep 6:39734

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  2. Aronson RB, Precht WF (2001) White-band disease and the changing face of Caribbean coral reefs. Hydrobiologia 460:25–38

    Article  Google Scholar 

  3. Baums IB, Baker AC, Davies SW, Grottoli AG, Kenkel CD, Kitchen SA, Kuffner IB, LaJeunesse TC, Matz MV, Miller MW, Parkinson JE, Shantz AA (2019) Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic. Ecol Appl 29:e01978

    PubMed  PubMed Central  Article  Google Scholar 

  4. Baums IB, Paris CB, Chérubin LM (2010) A bio-oceanographic filter to larval dispersal in a reef-building coral. Limnol Oceanogr 51:1969–1981

    Article  Google Scholar 

  5. Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the “deep reef refugia” hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327

    Article  Google Scholar 

  6. Budd AF, Nunes FLD, Weil E, Pandolfi JM (2012) Polymorphism in a common Atlantic reef coral (Montastraea cavernosa) and its long-term evolutionary implications. Evol Ecol 26:265–290

    Article  Google Scholar 

  7. Burman SG, Aronson RB, Van WR (2012) Biotic homogenization of coral assemblages along the Florida reef tract. Mar Ecol Prog Ser 467:89–96

    Article  Google Scholar 

  8. Devlin-Durante MK, Baums IB (2017) Genome-wide survey of single-nucleotide polymorphisms reveals fine-scale population structure and signs of selection in the threatened Caribbean elkhorn coral Acropora Palmata. Peerj 5:e4077

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  9. Dodge D, Studivan M, Eckert R, Chei E, Beal J, Voss J (2020) Population structure of the scleractinian coral Montastraea cavernosa in southeast Florida. Bull Mar Sci 96:767–782

    Article  Google Scholar 

  10. Drury C, Pérez Portela R, Serrano XM, Oleksiak M, Baker AC (2020) Fine-scale structure among mesophotic populations of the great star coral Montastraea cavernosa revealed by SNP genotyping. Ecol Evol 10:6009–6019

    PubMed  PubMed Central  Article  Google Scholar 

  11. Drury C, Schopmeyer S, Goergen E, Bartels E, Nedimyer K, Johnson M, Maxwell K, Galvan V, Manfrino C, Lirman D (2017) Genomic patterns in Acropora cervicornis show extensive population structure and variable genetic diversity. Ecol Evol 7:6188–6200

    PubMed  PubMed Central  Article  Google Scholar 

  12. Eckert RJ, Studivan MS, Voss JD (2019) Populations of the coral species Montastraea cavernosa on the Belize Barrier Reef lack vertical connectivity. Sci Rep 9:7200

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  13. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    CAS  PubMed  Article  Google Scholar 

  14. FKNMS, FDEP (2018) Case definition: Stony coral tissue loss disease. https://floridadep.gov/rcp/coral/documents/stony-coral-tissue-loss-disease-sctld-case-definition

  15. Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993

    PubMed  PubMed Central  Article  Google Scholar 

  16. Frys C, Saint-Amand A, Le Hénaff M, Figueiredo J, Kuba A, Walker B, Lambrechts J, Vallaeys V, Vincent D, Hanert E (2020) Fine-scale coral connectivity pathways in the Florida reef tract: implications for conservation and restoration. Front Mar Sci 7:312

    Article  Google Scholar 

  17. Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960

    CAS  PubMed  Article  Google Scholar 

  18. Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2005) Hurricanes and Caribbean coral reefs: impacts, recovery patterns, and role in long-term decline. Ecology 86:174–184

    Article  Google Scholar 

  19. Gil-Agudelo DL, Cintra-Buenrostro CE, Brenner J, González-Díaz P, Kiene W, Lustic C, Pérez-España H (2020) Coral reefs in the Gulf of Mexico large marine ecosystem: conservation status, challenges, and opportunities. Front Mar Sci 6:807

    Article  Google Scholar 

  20. Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Glob Chang Biol 2:495–509

    Article  Google Scholar 

  21. Goodbody-Gringley G, Woollacott RM, Giribet G (2012) Population structure and connectivity in the Atlantic scleractinian coral Montastraea cavernosa (Linnaeus, 1767). Mar Ecol 33:32–48

    CAS  Article  Google Scholar 

  22. Gordon A, Hannon G (2010) FASTX-Toolkit. FASTQ/A short-reads pre-processing tools. http://hannonlab.cshl.edu/fastx_toolkit/

