in

Population genetic structure of the great star coral, Montastraea cavernosa, across the Cuban archipelago with comparisons between microsatellite and SNP markers

  • 1.

    Carson, H. S., Cook, G. S., López-Duarte, P. C. & Levin, L. A. Evaluating the importance of demographic connectivity in a marine metapopulation. Ecology 92, 1972–1984. https://doi.org/10.1890/11-0488.1 (2011).

    PubMed  Article  Google Scholar 

  • 2.

    Jackson, J. B. C., Donovan, M. K., Cramer, K. L., Lam, V. & Lam, W. Status and trends of Caribbean coral reefs: 1970–2012. Glob. Coral Reef Monit. Network, IUCN, Gland. Switz. 306 (2014).

  • 3.

    Palumbi, S. R. Population genetics, demographic connectivity, and the design of marine reserves. 13, 146–158, https://doi.org/10.1890/1051-0761(2003)013[0146:PGDCAT]2.0.CO;2 (2003).

  • 4.

    Botsford, L. W. et al. Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical efforts to predictive needs. Coral Reefs 28, 327–337. https://doi.org/10.1007/s00338-009-0466-z (2009).

    ADS  PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 5.

    Galindo, H. M., Olson, D. B. & Palumbi, S. R. Seascape genetics: a coupled oceanographic-genetic model predicts population structure of Caribbean corals. Curr. Biol. 16, 1622–1626. https://doi.org/10.1016/j.cub.2006.06.052 (2006).

    PubMed  CAS  Article  Google Scholar 

  • 6.

    Rippe, J. P. et al. Population structure and connectivity of the mountainous star coral, Orbicella faveolata, throughout the wider Caribbean region. Ecol. Evol. 7, 9234–9246. https://doi.org/10.1002/ece3.3448 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  • 7.

    Studivan, M. S. & Voss, J. D. Population connectivity among shallow and mesophotic Montastraea cavernosa corals in the Gulf of Mexico identifies potential for refugia. Coral Reefs 37, 1183–1196. https://doi.org/10.1007/s00338-018-1733-7 (2018).

    ADS  Article  Google Scholar 

  • 8.

    Baums, I. B., Johnson, M. E., Devlin-Durante, M. K. & Miller, M. W. Host population genetic structure and zooxanthellae diversity of two reef-building coral species along the Florida Reef Tract and wider Caribbean. Coral Reefs 29, 835–842. https://doi.org/10.1007/s00338-010-0645-y (2010).

    ADS  Article  Google Scholar 

  • 9.

    Serrano, X. M. et al. Long distance dispersal and vertical gene flow in the Caribbean brooding coral Porites astreoides. Sci. Rep. 6, 21619. https://doi.org/10.1038/srep21619 (2016).

    ADS  PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 10.

    Serrano, X. et al. 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. https://doi.org/10.1111/mec.12861 (2014).

    PubMed  CAS  Article  Google Scholar 

  • 11.

    Bongaerts, P. et al. Deep reefs are not universal refuges: reseeding potential varies among coral species. Sci. Adv. 3, e1602373. https://doi.org/10.1126/sciadv.1602373 (2017).

    ADS  PubMed  PubMed Central  Article  Google Scholar 

  • 12.

    Eckert, R. J., Studivan, M. S. & Voss, J. D. Populations of the coral species Montastraea cavernosa on the Belize Barrier Reef lack vertical connectivity. Sci. Rep. 9, 7200. https://doi.org/10.1038/s41598-019-43479-x (2019).

    ADS  PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 13.

    Goodbody-Gringley, G., Vollmer, S. V., Woollacott, R. M. & Giribet, G. Limited gene flow in the brooding coral Favia fragum (Esper, 1797). Mar. Biol. 157, 2591–2602. https://doi.org/10.1007/s00227-010-1521-6 (2010).

    Article  Google Scholar 

  • 14.

    Goodbody-Gringley, G., Woollacott, R. M. & Giribet, G. Population structure and connectivity in the Atlantic scleractinian coral Montastraea cavernosa (Linnaeus, 1767). Mar. Ecol. 33, 32–48. https://doi.org/10.1111/j.1439-0485.2011.00452.x (2012).

    ADS  CAS  Article  Google Scholar 

  • 15.

