Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Genetic discontinuity among regional populations of Lophelia pertusa in the North Atlantic Ocean

Abstract

Knowledge of the degree to which populations are connected through larval dispersal is imperative to effective management, yet little is known about larval dispersal ability or population connectivity in Lophelia pertusa, the dominant framework-forming coral on the continental slope in the North Atlantic Ocean. Using nine microsatellite DNA markers, we assessed the spatial scale and pattern of genetic connectivity across a large portion of the range of L. pertusa in the North Atlantic Ocean. A Bayesian modeling approach found four distinct genetic groupings corresponding to ocean regions: Gulf of Mexico, coastal southeastern U.S., New England Seamounts, and eastern North Atlantic Ocean. An isolation-by-distance pattern was supported across the study area. Estimates of pairwise population differentiation were greatest with the deepest populations, the New England Seamounts (average F ST = 0.156). Differentiation was intermediate with the eastern North Atlantic populations (F ST = 0.085), and smallest between southeastern U.S. and Gulf of Mexico populations (F ST = 0.019), with evidence of admixture off the southeastern Florida peninsula. Connectivity across larger geographic distances within regions suggests that some larvae are broadly dispersed. Heterozygote deficiencies were detected within the majority of localities suggesting deviation from random mating. Gene flow between ocean regions appears restricted, thus, the most effective management scheme for L. pertusa involves regional reserve networks.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Addison JA, Hart MW (2005) Spawning, copulation and inbreeding coefficients in marine invertebrates. Biol Lett 1:450–453

  2. Avise JC (1994) Molecular markers, natural history and evolution. Chapman & Hall, New York, p 511

  3. Avise JC (2000) Phylogeography. Harvard University Press, Cambridge

  4. Ayre DJ, Hughes TP (2000) Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia. Evolution 54:1590–1605

  5. Ayre DJ, Hughes TP (2004) Climate change, genotypic diversity and gene flow in reef-building corals. Ecol Lett 7:273–278

  6. Bane JM Jr, Attkinson LP, Brooks DA (2001) Gulf Stream physical oceanography at the Charleston Bump: deflection, bimodality, meanders, and upwelling. In: Sedberry GR (ed) Island in the stream: oceanography and fisheries of the Charleston Bump, Amer Fish Soc Symp 25, Bethesda, MD, pp 25–36

  7. Barber PH, Palumbi SR, Erdmann MV, Moosa MK (2000) A marine Wallace’s line? Nature 406:692–693

  8. Baums IB, Miller MM, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390

  9. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2001) Genetix: logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions: CNRS UMR. 5000, Université de Montpellier II, Montpellier

  10. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833

  11. Bergquist DC, Ward T, Cordes EE, McNelis T, Howlett S, Kosoff R, Hourdez S, Carney R, Fisher CR (2003) Community structure of vestimentiferan-generated habitat islands from upper Louisiana slope cold seeps. J Exp Mar Biol Ecol 289:197–222

  12. Bohonak AJ (1999) Dispersal, gene flow, and population structure. Quart Rev Biol 74(1):21–45

  13. Bradbury IR, Bentzen P (2007) Non-linear genetic isolation by distance: implications for dispersal estimation in anadromous and marine fish populations. Mar Ecol Prog Ser 340:245–257

  14. Briggs JC (1974) Marine zoogeography. McGraw-Hill Book Co., New York

  15. Brooke S, Schroeder WW (2007) State of deep coral ecosystems in the Gulf of Mexico region: Texas to the Florida Straits. In: Lumsden SE, Hourigan TF, Bruckner AW, Dorr G (eds) The state of deep coral ecosystems of the United States. NOAA Tech Memo CRCP-3, Silver Spring, MD, pp 233–270

  16. Brooke SD, Young CM, Holmes M (2007) Biological characterization and studies, Part II. In: Characterization of northern Gulf of Mexico deepwater hard bottom communities with emphasis on Lophelia coral. Continental Shelf Associates, Inc., New Orleans, pp 119–147

  17. Cairns SD, Chapman RE (2001) Biogeographic affinities of the North Atlantic deep-water Scleractinia. In: Willison JHM, Jall J, Gass SE (eds) Proceedings of the first international symposium on deep-sea corals. Ecology Action Centre, Halifax, NS, pp 30–57

  18. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analyses: models and estimation procedures. Evolution 21:873–881

  19. Christie MR, Johnson DW, Stallings CD, Hixon MA (2010) Self recruitment and sweepstakes reproduction amid extensive gene flow in a coral–reef fish. Mol Ecol 19:1042–1057