  23. Hagedorn M, Page CA, O’Neil K, Flores DM, Tichy L, Chamberland VF, Lager C, Zuchowicz N, Lohr K, Blackburn H, Vardi T, Moore J, Moore T, Vermeij MJA, Marhaver KL (2018) Successful demonstration of assisted gene flow in the threatened coral Acropora palmata across genetically-isolated Caribbean populations using cryopreserved sperm. bioRxiv 492447. https://doi.org/10.1101/492447

  24. Haskell B, Leeworthy V, Wiley P, Beuttler T, Haflich M, Delaney J, Richards B, Franklin E (2000) Tortugas Ecological Reserve: final supplemental environmental impact statement/final supplemental management plan. Silver Spring, MD

  25. Jaap WC, Szmant A, Jaap K, Dupont J, Clarke R, Somerfield P, Ault J S, Bohnsack James A, Kellison Steven G, Todd Kellison G (2008) A perspective on the biology of Florida Keys coral reefs. In: Riegl BM, Dodge RE (eds) Coral Reefs USA 1. Springer, Netherlands, Dordrecht, pp 75–125

    Chapter  Google Scholar 

  26. Joyner JL, Sutherland KP, Kemp DW, Berry B, Griffin A, Porter JW, Amador MHB, Noren HKG, Lipp EK (2015) Systematic analysis of white pox disease in Acropora palmata of the Florida keys and role of Serratia marcescens. Appl Environ Microbiol 81:4451–4457

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  27. Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281

    Article  Google Scholar 

  28. Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  29. Korneliussen TS, Albrechtsen A, Nielsen R (2014) ANGSD: Analysis of Next Generation Sequencing Data. BMC Bioinformatics 15:356

    PubMed  PubMed Central  Article  Google Scholar 

  30. Kourafalou VH, Androulidakis YS, Kang H, Smith RH, Valle-Levinson A (2018) Physical connectivity between Pulley Ridge and Dry Tortugas coral reefs under the influence of the Loop Current/Florida Current system. Prog Oceanogr 165:75–99

    Article  Google Scholar 

  31. Kramer KL, Heck KL (2007) Top-down trophic shifts in Florida Keys patch reef marine protected areas. Mar Ecol Prog Ser 349:111–123

    Article  Google Scholar 

  32. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. Lapointe BE, Brewton RA, Herren LW, Porter JW, Hu C (2019) Nitrogen enrichment, altered stoichiometry, and coral reef decline at Looe Key, Florida Keys, USA: a 3-decade study. Mar Biol 166:108

    CAS  Article  Google Scholar 

  34. Lessios HA, Robertson DR, Cubit JD (1984) Spread of Diadema mass mortality through the Caribbean. Science 226:335–337

    CAS  PubMed  Article  Google Scholar 

  35. 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. Evolution 58:308–323

    PubMed  Article  Google Scholar 

  36. Li Y-L, Liu J-X (2018) StructureSelector: A web-based software to select and visualize the optimal number of clusters using multiple methods. Mol Ecol Resour 18:176–177

    PubMed  Article  Google Scholar 

  37. Liu H, Stephens TG, González-Pech RA, Beltran VH, Lapeyre B, Bongaerts P, Cooke I, Aranda M, Bourne DG, Forêt S, Miller DJ, van Oppen MJH, Voolstra CR, Ragan MA, Chan CX (2018) Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis. Commun Biol 1:95

    PubMed  PubMed Central  Article  Google Scholar 

  38. Manzello DP (2015) Rapid recent warming of coral reefs in the Florida Keys. Sci Rep 5:16762

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  39. Manzello DP, Matz MV, Enochs IC, Valentino L, Carlton RD, Kolodziej G, Serrano X, Towle EK, Jankulak M (2019) Role of host genetics and heat-tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming. Glob Chang Biol 25:1016–1031

    Article  PubMed  PubMed Central  Google Scholar 

  40. Mcleod E, Anthony KRN, Mumby PJ, Maynard J, Beeden R, Graham NAJ, Heron SF, Hoegh-Guldberg O, Jupiter S, MacGowan P, Mangubhai S, Marshall N, Marshall PA, McClanahan TR, Mcleod K, Nyström M, Obura D, Parker B, Possingham HP, Salm RV, Tamelander J (2019) The future of resilience-based management in coral reef ecosystems. J Environ Manage 233:291–301

    PubMed  Article  Google Scholar 

  41. Muller EM, Sartor C, Alcaraz NI, van Woesik R (2020) Spatial epidemiology of the Stony-Coral-Tissue-Loss Disease in Florida. Front Mar Sci 7:11

