Long distance dispersal and vertical gene flow in the Caribbean brooding coral Porites astreoides

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Serrano, Xaymara M ^a,f   Baums, Iliana B ^b   Smith, Tyler B ^c   Jones, Ross J ^d   Shearer, Tonya L ^e   Baker, Andrew C ^a  

^a UNIVERSITY OF MIAMI   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF THE VIRGIN ISLANDS   (United States)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^e GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^f ATLANTIC OCEANOGRAPHIC AND METEOROLOGICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BERMUDA; CARIBBEAN; CORAL; GENE FLOW; GENETIC VARIABILITY; MICROSATELLITE MARKER; SYMBIODINIUM; SYMBIONT; UNITED STATES; ZONATION; ANIMAL; ANTHOZOA; CORAL REEF; GENETICS; GENOTYPE; POPULATION GENETICS;

MICROSATELLITE DNA;

ANIMALS; ANTHOZOA; CARIBBEAN REGION; CORAL REEFS; GENE FLOW; GENETICS, POPULATION; GENOTYPE; MICROSATELLITE REPEATS;

EID: 84959019494     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep21619     Document Type: Article

References (75)

1. Miller, K. J. & Ayre, D. J. Population structure is not a simple function of reproductive mode and larval type: insights from tropical corals. Journal of Animal Ecology 77, 713-724, doi:10.1111/j.1365-2656.2008.01387.x (2008).
2. Magalon, H., Adjeroud, M. & Veuille, M. Patterns of genetic variation do not correlate with geographical distance in the reef-building coral Pocillopora meandrina in the South Pacific. Molecular ecology 14, 1861-1868, doi:10.1111/j.1365-294X.2004.02430.x (2005).
3. Fadlallah, Y. H. Sexual reproduction, development and larval biology in scleractinian corals. A review. Coral Reefs 2, 129-150, doi:10.1007/bf00336720 (1983).
4. Szmant, A. M. Reproductive ecology of Caribbean reef corals. Coral Reefs 5, 43-53, doi:10.1007/bf00302170 (1986).
5. Harrison, P. L. & Wallace, C. C. Ecosystems Of The world: 25. Coral Reefs. [Dubinsky, Z. (ed.)] [133-207] (Elsevier, Amsterdam, 1990).
6. Coffroth, M. A., Santos, S. R. & Goulet, T. L. Early ontogenetic expression of specificity in a cnidarian-algal symbiosis. Marine Ecology Progress Series 222, 85-96, doi:10.3354/meps222085 (2001).
7. Goreau, T. F. The ecology of Jamaican coral reefs .1. Species composition and zonation. Ecology 40, 67-90, doi:10.2307/1929924 (1959).
8. Goreau, T. F. & Wells, J. W. Shallow-water scleractinia of Jamaica- revised list of species and their vertical distribution range. B. Mar. Sci. 17, 442-453 (1967).
9. Bongaerts, P., Ridgway, T., Sampayo, E. M. & Hoegh-Guldberg, O. Assessing the 'deep reef refugia' hypothesis: focus on Caribbean reefs. Coral Reefs 29, 309-327, doi:10.1007/s00338-009-0581-x (2010).
10. Gleason, D. F. Differential-effects of ultraviolet-rdiation on green and brown morphs of the Caribbean coral Porites astreoides. Limnol. and Oceanogr. 38, 1452-1463 (1993).
11. McGuire, M. P. Timing of larval release by Porites astreoides in the northern Florida Keys. Coral Reefs 17, 369-375, doi:10.1007/s003380050141 (1998).
12. Goodbody-Gringley, G. et al. Toxicity of Deepwater Horizon Source Oil and the Chemical Dispersant, Corexit (R) 9500, to Coral Larvae. Plos One 8, doi:10.1371/journal.pone.0045574 (2013).
13. Chornesky, E. A. & Peters, E. C. Sexual reproduction and colony growth in the scleractinian coral Porites astreoides. Biol. Bull. 172, 161-177, doi:10.2307/1541790 (1987).
14. Baker, A. C. The symbiosis ecology of reef-building corals. Ph. D. thesis. (University of Miami, Miami, Florida, 1999).
15. Warner, M. E., LaJeunesse, T. C., Robison, J. D. & Thur, R. M. The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: Potential implications for coral bleaching. Limnology and Oceanography 51, 1887-1897 (2006).