  20. Clark M, Rowden AA, Schlacher T, Williams A, Consalvey M, Stocks KI, Rogers AD, O’Hara TD, White M, Shank T, Hall-Spencer JM (2010) The ecology of seamounts: structure, function, and human impacts. Annu Rev Mar Sci 2:253–278

  21. Cowan RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annu Rev Mar Sci 1:443–466

  22. Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527

  23. Cunningham CW, Collins TM (1998) Beyond area relationships: extinction and recolonization in molecular marine biogeography. In: De Salle R, Schierwater B (eds) Molecular approaches to ecology, evolution. Birkhauser-Verlag, Basel, pp 297–321

  24. Davies AJ, Roberts JM, Hall-Spenser J (2007) Preserving deep-sea natural heritage: emerging issues in offshore conservation and management. Biol Conserv 138:299–312

  25. Davies AJ, Duineveld GCA, van Weering TCE, Mienis F, Quattrini AM, Seim HE, Bane JM, Ross SW (2010) Short-term environmental variability in cold-water coral habitat at Viosca Knoll, Gulf of Mexico. Deep-Sea Res I 57:199–212

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

  27. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

  28. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

  29. Eytan RI, Hayes M, Arbour-Reily P, Miller M, Hellberg ME (2009) Nulcear sequences reveal mid-range isolation of imperilled deep-water coral populations. Mol Ecol 18:2375–2389

  30. Falush D, Stephens M, Pritchard J (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

  31. Fontaine M, Baird S, Piry S et al (2007) Rise of oceanographic barriers in continuous populations of a cetacean: the genetic structure of harbour porpoises in old world waters. BMC Biol 5:30. doi:10.1186/1741-7007-5-30

  32. Fuller C et al (2004) Comparative toxicity of oil, dispersant, and oil plus dispersant to several marine species. Environ Toxicol Chem 23(12):2929–2941

  33. Garnier S, Alibert P, Audiot P, Prieur B, Rasplus J-Y (2004) Isolation by distance and sharp discontinuities in gene frequencies: implications for the phylogeography of an alpine insect species, Carabus solieri. Mol Ecol 13:1883–1897

  34. Grasmueck M, Eberli GP, Viggiano DA et al (2006) Autonomous underwater vehicle (AUV) mapping reveals coral mound distribution, morphology, and oceanography in deep water of the Straights of Florida. Geophys Res Lett 33:L23616

  35. Guinotte JM, Orr JC, Cairns SD, 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

  36. Haapkyla J et al (2007) Oil pollution on coral reefs: a review of the state of knowledge and management needs. Vie et Millieu 57(1–2):95–111

  37. Hellberg ME (1996) Dependence of gene flow on geographic distance in two solitary corals with different larval dispersal capabilities. Evolution 50(3):1167–1175

  38. Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70(Suppl. 1):273–290

  39. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

  40. Jochens AE, DiMarco SF (2008) Physical oceanographic conditions in deepwater Gulf of Mexico in summer 2000–2002. Deep-Sea Res II 55:2541–2554

  41. Johnson MTJ, Stinchcombe JR (2007) An emerging synthesis between community ecology and evolutionary biology. Trends Ecol Evol 22:250–257

  42. Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543

  43. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

  44. Knowlton N (2000) Molecular genetic analysis of species boundaries in the sea. Hydrobiologia 420:73–90

  45. Ledoux J-B, Garrabou J, Bianchimani O, Drap P, Feral J-P, Aurelle D (2010) Fine-scale genetic structure and inferences on population biology in the threatened Mediterranean red coral, Corallium rubrum. Mol Ecol 19:4204–4216

  46. LeGoff MC, Rogers AD (2002) Characterization of ten microsatellite loci for the deep-sea coral Lophelia pertusa (Linnaeus, 1758). Mol Ecol Notes 2:164–166

  47. LeGoff-Vitry MC, Pybus OG, Rogers AD (2004a) Genetic structure of the deep-sea coral Lophelia pertusa in the northeast Atlantic revealed by microsatellites and internal transcribed spacer sequences. Mol Ecol 13:537–549

  48. LeGoff-Vitry MC, Rogers AD, Baglow D (2004b) A deep-sea slant on the molecular phylogeny of the Scleractinia. Mol Phylogenet Evol 30:167–177

  49. Levin LA (2006) Recent progress in understanding larval dispersal: new directions and digressions. Integr Comp Biol 46(3):282–297

  50. Levin LA, Dayton PK (2009) Ecological theory and continental margins: where shallow meets deep. Trends Ecol Evol 24(11):606–617