    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, e22298. https://doi.org/10.1371/journal.pone.0022298 (2011).

    ADS  PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 16.

    Brazeau, D. A., Lesser, M. P. & Slattery, M. Genetic structure in the coral, Montastraea cavernosa: assessing genetic differentiation among and within mesophotic reefs. PLoS ONE 8, e65845. https://doi.org/10.1371/journal.pone.0065845 (2013).

    ADS  PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 17.

    Foster, N. L. et al. Connectivity of Caribbean coral populations: complementary insights from empirical and modelled gene flow. Mol. Ecol. 21, 1143–1157. https://doi.org/10.1111/j.1365-294X.2012.05455.x (2012).

    PubMed  Article  Google Scholar 

  • 18.

    García-Machado, E., Ulmo-Díaz, G., Castellanos-Gell, J. & Casane, D. Patterns of population connectivity in marine organisms of Cuba. Bull. Mar. Sci. 94, 193–211. https://doi.org/10.5343/bms.2016.1117 (2018).

    Article  Google Scholar 

  • 19.

    Ulmo-Díaz, G. et al. Genetic differentiation in the mountainous star coral Orbicella faveolata around Cuba. Coral Reefs 37, 1217–1227. https://doi.org/10.1007/s00338-018-1722-x (2018).

    ADS  Article  Google Scholar 

  • 20.

    Creary, M. et al. Status of coral reefs in the northern Caribbean and western Atlantic GCRMN node in 2008. in Status of Coral Reefs of the World (ed. Wilkinson, C.) 239–252 (2008).

  • 21.

    Claro, R., Reshetnikov, Y. S. & Alcolado, P. M. Physical attributes of coastal Cuba. Ecol. Mar. fishes Cuba 1–20 (2001).

  • 22.

    Whittle, D. & Rey Santos, O. Protecting Cuba’s environment: efforts to design and implement effective environmental laws and policies in Cuba. Cuban Stud. 37, 73–103. https://doi.org/10.1353/cub.2007.0018 (2006).

    Article  Google Scholar 

  • 23.

    Caballero, H., Alcolado, P. M. & Semidey, A. Condición de los arrecifes de coral frente a costas con asentamientos humanos y aportes terrígenos: el caso del litoral habanero. Cuba. Rev. Ciencias Mar. y Costeras 1, 49. https://doi.org/10.15359/revmar.1.3 (2009).

    Article  Google Scholar 

  • 24.

    González-Díaz, P. et al. Status of Cuban coral reefs. Bull. Mar. Sci. 94, 229–247. https://doi.org/10.5343/bms.2017.1035 (2018).

    Article  Google Scholar 

  • 25.

    Alcolado, P. M., Caballero, H. & Perera, S. Tendencia del cambio en el cubrimiento vivo por corales pétreos en los arrecifes coralinos de Cuba. Ser. Ocean. 5, 1–14 (2009).

    Google Scholar 

  • 26.

    Toth, L. T. et al. Do no-take reserves benefit Florida’s corals? 14 years of change and stasis in the Florida Keys National Marine Sanctuary. Coral Reefs 33, 565–577. https://doi.org/10.1007/s00338-014-1158-x (2014).

    ADS  Article  Google Scholar 

  • 27.

    Zlatarski, V. N. & Estalella, N. M. Los esclaractinios de Cuba. (2017).

  • 28.

    Zlatarski, V. N. Investigations on mesophotic coral ecosystems in Cuba (1970–1973) and Mexico (1983–1984). CICIMAR Oceánides 33, 27–43 (2018).

    Google Scholar 

  • 29.

    Reed, J. et al. Cuba’s mesophotic coral reefs and associated fish communities. Rev. Investig. Mar. 38, 56–125 (2018).

    Google Scholar 

  • 30.

    Baisre, J. A. An overview of Cuban commercial marine fisheries: the last 80 years. Bull. Mar. Sci. 94, 359–375. https://doi.org/10.5343/bms.2017.1015 (2018).

    Article  Google Scholar 

  • 31.

    Gil-Agudelo, D. L. et al. Coral reefs in the Gulf of Mexico large marine ecosystem: conservation status, challenges, and opportunities. Front. Mar. Sci. 6, 807. https://doi.org/10.3389/fmars.2019.00807 (2020).

