Palau’s warmest reefs harbor thermally tolerant corals that thrive across different habitats
Baker, A. C., Glynn, P. W. & Riegl, B. Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar. Coast Shelf Sci. 80, 435–471 (2008).Article
Google Scholar
Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).Article
CAS
Google Scholar
Normille, D. El Niño’s warmth devastating reefs worldwide. Science 352, 2015–2016 (2016).
Google Scholar
Morikawa, M. K. & Palumbi, S. R. Using naturally occurring climate resilient corals to construct bleaching-resistant nurseries. Proc Natl Acad Sci USA 116, 10586–10591 (2019).Safaie, A. et al. High frequency temperature variability reduces the risk of coral bleaching. Nat. Commun. 9, 1671 (2018).Article
Google Scholar
Thomas, L. et al. Mechanisms of thermal tolerance in Reef-building corals across a fine-grained environmental mosaic: lessons from Ofu. Am. Samoa. Front Mar. Sci. 4, 434 (2018).Article
Google Scholar
Kenkel, C. D., Meyer, E. & Matz, M. V. Gene expression under chronic heat stress in populations of the mustard hill coral (Porites astreoides) from different thermal environments. Mol. Ecol. 22, 4322–4334 (2013).Article
CAS
Google Scholar
Gomulkiewicz, R. & Holt, R. D. When does evolution by natural selection prevent extinction? Evolution 49, 201–207 (1995).
Google Scholar
Bruno, J. F., Siddon, C. E., Witman, J. D., Colin, P. L. & Toscano, M. A. El Niño related coral bleaching in Palau, western Caroline Islands. Coral Reefs 20, 127–136 (2001).Article
Google Scholar
Golbuu, Y. et al. Palau’s coral reefs show differential habitat recovery following the 1998-bleaching event. Coral Reefs 26, 319–332 (2007).Article
Google Scholar
van Woesik, R. et al. Climate-change refugia in the sheltered bays of Palau: analogs of future reefs. Ecol. Evol. 2, 2474–2484 (2012).Article
Google Scholar
Barkley, H. C. & Cohen, A. L. Skeletal records of community-level bleaching in Porites corals from Palau. Coral Reefs 35, 1407–1417 (2016).Article
Google Scholar
Gouezo, M. et al. Drivers of recovery and reassembly of coral reef communities. Proc. R. Soc. B Biol. Sci. 286, 20182908 (2019).Shamberger, K. E. F. et al. Diverse coral communities in naturally acidified waters of a Western Pacific reef. Geophys. Res. Lett. 41, 499–504 (2014).Article
Google Scholar
Barkley, H. C. et al. Changes in coral reef communities across a natural gradient in seawater pH. Sci. Adv. 1, e1500328 (2015).Article
Google Scholar
Fabricius, K. E., Mieog, J. C., Colin, P. L., Idip, D. & van Oppen, M. J. H. Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol. Ecol. 13, 2445–2458 (2004).Article
CAS
Google Scholar
Anthony, K. R. N., Kline, D. I., Diaz-Pulido, G., Dove, S. & Hoegh-Guldberg, O. Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc. Natl Acad. Sci. USA 105, 17442–17446 (2008).Article
CAS
Google Scholar
Gibbin, E. M., Putnam, H. M., Gates, R. D., Nitschke, M. R. & Davy, S. K. Species-specific differences in thermal tolerance may define susceptibility to intracellular acidosis in reef corals. Mar. Biol. 162, 717–723 (2015).Article
CAS
Google Scholar
Boulay, J. N., Hellberg, M. E., Cortés, J. & Baums, I. B. Unrecognized coral species diversity masks differences in functional ecology. Proc. R. Soc. B Biol. Sci. 281, 20131580 (2013).Baums, I. B., Boulay, J. N., Polato, N. R. & Hellberg, M. E. No gene flow across the Eastern Pacific Barrier in the reef-building coral Porites lobata. Mol. Ecol. 21, 5418–5433 (2012).Article
Google Scholar
Forsman, Z. H., Wellington, G. M., Fox, G. E. & Toonen, R. J. Clues to unraveling the coral species problem: Distinguishing species from geographic variation in Porites across the Pacific with molecular markers and microskeletal traits. PeerJ 3, e751 (2015).Article
Google Scholar
Levas, S. J., Grottoli, A. G., Hughes, A., Osburn, C. L. & Matsui, Y. Physiological and biogeochemical traits of bleaching and recovery in the mounding species of coral Porites lobata: implications for resilience in mounding corals. PLoS ONE 8, e63267 (2013).Article
CAS
Google Scholar
Linsley, B. K. et al. Coral carbon isotope sensitivity to growth rate and water depth with Paleo-sea level implications. Nat. Commun. 10, 1–9 (2019).