    Article  Google Scholar 

  42. Nunes F, Norris RD, Knowlton N (2009) Implications of isolation and low genetic diversity in peripheral populations of an amphi-Atlantic coral. Mol Ecol 18:4283–4297

    CAS  PubMed  Article  Google Scholar 

  43. Oksanen J, F. Guillaume Blanchet RK, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, M. Henry H. Stevens HW (2019) Vegan: community ecology package

  44. Olascoaga MJ, Miron P, Paris C, Pérez-Brunius P, Pérez-Portela R, Smith RH, Vaz A (2018) Connectivity of Pulley Ridge with remote locations as inferred from satellite-tracked drifter trajectories. J Geophys Res Ocean 123:5742–5750

    Article  Google Scholar 

  45. Pembleton LW, Cogan NOI, Forster JW (2013) StAMPP: An R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Mol Ecol Resour 13:946–952

    CAS  PubMed  Article  Google Scholar 

  46. Porter JW, Dustan P, Jaap WC, Patterson KL, Kosmynin V, Meier OW, Patterson ME, Parsons M (2001) Patterns of spread of coral disease in the Florida Keys. Hydrobiologia 460:1–24

    Article  Google Scholar 

  47. Precht W (2019) Failure to respond to a coral disease outbreak: potential costs and consequences. PeerJ Prepr. https://doi.org/10.7287/peerj.preprints.27860v2

  48. Puechmaille SJ (2016) The program structure does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Mol Ecol Resour 16:608–627

    PubMed  Article  Google Scholar 

  49. R Core Team (2019) R: A language and environment for statistical computing

  50. Reed JK (1985) Deepest distribution of Atlantic hermaptypic corals discovered in the Bahamas. Proc Fifth Int Coral Reef Congr 6:249–254

    Google Scholar 

  51. Reed J, Farrington S, Harter S, Moe H, Hanisak D, David A (2015) Characterization of the mesophotic benthic habitat and fish assemblages from ROV dives on Pulley Ridge and Tortugas during 2014 R/V Walton Smith Cruise

  52. Riegl B, Piller WE (2003) Possible refugia for reefs in times of environmental stress. Int J Earth Sci 92:520–531

    Article  Google Scholar 

  53. Rippe JP, Dixon G, Fuller ZL, Liao Y, Matz M (2021) Environmental specialization and cryptic genetic divergence in two massive coral species from the Florida Keys Reef Tract. Mol Ecol. https://doi.org/10.1111/mec.15931

  54. Rippe JP, Matz MV, Green EA, Medina M, Khawaja NZ, Pongwarin T, Pinzón CJH, Castillo KD, Davies SW (2017) Population structure and connectivity of the mountainous star coral, Orbicella faveolata, throughout the wider Caribbean region. Ecol Evol 7:9234–9246

    PubMed  PubMed Central  Article  Google Scholar 

  55. Roth L, Kramer PR, Doyle E, O’Sullivan C (2020) Caribbean SCTLD dashboard. www.agrra.org

  56. Ruzicka RR, Colella MA, Porter JW, Morrison JM, Kidney JA, Brinkhuis V, Lunz KS, MacAulay KA, Bartlett LA, Meyers MK, Colee J (2013) Temporal changes in benthic assemblages on Florida Keys reefs 11 years after the 1997/1998 El Niño. Mar Ecol Prog Ser 489:125–141

    Article  Google Scholar 

  57. Schopmeyer SA, Lirman D, Bartels E, Byrne J, Gilliam DS, Hunt J, Johnson ME, Larson EA, Maxwell K, Nedimyer K, Walter C (2012) In situ coral nurseries serve as genetic repositories for coral reef restoration after an extreme cold-water event. Restor Ecol 20:696–703

    Article  Google Scholar 

  58. Serrano X, Baums IB, O’Reilly K, Smith TB, Jones RJ, Shearer TL, Nunes FLD, 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

    CAS  PubMed  Article  Google Scholar 

  59. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. Sharp W, Maxwell K, Smith K, Hunt J (2020) Investigating the ongoing coral disease outbreak in the Florida Keys: continued SCTLD monitoring at middle and lower Florida Keys, experimental coral restoration of SCTLD-susceptible coral species, and assessing the prevalence of SCTLD on intermediate reef habitat

  61. Shoguchi E, Beedessee G, Hisata K, Tada I, Narisoko H, Satoh N, Kawachi M, Shinzato C (2021) A new dinoflagellate genome illuminates a conserved gene cluster involved in sunscreen biosynthesis. Genome Biol Evol 13:1–7