    Article  Google Scholar 

  • 32.

    Perera Valderrama, S. et al. Marine protected areas in Cuba. Bull. Mar. Sci. 94, 423–442. https://doi.org/10.5343/bms.2016.1129 (2018).

    Article  Google Scholar 

  • 33.

    NOAA. Sister Sanctuary: Memorandum of Understanding. (2015).

  • 34.

    Budd, A. F., Nunes, F. L. D., Weil, E. & Pandolfi, J. M. Polymorphism in a common Atlantic reef coral (Montastraea cavernosa) and its long-term evolutionary implications. Evol. Ecol. 26, 265–290. https://doi.org/10.1007/s10682-010-9460-8 (2012).

    Article  Google Scholar 

  • 35.

    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. https://doi.org/10.1007/s00338-009-0581-x (2010).

    Article  Google Scholar 

  • 36.

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

    Google Scholar 

  • 37.

    Szmant, A. M. Sexual reproduction by the Caribbean reef corals Montastrea annularis and M. cavernosa. Mar. Ecol. Prog. Ser. 74, 13–25. https://doi.org/10.3354/meps074013 (1991).

    ADS  Article  Google Scholar 

  • 38.

    Highsmith, R. C., Lueptow, R. L. & Schonberg, S. C. Growth and bioerosion of three massive corals on the Belize barrier reef. Mar. Ecol. Prog. Ser. 13, 261–271 (1983).

    ADS  Article  Google Scholar 

  • 39.

    Kitchen, S. A., Crowder, C. M., Poole, A. Z., Weis, V. M. & Meyer, E. De novo assembly and characterization of four anthozoan (Phylum Cnidaria) transcriptomes. G3 (Genes|Genomes|Genetics). 5, 2441–2452, https://doi.org/10.1534/g3.115.020164 (2015).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 40.

    Matz Lab. Montastraea cavernosa annotated genome. (2018).

  • 41.

    Drury, C., Pérez Portela, R., Serrano, X. M., Oleksiak, M. & Baker, A. C. Fine-scale structure among mesophotic populations of the great star coral Montastraea cavernosa revealed by SNP genotyping. Ecol. Evol. 1–11, https://doi.org/10.1002/ece3.6340 (2020).

  • 42.

    Ellegren, H. Microsatellites: simple sequences with complex evolution. Nat. Rev. Genet. 5, 435–445. https://doi.org/10.1038/nrg1348 (2004).

    PubMed  CAS  Article  Google Scholar 

  • 43.

    Joshi, D., Ram, R. N. & Lohani, P. Microsatellite markers and their application in fisheries. Int. J. Adv. Agric. Sci. Technol. 4, 67–104 (2017).

    Google Scholar 

  • 44.

    Jarne, P. & Lagoda, P. J. L. Microsatellites, from molecules to populations and back. Trends Ecol. Evol. 11, 424–429. https://doi.org/10.1016/0169-5347(96)10049-5 (1996).

    PubMed  CAS  Article  Google Scholar 

  • 45.

    Flores-Rentería, L. & Krohn, A. Scoring microsatellite loci. in Methods in molecular biology (ed. Kantartzi, S. K.) 319–336, https://doi.org/10.1007/978-1-62703-389-3_21 (Elsevier, 2013).

  • 46.

    Andrews, K. R., Good, J. M., Miller, M. R., Luikart, G. & Hohenlohe, P. A. Harnessing the power of RADseq for ecological and evolutionary genomics. Nat. Rev. Genet. 17, 81–92. https://doi.org/10.1038/nrg.2015.28 (2016).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 47.

    Davey, J. L. & Blaxter, M. W. RADseq: next-generation population genetics. Brief. Funct. Genomics 9, 416–423. https://doi.org/10.1093/bfgp/elq031 (2010).

    PubMed  CAS  Article  Google Scholar 

  • 48.

    Wang, S., Meyer, E., McKay, J. K. & Matz, M. V. 2b-RAD: a simple and flexible method for genome-wide genotyping. Nat. Methods 9, 808–810. https://doi.org/10.1038/nmeth.2023 (2012).

    PubMed  CAS  Article  Google Scholar 

  • 49.