Google Scholar
Peyrot-Clausade, M., Hutchings, P. & Richard, G. Temporal variations of macroborers in massive Porites lobata on Moorea, French Polynesia. Coral Reefs 11, 161–166 (1992).Article
Google Scholar
Nanami, A. & Nishihira, M. Microhabitat association and temporal stability in reef fish assemblages on massive Porites microatolls. Ichthyol. Res. 51, 165–171 (2004).Article
Google Scholar
Cantin, N. E. & Lough, J. M. Surviving coral bleaching events: porites growth anomalies on the Great Barrier Reef. PLoS ONE 9, e88720 (2014).Article
Google Scholar
Carilli, J. E., Norris, R. D., Black, B., Walsh, S. M. & Mcfield, M. Century-scale records of coral growth rates indicate that local stressors reduce coral thermal tolerance threshold. Glob. Chang Biol. 16, 1247–1257 (2010).Article
Google Scholar
Cantin, N. E., Cohen, A. L., Karnauskas, K. B., Tarrant, A. M. & McCorkle, D. C. Ocean warming slows coral growth in the central Red Sea. Science 329, 322–325 (2010).Article
CAS
Google Scholar
Lough, J. M. & Cooper, T. F. New insights from coral growth band studies in an era of rapid environmental change. Earth Sci. Rev. 108, 170–184 (2011).Article
CAS
Google Scholar
Mollica, N. R. N. et al. Skeletal records of bleaching reveal different thermal thresholds of Pacific coral reef assemblages. Coral Reefs 38, 743–757 (2019).Article
Google Scholar
Barkley, H. C. et al. Repeat bleaching of a central Pacific coral reef over the past six decades (1960–2016). Commun. Biol. 1, 177 (2018).DeCarlo, T. M. & Cohen, A. L. Dissepiments, density bands and signatures of thermal stress in Porites skeletons. Coral Reefs 36, 749–761 (2017).Article
Google Scholar
DeCarlo, T. M. et al. Acclimatization of massive reef-building corals to consecutive heatwaves. Proc. R. Soc. B 286, 20190235 (2019).DeCarlo, T. M. The past century of coral bleaching in the Saudi Arabian central Red Sea. PeerJ 8, e10200 (2020).Article
Google Scholar
Silverstein, R. N., Cunning, R. & Baker, A. C. Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob. Chang Biol. 21, 236–249 (2015).Article
Google Scholar
Fabricius, K. E. Effects of irradiance, flow, and colony pigmentation on the temperature microenvironment around corals: Implications for coral bleaching? Limnol. Oceanogr. 51, 30–37 (2006).Article
Google Scholar
Edmunds, P. J., Putnam, H. M. & Gates, R. D. Photophysiological consequences of vertical stratification of Symbiodinium in tissue of the coral Porites lutea. Biol. Bull. 223, 226–235 (2012).Article
CAS
Google Scholar
Smith, L. W., Wirshing, H., Baker, A. C. & Birkeland, C. Environmental versus genetic influences on growth rates of the corals Pocillopora eydouxi and Porites lobata. Pac. Sci. 62, 57–69 (2008).Article
Google Scholar
Kenkel, C. D. & Bay, L. K. Exploring mechanisms that affect coral cooperation: symbiont transmission mode, cell density and community composition. PeerJ 2018, e6047 (2018).Article
Google Scholar
Sunde, J., Yıldırım, Y., Tibblin, P. & Forsman, A. Comparing the performance of microsatellites and RADseq in population genetic studies: analysis of data for Pike (Esox lucius) and a synthesis of previous studies. Front. Genet. 11, 218 (2020).Article