16. Bongaerts, P. et al. Prevalent endosymbiont zonation shapes the depth distributions of scleractinian coral species. Royal Society Open Science 2, 140297-140297, doi:10.1098/rsos.140297 (2015).
17. Green, D. H., Edmunds, P. J. & Carpenter, R. C. Increasing relative abundance of Porites astreoides on Caribbean reefs mediated by an overall decline in coral cover. Marine Ecology Progress Series 359, 1-10, doi:10.3354/meps07454 (2008).
18. Serrano, X. et al. Geographic differences in vertical connectivity in the Caribbean coral Montastraea cavernosa despite high levels of horizontal connectivity at shallow depths. Molecular ecology 23, 4226-4240, doi:10.1111/mec.12861 (2014).
19. Pochon, X. & Gates, R. D. A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Molecular phylogenetics and evolution 56, 492-497, doi:10.1016/j.ympev.2010.03.040 (2010).
20. Iglesias-Prieto, R., Beltran, V. H., LaJeunesse, T. C., Reyes-Bonilla, H. & Thome, P. E. Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proceedings. Biological sciences/The Royal Society 271, 1757-1763, doi:10.1098/rspb.2004.2757 (2004).
21. Mieog, J. C., MJ, V. A. N. O., Berkelmans, R., Stam, W. T. & Olsen, J. L. Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR. Mol Ecol Resour 9, 74-82, doi:10.1111/j.1755-0998.2008.02222.x (2009).
22. Baums, I. B., Miller, M. W. & Hellberg, M. E. Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Molecular ecology 14, 1377-1390, doi:10.1111/j.1365-294X.2005.02489.x (2005).
23. Foster, N. L. et al. Connectivity of Caribbean coral populations: complementary insights from empirical and modelled gene flow. Molecular ecology 21, 1143-1157, doi:10.1111/j.1365-294X.2012.05455.x (2012).
24. Holstein, D. M., Paris, C. B. & Mumby, P. J. Consistency and inconsistency in multispecies population network dynamics of coral reef ecosystems. Marine Ecology Progress Series 499, 1-18, doi:10.3354/meps10647 (2014).
25. Nunes, F. L. D., Norris, R. D. & Knowlton, N. Long Distance Dispersal and Connectivity in Amphi-Atlantic Corals at Regional and Basin Scales. Plos One 6, doi:10.1371/journal.pone.0022298 (2011).
26. Kourafalou, V. H. & Kang, H. Florida Current meandering and evolution of cyclonic eddies along the Florida Keys Reef Tract: Are they interconnected? Journal of Geophysical Research 117, doi:10.1029/2011jc007383 (2012).
27. Hitchcock, G. L. et al. Property fields in a Tortugas Eddy in the southern straits of Florida. Deep Sea Research Part I: Oceanographic Research Papers 52, 2195-2213, doi:10.1016/j.dsr.2005.08.006 (2005).
28. Brazeau, D. A., Lesser, M. P. & Slattery, M. Genetic Structure in the Coral, Montastraea cavernosa: Assessing Genetic Differentiation among and within Mesophotic Reefs. PLOSone 8, e65845, doi:10.1371/journal.pone.0065845.t001 (2013).
29. Prada, C. & Hellberg, M. E. Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral. Proceedings of the National Academy of Sciences of the United States of America 110, 3961-3966, doi:10.1073/pnas.1208931110 (2013).
30. Prada, C. et al. Cryptic diversity hides host and habitat specialization in a gorgonian-algal symbiosis. Molecular ecology 23, 3330-3340, doi:10.1111/mec.12808 (2014).
31. Eytan, R. I., Hayes, M., Arbour-Reily, P., Miller, M. & Hellberg, M. E. Nuclear sequences reveal mid-range isolation of an imperilled deep-water coral population. Molecular ecology 18, 2375-2389, doi:10.1111/j.1365-294X.2009.04202.x (2009).
32. Frade, P. R. et al. Semi-permeable species boundaries in the coral genus Madracis: introgression in a brooding coral system. Molecular phylogenetics and evolution 57, 1072-1090, doi:10.1016/j.ympev.2010.09.010 (2010).