  51. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

  52. Morey SL, Schroeder WW, O’Brien JJ, Zavala-Hidalgo J (2003) The annual cycle of riverine influence in the eastern Gulf of Mexico basin. Geophys Res Lett 30(16):1867

  53. Morrison CL, Eackles MS, Johnson RL, King TL (2008) Characterization of 13 microsatellite loci for the deep-sea coral, Lophelia pertusa (Linnaeus 1758), from the western North Atlantic Ocean and Gulf of Mexico. Mol Ecol Resour 8:1037–1039

  54. Nei M (1973) The theory and estimation of genetic distances. In: Morton NE (ed) Genetic structure of populations. University of Hawaii Press, Honolulu, pp 45–54

  55. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

  56. Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13(1):S146–S158

  57. Palumbi SR (2004) Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annu Rev Environ Resour 29:31–68

  58. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

  59. Pickart RS, Watts DR (1990) Deep western boundary current variability at Cape Hatteras. J Mar Res 48:765–791

  60. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

  61. Raymond M, Roussett F (1995) An exact test for population differentiation. Evolution 49:1280–1283

  62. Reed JK, Weaver DC, Pomponi SA (2006) Habitat and fauna of deep-water Lophelia pertusa coral reefs off the southeastern U.S.: Blake Plateau, Straights of Florida, and Gulf of Mexico. Bull Mar Sci 78:343–375

  63. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

  64. Roberts JM, Wheeler AJ, Freiwald A (2006) Reefs of the deep: the biology and geology of cold-water coral ecosystems. Science 312:543–547

  65. Roberts JM, Wheeler AJ, Freiwald A, Cairns S (2009) Cold-water corals: the biology and geology of deep sea coral habitats. Cambridge University Press, New York

  66. Rogers AD (1999) The biology of Lophelia pertusa (Linnaeus 1758) and other deep-water reef-forming corals and impacts from human activities. Int Rev Hydrobiol 84:315–406

  67. Rogers AD (2002) Molecular ecology and evolution of slope species. In: Wefer G, Billet D, Hebbeln D et al (eds) Ocean margin systems. Springer-Verlag, Berlin, pp 323–337

  68. Rohlf FJ (2000) NTSYS-PC: numerical taxonomy and multivariate analysis systems, Version 2.10. Exeter Software, Setauket

  69. Rosel PE, Hansen L, Hohn AA (2009) Restricted dispersal in a continuously distributed marine species: common bottlenose dolphins Tursiops truncatus in coastal waters of the western Atlantic. Mol Ecol 18:5030–5045

  70. Ross SW, Nizinski MS (2007) State of deep coral ecosystems in the U.S. southeast region: Cape Hatteras to Southeastern Florida. In: Lumsden SE, Hourigan TF, Bruckner AW, Dorr G (eds) The state of deep coral ecosystems of the United States. NOAA Tech Memo CRCP-3, Silver Spring, MD, pp 233–270

  71. Ross SW, Quattrini AM (2007) The fish fauna associated with deep coral banks off the southeastern United States. Deep-Sea Res I 54:975–1007

  72. Ross SW, Quattrini AM (2009) Deep-sea fish assemblage patterns on the Blake Plateau (Western North Atlantic Ocean). Mar Ecol 30:74–92

  73. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

  74. Rousset F (2008) GENEPOP ‘007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

  75. Selkoe K, Henzler C, Gaines S (2008) Seascape genetics and the spatial ecology of marine populations. Fish Fish 9:363–377

  76. Shanks AL, Grantham BA, Carr MH (2003) Propagule dispersal and the size and spacing of marine reserves. Ecol Appl 13:S159–S169

  77. Slatkin M (1993) Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47:264–279

  78. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

  79. Sotka EE, Wares JP, Barth JA, Grosberg RK, Palumbi SR (2004) Strong genetic clines and geographic variation in gene flow in the rocky intertidal barnacle Balanus glandula. Mol Ecol 13:2143–2156

  80. Swearer SE, Shima JS, Hellberg ME et al (2002) Evidence of self-recruitment in demersal marine populations. Bull Mar Sci 70:251–271

  81. Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107

  82. Underwood JN, Smith LD, van Oppen MJH, Gilmour JP (2007) Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Mol Ecol 16:771–784

  83. Underwood JN, Smith LD, van Oppen MJH, Gilmour JP (2009) Ecologically relevant dispersal of corals on isolated reefs: implications for managing resilience. Ecol Appl 19(1):18–29