Google Scholar
Barkley, H. C., Cohen, A. L., McCorkle, D. C. & Golbuu, Y. Mechanisms and thresholds for pH tolerance in Palau corals. J. Exp. Mar. Biol. Ecol. 489, 7–14 (2017).Article
CAS
Google Scholar
Mollica, N. R. et al. Ocean acidification affects coral growth by reducing skeletal density. Proc. Natl Acad. Sci. USA 115, 1754–1759 (2018).Article
CAS
Google Scholar
DeCarlo, T. M. et al. Coral macrobioerosion is accelerated by ocean acidification and nutrients. Geology 43, 7–10 (2014).Article
Google Scholar
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. Chang Biol. 25, 1016–1031 (2019).Article
Google Scholar
Rippe, J. P., Dixon, G., Fuller, Z. L., Liao, Y. & Matz, M. Environmental specialization and cryptic genetic divergence in two massive coral species from the Florida Keys Reef Tract. Mol. Ecol. 1–17 https://doi.org/10.1111/mec.15931 (2021).Schoepf, V. et al. Thermally variable, macrotidal Reef habitats promote rapid recovery from mass coral bleaching. Front. Mar. Sci. 7, 245 (2020).Article
Google Scholar
Dixon, G. B. et al. Genomic determinants of coral heat tolerance across latitudes. Science 348, 1460–1462 (2015).Article
CAS
Google Scholar
Baums, I. B. et al. Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic. Ecol. Appl. 29, 1–23 (2019).Article
Google Scholar
Gosselin, L. A. & Qian, P.-Y. Juvenile mortality in benthic marine invertebrates. Mar. Ecol. Prog. Ser. 146, 265–282 (1997).Article
Google Scholar
Gouezo, M. et al. Modelled larval supply predicts coral population recovery potential following disturbance. Mar. Ecol. Prog. Ser. 661, 127–145 (2021).Golbuu, Y., Gouezo, M., Kurihara, H., Rehm, L. & Wolanski, E. Long-term isolation and local adaptation in Palau’s Nikko Bay help corals thrive in acidic waters. Coral Reefs 35, 909–918 (2016).Article
Google Scholar
Golbuu, Y. et al. Predicting coral recruitment in Palau’s complex reef archipelago. PLoS ONE 7, e50998 (2012).Article
CAS
Google Scholar
Barshis, D. J., Birkeland, C., Toonen, R. J., Gates, R. D. & Stillman, J. H. High-frequency temperature variability mirrors fixed differences in thermal limits of the massive coral Porites lobata (Dana, 1846). J. Exp. Biol. jeb.188581 https://doi.org/10.1242/jeb.188581 (2018).Shamberger, K. E. F., Lentz, S. J. & Cohen, A. L. Low and variable ecosystem calcification in a coral reef lagoon under natural acidification. Limnol. Oceanogr. https://doi.org/10.1002/lno.10662 (2017).Cacciapaglia, C. & van Woesik, R. Climate-change refugia: shading reef corals by turbidity. Glob. Chang Biol. 22, 1145–1154 (2016).Article
Google Scholar
Anthony, K. R. Enhanced energy status of corals on coastal, high-turbidity reefs. Mar. Ecol. Prog. Ser. 319, 111–116 (2006).Article
Google Scholar
Houlbrèque, F. & Ferrier-Pagès, C. Heterotrophy in tropical scleractinian corals. Biol. Rev. Camb. Philos. Soc. 84, 1–17 (2009).Article
Google Scholar
Aichelman, H. E. et al. Heterotrophy mitigates the response of the temperate coral Oculina arbuscula to temperature stress. Ecol. Evol. 6, 6758–6769 (2016).Article
Google Scholar
Gómez‐Corrales, M. & Prada, C. Cryptic lineages respond differently to coral bleaching. Mol. Ecol. 0, 1–9 (2020).