33. van Oppen, M. J., Bongaerts, P., Underwood, J. N., Peplow, L. M. & Cooper, T. F. The role of deep reefs in shallow reef recovery: an assessment of vertical connectivity in a brooding coral from west and east Australia. Molecular ecology 20, 1647-1660, doi:10.1111/j.1365-294X.2011.05050.x (2011).
34. Holstein, D. M., Paris, C. B., Vaz, A. C. & Smith, T. B. Modeling vertical coral connectivity and mesophotic refugia. Coral Reefs, doi:10.1007/s00338-015-1339-2 (2015).
35. Levitan, D. R. et al. Mechanisms of Reproductive Isolation among Sympatric Broadcast-Spawning Corals of the Montastraea annularis Species Complex. Evolution 58, 308-323 (2004).
36. Rowan, R. & Knowlton, N. Intraspecific diversity and ecological zonation in coral algal symbiosis. Proc. Acad. Sci. USA 92, 2850-2853, doi:10.1073/pnas.92.7.2850 (1995).
37. LaJeunesse, T. C. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology 141, 387-400, doi:10.1007/s00227-002-0829-2 (2002).
38. Richmond, R. H. Energetics, competence, and long-distance dispersal of planula larvae of the coral Pocillopora damicornis. Mar. Biol. 93, 527-533 (1988).
39. Kenkel, C. D. et al. Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Molecular ecology 22, 4335-4348, doi:10.1111/mec.12391 (2013).
40. th Int. Congr. Syst. Evol. Biol. 1, 170-178 (1991).
41. th Int. Coral Reef Symp. 2, 643-656 (1993).
42. Baker, A. C. Flexibility andspecificity incoral-algalsymbiosis: Diversity, Ecology, and Biogeography of Symbiodinium. Annual Review of Ecology, Evolution, and Systematics 34, 661-689, doi:10.1146/annurev.ecolsys.34.011802.132417 (2003).
43. van Oppen, M. J. H., Bongaerts, P., Underwood, J. N., Peplow, L. M. & Cooper, T. F. The role of deep reefs in shallow reef recovery: an assessment of vertical connectivity in a brooding coral from west and east Australia. Molecular ecology 20, 1647-1660, doi:10.1111/j.1365-294X.2011.05050.x (2011).
44. Flood, V. S., Pitt, J. M. & Smith, S. R. Historical and ecological analysis of coral communities in Castle Harbour (Bermuda) after more than a century of environmental perturbation. Mar Pollut Bull 51, 545-557, doi:10.1016/j.marpolbul.2005.07.010 (2005).
45. Banaszak, A. T., LaJeunesse, T. C. & Trench, R. K. The synthesis of mycosporine-like amino acids (MAAs) by cultured, symbiotic dinoflagellates. Journal of Experimental Marine Biology and Ecology 249, 219-233 (2000).
46. Severance, E. G. & Karl, S. A. Contrasting population genetic structures of sympatric, mass-spawning Caribbean corals. Marine Biology 150, 57-68, doi:10.1007/s00227-006-0332-2 (2006).
47. Vollmer, S. V. & Palumbi, S. R. Restricted gene flow in the Caribbean staghorn coral Acropora cervicomis: Implications for the recovery of endangered reefs. Journal of Heredity 98, 40-50, doi:10.1093/jhered/esl057 (2007).
48. Vermeij, M. J. A. Substrate composition and adult distribution determme recruitment patterns in a Caribbean brooding coral. Marine Ecology Progress Series 295, 123-133, doi:10.3354/meps295123 (2005).
49. Brazeau, D. A., Sammarco, P. W. & Gleason, D. F. A multi-locus genetic assignment technique to assess sources of Agaricia agaricites larvae on coral reefs. Marine Biology 147, 1141-1148, doi:10.1007/s00227-005-0022-5 (2005).
50. Davies, S. W., Treml, E. A., Kenkel, C. D. & Matz, M. V. Exploring the role of Micronesian islands in the maintenance of coral genetic diversity in the Pacific Ocean. Molecular ecology 24, 70-82, doi:10.1111/mec.13005 (2015).
51. Falkowski, P. G., Jokiel, P. L. & Kinzie, R. A. III. Ecosystems Of The world: 25. Coral Reefs [Dubinsky, Z. (ed.)] [89-107] (Elsevier, Amsterdam, 1990).
52. Mundy, C. N. & Babcock, R. C. Role of light intensity and spectral quality in coral settlement: Implications for depth-dependent settlement? Journal of Experimental Marine Biology and Ecology 223, 235-255, doi:10.1016/s0022-0981(97)00167-6 (1998).