    Bradbury, I. R. et al. Transatlantic secondary contact in Atlantic Salmon, comparing microsatellites, a single nucleotide polymorphism array and restriction-site associated DNA sequencing for the resolution of complex spatial structure. Mol. Ecol. 24, 5130–5144. https://doi.org/10.1111/mec.13395 (2015).

    PubMed  CAS  Article  Google Scholar 

  • 50.

    Jeffries, D. L. et al. Comparing RADseq and microsatellites to infer complex phylogeographic patterns, an empirical perspective in the Crucian carp, Carassius carassius. L. Mol. Ecol. 25, 2997–3018. https://doi.org/10.1111/mec.13613 (2016).

    PubMed  Article  Google Scholar 

  • 51.

    Bohling, J., Small, M., Von Bargen, J., Louden, A. & DeHaan, P. Comparing inferences derived from microsatellite and RADseq datasets: a case study involving threatened bull trout. Conserv. Genet. 20, 329–342. https://doi.org/10.1007/s10592-018-1134-z (2019).

    CAS  Article  Google Scholar 

  • 52.

    Thornhill, D. J., Xiang, Y., Fitt, W. K. & Santos, S. R. Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals. PLoS ONE https://doi.org/10.1371/journal.pone.0006262 (2009).

    PubMed  PubMed Central  Article  Google Scholar 

  • 53.

    Eckert, R. J., Reaume, A. M., Sturm, A. B., Studivan, M. S. & Voss, J. D. Depth influences Symbiodiniaceae associations among Montastraea cavernosa corals on the Belize Barrier Reef. Front. Microbiol. 11, 1–13. https://doi.org/10.3389/fmicb.2020.00518 (2020).

    Article  Google Scholar 

  • 54.

    Hume, B. C. C. et al. SymPortal: a novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Mol. Ecol. Resour. 19, 1063–1080. https://doi.org/10.1111/1755-0998.13004 (2019).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 55.

    Pochon, X., Putnam, H. M., Burki, F. & Gates, R. D. Identifying and characterizing alternative molecular markers for the symbiotic and free-living dinoflagellate genus Symbiodinium. PLoS ONE https://doi.org/10.1371/journal.pone.0029816 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  • 56.

    LaJeunesse, T. C. & Thornhill, D. J. Improved resolution of reef-coral endosymbiont (Symbiodinium) species diversity, ecology, and evolution through psbA non-coding region genotyping. PLoS ONE https://doi.org/10.1371/journal.pone.0029013 (2011).

    PubMed  PubMed Central  Article  Google Scholar 

  • 57.

    Manzello, D. P. et al. 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. Change Biol. 25, 1016–1031. https://doi.org/10.1111/gcb.14545 (2018).

    ADS  Article  Google Scholar 

  • 58.

    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. Limnol Ocean. https://doi.org/10.4319/lo.2006.51.4.1887 (2006).

    Article  Google Scholar 

  • 59.

    Finney, J. C. et al. The relative significance of host–habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium. Microb. Ecol. 60, 250–263. https://doi.org/10.1007/s00248-010-9681-y (2010).

    PubMed  Article  Google Scholar 

  • 60.

    Bongaerts, P. et al. Deep down on a Caribbean reef: lower mesophotic depths harbor a specialized coral-endosymbiont community. Sci. Rep. https://doi.org/10.1038/srep07652 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  • 61.

    Reed, J. et al. Cruise report Cuba’s twilight zone reefs: Remotely Operated Vehicle surveys of deep/mesophotic coral reefs and associated fish communities of Cuba. (2017).

  • 62.

    Arriaza, L. et al. Modelación numérica de corrientes marinas alrededor del occidente de Cuba. Serie Oceanológica. 10, 11–22. (2012).

    Google Scholar 

  • 63.

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

  • 64.

    Bayer, T. et al. Symbiodinium transcriptomes: genome insights into the dinoflagellate symbionts of reef-building corals. PLoS ONE https://doi.org/10.1371/journal.pone.0035269 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  • 65.

    Davies, S. W., Ries, J. B., Marchetti, A. & Castillo, K. D. Symbiodinium functional diversity in the coral Siderastrea siderea is influenced by thermal stress and reef environment, but not ocean acidification. Front. Mar. Sci. 5, 1–14. https://doi.org/10.3389/fmars.2018.00150 (2018).