  84. Urcuyo IA, Massoth GJ, Julian D, Fisher CR (2003) Habitat, growth and physiological ecology of a basaltic community of Ridgeia piscesae from the Juan de Fuca Ridge. Deep-Sea Res I 50:763–780

  85. VanOppen MJH, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15:3863–3883

  86. Van Oosterhaut C, Hutchinson WF, Wills DPM, Shipley P (2004) MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 3:535–538

  87. Vellend M, Geber MA (2005) Connections between species diversity and genetic diversity. Ecol Lett 8:767–781

  88. Waller RG, Tyler PA (2005) The reproductive biology of two deep-water, reef-building scleractinians from the NE Atlantic Ocean. Coral Reefs 24:514–522

  89. Wang J, Santure A (2009) Parentage and sibship inference from multilocus genotype data under polygamy. Genetics 181:1579–1594

  90. Warner RR, Cowen RK (2002) Larval retention of production in marine populations: evidence, mechanisms, and consequences. Bull Mar Sci 70:245–249

  91. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1360

  92. Whitaker K (2004) Non-random mating and population genetic subdivision of two broadcasting corals at Ningaloo Reef, Western Australia. Mar Biol 144:593–603

  93. White C, Selkoe KA, Watson J, Siegel DA, Zacherl DC, Toonen RJ (2010) Ocean currents help explain population genetic structure. Proc R Soc B 277:1685–1694

  94. Wilberg MJ, Dreher BP (2004) GENECAP: a program for analysis of multilocus genotype data for non-invasive sampling and capture-recapture population estimation. Mol Ecol Notes 4:783–785

  95. Woods JG, Paetkau D, Lewis D et al (1999) Genetic tagging of free-ranging black and brown bears. Wildl Soc Bull 27:616–627

  96. Wright S (1943) Isolation by distance. Genetics 28:114–138

  97. Wright S (1951) The genetical structure of populations. Ann. Eugenics 15:323–354

  98. Zardus JD, Etter RJ, Chase MR, Rex MA, Boyle EE (2006) Bathymetric and geographic population structure in the pan-Atlantic deep-sea bivalve Deminucula atacellana (Schenck, 1939). Mol Ecol 15:639–651

Download references

Acknowledgments

This investigation was financially supported by the USGS Outer Continental Shelf Ecosystem Program and was sponsored by the Minerals Management Service. NOAA Office of Ocean Exploration supported field work both in the SEUS via four cruises (grants to S.W. Ross and S. Brooke, lead PIs) and also to the New England and Corner Rise Seamounts (cruise DASS2005, grant to L. Watling, T. Shank, S. France, R. Waller and P. Auster, lead PIs). Thanks to the ROV pilots and crew of the R/V Ronald H. Brown facilitating collection of the NES samples. The two R/V Cape Hatteras missions were sponsored by the Duke/UNC Oceanographic Consortium (to SWR), and we thank that ship’s personnel for excellent support. We thank J.M. Roberts and G. Duineveld for facilitating cruise participation of SWR on R/V Pelagia where ENAO samples were collected. Norwegian collections were financially supported by Statoil Hydro and The Norwegian Academy of Science and Letters. Special thanks to USGS Lophelia I research colleagues: G. Brewer, C. Kellogg, K. Sulak and the crew at the USGS Coastal Ecology and Conservation Research. We also thank the Continental Shelf Associates Lophelia I scientists for allowing an author (CLM) to participate on GOM cruises. The USGS-BRD Leetown Science Center, Aquatic Ecology Branch, provided partial funding to CLM. The following individuals kindly donated coral samples: E. Cordes, C. Fisher, W. Schroeder, A. Davies, J. Reed, C. Messing. Thanks are extended to the following individuals for helpful discussions regarding data collection and analyses: M. Eackles, B. Lubinski, C. Young, and J. Switzer. Harbor Branch Oceanographic Institution, the crew members of the R/V Seward Johnson I and II, and the JSL submersible crew helped make this research possible. M. Carlson produced maps and calculated geographic distances. M. Rhode and M. Springmann assisted with Figs 1 and 2, respectively. Comments by J. Switzer, M. Miller and 3 anonymous reviewers improved the manuscript. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Author information

Correspondence to Cheryl L. Morrison.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Morrison, C.L., Ross, S.W., Nizinski, M.S. et al. Genetic discontinuity among regional populations of Lophelia pertusa in the North Atlantic Ocean. Conserv Genet 12, 713–729 (2011). https://doi.org/10.1007/s10592-010-0178-5

Download citation

Keywords

  • Cold-water coral
  • Connectivity
  • Gene flow
  • Dispersal barriers
  • Isolation by distance