53. Murdoch, T. J. T. & Aronson. R. B. Scale dependent variability of coral assemblages along the Florida Reef Tract. Coral Reefs 18, 341-351 (1999).
54. Smith, S. G., Swanson, D. W., Chiappone, M., Miller, S. L. & Ault, J. S. Probability sampling of stony coral populations in the Florida Keys. Environ Monit Assess 183, 121-138, doi:10.1007/s10661-011-1912-2 (2011).
55. Barron, M. G., Vivian, D. N., Yee, S. H. & Santavy, D. L. Methods to estimate solar radiation dosimetry in coral reefs using remote sensed, modeled, and in situ data. Environ Monit Assess 151, 445-455, doi:10.1007/s10661-008-0288-4 (2009).
56. Rowan, R. & Powers, D. A. Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar. Ecol. Prog. Ser. 71, 65-73, doi:10.3354/meps071065 (1991).
57. Vera, J. C. et al. Rapid transcriptome characterization for a nonmodel organism using 454 pyrosequencing. Molecular ecology 17, 1636-1647, doi:10.1111/j.1365-294X.2008.03666.x (2008).
58. Benson, G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573-580 (1999).
59. Untergasser, A. et al. Primer3-new capabilities and interfaces. Nucleic Acids Research 40, doi:10.1093/nar/gks596 (2012).
60. Peakall, R. & Smouse, P. E. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288-295, doi:10.1111/j.1471-8286.2005.01155.x (2006).
61. Rousset, F. & Raymond, M. Testing heterozygore excess and deficiency. Genetics 140, 1413-1419 (1995).
62. Strimmer, K. fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinformatics 24, 1461-1462, doi:10.1093/bioinformatics/btn209 (2008).
63. Addison, J. A. & Hart, M. W. Spawning, copulation and inbreeding coefficients in marine invertebrates. Biology Letters 1, 450-453, doi:10.1098/rsbl.2005.0353 (2005).
64. Baums, I. B. A restoration genetics guide for coral reef conservation. Molecular ecology 17, 2796-2811, doi:10.1111/j.1365-294X.2008.03787.x (2008).
65. Chybicki, I. J. & Burczyk, J. Simultaneous Estimation of Null Alleles and Inbreeding Coefficients. Journal of Heredity 100, 106-113, doi:10.1093/jhered/esn088 (2009).
66. Meirmans, P. G. & Van Tienderen, P. H. GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes 4, 792-794, doi:10.1111/j.1471-8286.2004.00770.x (2004).
67. Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945-959 (2000).
68. Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular ecology 14, 2611-2620, doi:10.1111/j.1365-294X.2005.02553.x (2005).
69. Earl, D. A. & vonHoldt, B. M. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359-361, doi:10.1007/s12686-011-9548-7 (2012).
70. Gayevskiy, V., Klaere, S., Knight, S. & Goddard, M. R. ObStruct: a method to objectively analyse factors driving population structure using Bayesian ancestry profiles. PLoS One 9, e85196, doi:10.1371/journal.pone.0085196 (2014).
71. Jakobsson, M. & Rosenberg, N. A. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801-1806, doi:10.1093/bioinformatics/btm233 (2007).
72. Rosenberg, N. A. DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes 4, 137-138, doi:10.1046/j.1471-8286.2003.00566.x (2004).
73. LaJeunesse, T. C. & Trench, R. K. Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biological Bulletin 199, 126-134, doi:10.2307/1542872 (2000).
74. Correa, A. M. S., McDonald, M. D. & Baker, A. C. Development of clade-specific Symbiodinium primers for quantitative PCR (qPCR) and their application to detecting clade D symbionts in Caribbean corals. Marine Biology 156, 2403-2411, doi:10.1007/s00227-009-1263-5 (2009).
75. Cunning, R. & Baker, A. C. Excess algal symbionts increase the suscceptibility of reef corals to bleaching. Nature Climate Change, doi:10.1038/nclimate1711 (2013).