    Article  Google Scholar 

  • 66.

    Ladner, J. T., Barshis, D. J. & Palumbi, S. R. Protein evolution in two co-occurring types of Symbiodinium: an exploration into the genetic basis of thermal tolerance in Symbiodinium clade D. BMC Evol. Biol. 12, 217. https://doi.org/10.1186/1471-2148-12-217 (2012).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 67.

    Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359. https://doi.org/10.1038/nmeth.1923 (2012).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 68.

    Korneliussen, T. S., Albrechtsen, A. & Nielsen, R. ANGSD: Analysis of Next Generation Sequencing Data. BMC Bioinformatics 15, 356. https://doi.org/10.1186/s12859-014-0356-4 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  • 69.

    Peakall, R. & Smouse, P. E. GenALEx 65: Genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28, 2537–2539. https://doi.org/10.1093/bioinformatics/bts460 (2012).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 70.

    Excoffier, L., Smouse, P. E. & Quattro, J. M. Analysis of Molecular Variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491 (1992).

    PubMed  PubMed Central  CAS  Google Scholar 

  • 71.

    Benjamini, Y. & Hochberg, Y. Controlling the False Discovery Rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57, 289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x (1995).

    MathSciNet  MATH  Article  Google Scholar 

  • 72.

    Prevosti, A., Ocaña, J. & Alonso, G. Distances between populations of Drosophila subobscura, based on chromosome arrangement frequencies. Theor. Appl. Genet. 45, 231–241. https://doi.org/10.1007/BF00831894 (1975).

    PubMed  CAS  Article  Google Scholar 

  • 73.

    Kamvar, Z. N., Tabima, J. F. & Gr̈unwald, N. J. ,. Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2014, 1–14. https://doi.org/10.7717/peerj.281 (2014).

    Article  Google Scholar 

  • 74.

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

  • 75.

    Jombart, T. & Ahmed, I. adegenet 13–1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070–3071. https://doi.org/10.1093/bioinformatics/btr521 (2011).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 76.

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

    PubMed  CAS  Google Scholar 

  • 77.

    Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).

    PubMed  PubMed Central  CAS  Google Scholar 

  • 78.

    Besnier, F. & Glover, K. A. ParallelStructure: A R package to distribute parallel runs of the population genetics program STRUCTURE on multi-core computers. PLoS ONE 8, 1–5. https://doi.org/10.1371/journal.pone.0070651 (2013).

    CAS  Article  Google Scholar 

  • 79.

    Earl, D. A. & vonHoldt, B. M. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359–361. https://doi.org/10.1007/s12686-011-9548-7 (2012).

    Article  Google Scholar 

  • 80.

    Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A. & Cresko, W. A. Stacks: an analysis tool set for population genomics. Mol. Ecol. 22, 3124–3140. https://doi.org/10.1111/mec.12354 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  • 81.

    Pembleton, L. W., Cogan, N. O. I. & Forster, J. W. StAMPP: An R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Mol. Ecol. Resour. 13, 946–952. https://doi.org/10.1111/1755-0998.12129 (2013).

    PubMed  CAS  Article  Google Scholar 

  • 82.

    Oksanen, J. et al. Vegan: community ecology package. (2019).

  • 83.

    Alexander, D. H. D., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664. https://doi.org/10.1101/gr.094052.109 (2009).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 84.

    Skotte, L., Korneliussen, T. S. & Albrechtsen, A. Estimating individual admixture proportions from next generation sequencing data. Genetics 195, 693–702. https://doi.org/10.1534/genetics.113.154138 (2013).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 85.

    Foll, M. & Gaggiotti, O. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180, 977–993. https://doi.org/10.1534/genetics.108.092221 (2008).

    PubMed  PubMed Central  Article  Google Scholar 

  • 86.

    Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x (2005).

    PubMed  CAS  Article  Google Scholar 

  • 87.

    Centurioni, L. R. & Niiler, P. P. On the surface currents of the Caribbean Sea. Geophys. Res. Lett. 30, 10–13. https://doi.org/10.1029/2002GL016231 (2003).

    Article  Google Scholar 

  • 88.

    Candela, J. et al. The flow through the gulf of Mexico. J. Phys. Oceanogr. 49, 1381–1401. https://doi.org/10.1175/JPO-D-18-0189.1 (2019).