    CAS  Article  Google Scholar 

  62. Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpakdee S, Koyanagi R, Takeuchi T, Hisata K, Tanaka M, Fujiwara M (2013) Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr Biol 23:1399-1408 

    Article  PubMed  Google Scholar 

  63. Skotte L, Korneliussen TS, Albrechtsen A (2013) Estimating individual admixture proportions from next generation sequencing data. Genetics 195:693–702

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. Studivan MS, Voss JD (2018) Population connectivity among shallow and mesophotic Montastraea cavernosa corals in the Gulf of Mexico identifies potential for refugia. Coral Reefs 37:1183–1196

    Article  Google Scholar 

  65. Sturm A (2020) Montastraea cavernosa DNA extraction with dispersion buffer. https://doi.org/10.5281/zenodo.3836665

  66. Sturm AB, Eckert RJ, González Méndez, Juliett González-Díaz P, Voss JD (2020) Population genetic structure of the great star coral, Montastraea cavernosa, across the Cuban archipelago with comparisons between microsatellite and SNP markers. Sci Rep 10:15432

  67. Szmant AM (1991) Sexual reproduction by the Caribbean reef corals Montastrea annularis and M. cavernosa. Mar Ecol Prog Ser 74:13–25

    Article  Google Scholar 

  68. Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28:33–36

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  69. Valle-Levinson A, Kourafalou VH, Smith RH, Androulidakis Y (2020) Flow structures over mesophotic coral ecosystems in the eastern Gulf of Mexico. Cont Shelf Res 207:104219

    Article  Google Scholar 

  70. Vaz AC, Paris CB, Olascoaga MJ, Kourafalou VH, Kang H, Reed JK (2016) The perfect storm: match-mismatch of bio-physical events drives larval reef fish connectivity between Pulley Ridge mesophotic reef and the Florida Keys. Cont Shelf Res 125:136–146

    Article  Google Scholar 

  71. Villemereuil P, Gaggiotti OE (2015) A new FST-based method to uncover local adaptation using environmental variables. Methods Ecol Evol 6:1248–1258

    Article  Google Scholar 

  72. Vize PD (2006) Deepwater broadcast spawning by Montastraea cavernosa, Montastraea franksi, and Diploria strigosa at the Flower Garden Banks, Gulf of Mexico. Coral Reefs 25:169–171

    Article  Google Scholar 

  73. Wang S, Meyer E, McKay JK, Matz MV (2012) 2b-RAD: a simple and flexible method for genome-wide genotyping. Nat Methods 9:808–810

    CAS  PubMed  Article  Google Scholar 

  74. Wright RM, Aglyamova GV, Meyer E, Matz MV (2015) Gene expression associated with white syndromes in a reef building coral, Acropora hyacinthus. BMC Genomics 16:371

    CAS  Google Scholar 

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Acknowledgements

We are grateful for the participants on the 2019 FAU Harbor Branch CIOERT research cruise Mesophotic Coral Reefs: Connectivity and Health in the FKNMS and Pulley Ridge including the authors and J. Reed, S. Pomponi, M.D. Hanisak, S. Farrington, I. Combs, M. Conkling, M.C. Diaz, K. Beckett, D. Liberatore, M. Studivan, E. Shilling, M. McCallister, C. Haymaker, and J. Ruggiero. We thank J. White and E. Glidden from the Undersea Vehicle Program at University of North Carolina at Wilmington who provided remotely operated vehicle expertise to help identify target sites, J. Emmert from Moody Gardens for technical diving support, and the University of Texas at Austin’s Genome Sequencing and Analysis Facility for sequencing support. Computation capacity was provided by Research Computing services at Florida Atlantic University. Funding for this research was awarded to J. Voss by the NOAA Office of Ocean Exploration and Research under award NA14OAR4320260 through the Cooperative Institute for Ocean Exploration, Research, and Technology (CIOERT). Additional funding was provided to A. Sturm through a National Science Foundation Graduate Research Fellowship and scholarships from Florida Sea Grant and the Women Divers Hall of Fame. All corals were collected under permit FKNMS-2019-088 from Florida Keys National Marine Sanctuary. This is contribution 2295 from Harbor Branch Oceanographic Institute.

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Sturm, A.B., Eckert, R.J., Carreiro, A.M. et al. Population genetic structure of the broadcast spawning coral, Montastraea cavernosa, demonstrates refugia potential of upper mesophotic populations in the Florida Keys. Coral Reefs (2021). https://doi.org/10.1007/s00338-021-02112-y

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Keywords

  • Population genetics
  • Genetic connectivity
  • Mesophotic coral ecosystems
  • Montastraea cavernosa
  • Marine protected areas