    ADS  Article  Google Scholar 

  • 89.

    Kourafalou, V., Androulidakis, Y., Le Hénaff, M. & Kang, H. S. The Dynamics of Cuba Anticyclones (CubANs) and interaction with the Loop Current/Florida Current system. J. Geophys. Res. Ocean. 122, 7897–7923. https://doi.org/10.1002/2017JC012928 (2017).

    ADS  Article  Google Scholar 

  • 90.

    Arriaza, L. et al. Marine current estimations in southeast Cuban shelf. Ser. Ocean. 4, 1–10 (2008).

    Google Scholar 

  • 91.

    Carracedo-Hidalgo, D., Reyes-Perdomo, D., Calzada-estrada, A., Chang-Domínguez, D. & Rodríguez-Pupo, A. Characterization of sea currents in sea adjacent to Cuba . Main trends in the last years. Rev. Cuba. Meteorol. 25, (2019).

  • 92.

    Frys, C. et al. Fine-scale coral connectivity pathways in the Florida Reef Tract: implications for conservation and restoration. Front. Mar. Sci. 7, 1–42. https://doi.org/10.3389/fmars.2020.00312 (2020).

    Article  Google Scholar 

  • 93.

    Kuba, A. Transgenerational effects of thermal stress: impacts on and beyond coral reproduction. (Nova Southeastern University, 2016).

  • 94.

    Claro, R., Lindeman, K. C., Kough, A. S. & Paris, C. B. Biophysical connectivity of snapper spawning aggregations and marine protected area management alternatives in Cuba. Fish. Oceanogr. 28, 33–42. https://doi.org/10.1111/fog.12384 (2019).

    Article  Google Scholar 

  • 95.

    Holstein, D. M., Paris, C. B. & Mumby, P. J. Consistency and inconsistency in multispecies population network dynamics of coral reef ecosystems. Mar. Ecol. Prog. Ser. 499, 1–18. https://doi.org/10.3354/meps10647 (2014).

    ADS  Article  Google Scholar 

  • 96.

    Szmant, A. M. Reproductive ecology of Caribbean reef corals. Coral Reefs 5, 43–53. https://doi.org/10.1007/BF00302170 (1986).

    ADS  Article  Google Scholar 

  • 97.

    Drury, C. et al. Genomic variation among populations of threatened coral: Acropora cervicornis. BMC Genomics 17, 286. https://doi.org/10.1186/s12864-016-2583-8 (2016).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 98.

    Devlin-Durante, M. K. & Baums, I. B. 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. https://doi.org/10.7717/peerj.4077 (2017).

    PubMed  CAS  Article  Google Scholar 

  • 99.

    Wang, J., Feng, C., Jiao, T., Von Wettberg, E. B. & Kang, M. Genomic signature of adaptive divergence despite strong nonadaptive forces on Edaphic Islands: a case study of Primulina juliae. Genome Biol. Evol. 9, 3495–3508. https://doi.org/10.1093/gbe/evx263 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  • 100.

    Ramos-Silva, P. et al. The skeletal proteome of the coral Acropora millepora: the evolution of calcification by co-option and domain shuffling. Mol. Biol. Evol. 30, 2099–2112. https://doi.org/10.1093/molbev/mst109 (2013).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 101.

    Takeuchi, T., Yamada, L., Shinzato, C., Sawada, H. & Satoh, N. Stepwise evolution of coral biomineralization revealed with genome-wide proteomics and transcriptomics. PLoS ONE https://doi.org/10.1371/journal.pone.0156424 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  • 102.

    Aranda, M. et al. Differential sensitivity of coral larvae to natural levels of ultraviolet radiation during the onset of larval competence. Mol. Ecol. 20, 2955–2972. https://doi.org/10.1111/j.1365-294X.2011.05153.x (2011).

    PubMed  CAS  Article  Google Scholar 

  • 103.

    Reynolds, W. S., Schwarz, J. A. & Weis, V. M. Symbiosis-enhanced gene expression in cnidarian-algal associations: cloning and characterization of a cDNA, sym32, encoding a possible cell adhesion protein. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 126, 33–44. https://doi.org/10.1016/S0742-8413(00)00099-2 (2000).

    CAS  Article  Google Scholar 

  • 104.

    Iguchi, A. et al. Apparent involvement of a β1 type integrin in coral fertilization. Mar. Biotechnol. 9, 760–765. https://doi.org/10.1007/s10126-007-9026-0 (2007).

    PubMed  CAS  Article  Google Scholar 

  • 105.

    Lesser, M. P. et al. Photoacclimatization by the coral Montastraea cavernosa in the mesophotic zone: light, food, and genetics. Ecology 91, 990–1003. https://doi.org/10.1890/09-0313.1 (2010).

    PubMed  Article  Google Scholar 

  • 106.

    Klepac, C. et al. Seasonal stability of coral-Symbiodinium associations in the subtropical coral habitat of St. Lucie Reef, Florida. Mar. Ecol. Prog. Ser. 532, 137–151. https://doi.org/10.3354/meps11369 (2015).

    ADS  Article  Google Scholar 

  • 107.

    Polinski, J. M. & Voss, J. D. Evidence of photoacclimatization at mesophotic depths in the coral-Symbiodinium symbiosis at Flower Garden Banks National Marine Sanctuary and McGrail Bank. Coral Reefs 37, 779–789. https://doi.org/10.1007/s00338-018-1701-2 (2018).

    ADS  Article  Google Scholar 

  • 108.

    LaJeunesse, T. C. et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 1–11. https://doi.org/10.1016/j.cub.2018.07.008 (2018).

    CAS  Article  Google Scholar 

  • 109.

    Swain, T. D., Chandler, J., Backman, V. & Marcelino, L. Consensus thermotolerance ranking for 110 Symbiodinium phylotypes: an exemplar utilization of a novel iterative partial-rank aggregation tool with broad application potential. Funct. Ecol. 31, 172–183. https://doi.org/10.1111/1365-2435.12694 (2017).

    Article  Google Scholar 

  • 110.

    Hodel, R. G. J. et al. Adding loci improves phylogeographic resolution in red mangroves despite increased missing data: comparing microsatellites and RAD-Seq and investigating loci filtering. Sci. Rep. 7, 1–14. https://doi.org/10.1038/s41598-017-16810-7 (2017).

    CAS  Article  Google Scholar 

  • 111.

    Lemopoulos, A. et al. Comparing RADseq and microsatellites for estimating genetic diversity and relatedness — implications for brown trout conservation. Ecol. Evol. 9, 2106–2120. https://doi.org/10.1002/ece3.4905 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  • 112.

    Puckett, E. E. Variability in total project and per sample genotyping costs under varying study designs including with microsatellites or SNPs to answer conservation genetic questions. Conserv. Genet. Resour. 9, 289–304. https://doi.org/10.1007/s12686-016-0643-7 (2017).

    Article  Google Scholar 

  • 113.

    Hale, M. L., Burg, T. M. & Steeves, T. E. Sampling for microsatellite-based population genetic studies: 25 to 30 individuals per population is enough to accurately estimate allele frequencies. PLoS ONE 7, e45170. https://doi.org/10.1371/journal.pone.0045170 (2012).

    ADS  PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 114.

    Luikart, G., Sherwin, W. B., Steele, B. M. & Allendorf, F. W. Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Mol. Ecol. 7, 963–974. https://doi.org/10.1046/j.1365-294x.1998.00414.x (1998).

    PubMed  CAS  Article  Google Scholar 

  • 115.

    Willing, E.-M., Dreyer, C. & van Oosterhout, C. Estimates of genetic differentiation measured by FST do not necessarily require large sample sizes when using many SNP markers. PLoS ONE 7, e42649. https://doi.org/10.1371/journal.pone.0042649 (2012).

    ADS  PubMed  PubMed Central  CAS  Article  Google Scholar 

  • 116.

    Nazareno, A. G., Bemmels, J. B., Dick, C. W. & Lohmann, L. G. Minimum sample sizes for population genomics: an empirical study from an Amazonian plant species. Mol. Ecol. Resour. 17, 1136–1147. https://doi.org/10.1111/1755-0998.12654 (2017).

    PubMed  CAS  Article  Google Scholar 


  • Source: Ecology - nature.com

    Evaluating battery revenues for offshore wind farms using advanced modeling

    Phytoliths in selected broad-leaved trees in China