Google Scholar
Fifer, J. E., Yasuda, N., Yamakita, T., Bove, C. B. & Davies, S. W. Genetic divergence and range expansion in a western North Pacific coral. Sci. Total Environ. 152423 https://doi.org/10.1016/J.SCITOTENV.2021.152423 (2021).Euclide, P. T. et al. Attack of the PCR clones: rates of clonality have little effect on RAD-seq genotype calls. Mol. Ecol. Resour. 20, 66–78 (2020).Article
CAS
Google Scholar
Noonan, S. H. C., DiPerna, S., Hoogenboom, M. O. & Fabricius, K. E. Effects of variable daily light integrals and elevated CO2 on the adult and juvenile performance of two Acropora corals. Mar. Biol. 169, 1–15 (2022).Article
Google Scholar
Martins, C. P. P. et al. Growth response of reef-building corals to ocean acidification is mediated by interplay of taxon-specific physiological parameters. Front. Mar. Sci. 0, 879 (2022).
Google Scholar
Bairos-Novak, K. R., Hoogenboom, M. O., van Oppen, M. J. H. & Connolly, S. R. Coral adaptation to climate change: meta-analysis reveals high heritability across multiple traits. Glob. Chang. Biol. 27, 5694–5710 (2021).Article
CAS
Google Scholar
Kenkel, C. D., Setta, S. P. & Matz, M. V. Heritable differences in fitness-related traits among populations of the mustard hill coral, Porites astreoides. Heredity 115, 509–516 (2015).Article
CAS
Google Scholar
Dziedzic, K. E., Elder, H., Tavalire, H. & Meyer, E. Heritable variation in bleaching responses and its functional genomic basis in reef-building corals (Orbicella faveolata). Mol. Ecol. 28, 2238–2253 (2019).Article
Google Scholar
Quigley, K. M., Bay, L. K. & Oppen, M. J. H. Genome‐wide SNP analysis reveals an increase in adaptive genetic variation through selective breeding of coral. Mol. Ecol. 2176–2188 https://doi.org/10.1111/mec.15482 (2020).Veron, J. E. N. Corals of the World (Australian Institute of Marine Science, 2000).Polato, N. R., Concepcion, G. T., Toonen, R. J. & Baums, I. B. Isolation by distance across the Hawaiian Archipelago in the reef-building coral Porites lobata. Mol. Ecol. 19, 4661–4677 (2010).Article
CAS
Google Scholar
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 (2013).Article
Google Scholar
Puritz, J. B., Hollenbeck, C. M. & Gold, J. R. dDocent: a RADseq, variant-calling pipeline designed for population genomics of non-model organisms. PeerJ 2, e431 (2014).Article
Google Scholar
Li, W. & Godzik, A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659 (2006).Article
CAS
Google Scholar
Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. ArXiv (2013).Garrison, E. & Marth, G. Haplotype-based variant detection from short-read sequencing. ArXiv (2012).Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).Article
CAS
Google Scholar
Kopelman, N. M., Mayzel, J., Jakobsson, M. & Rosenberg, N. A. CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Mol. Ecol. Resour. 15, 1179–1191 (2015).Article
CAS
Google Scholar
Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).Article
CAS
Google Scholar
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 (2005).Article
CAS
Google Scholar
Puechmaille, S. J. 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 (2016).Article
Google Scholar
Jombart, T. & Ahmed, I. adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070–3071 (2011).Article
CAS
Google Scholar
Goudet, J. Hierfstat, a package for R to compute and test hierarchical F-statistics. Molecular Ecology Notes. 5, 184–186 (2005).Zeileis, A. & Grothendieck, G. zoo: S3 infrastructure for regular and irregular time series. J. Stat. Softw. 14, 1–27 (2005).Ryan, J. A. & Ulrich, J. M. xts: eXtensible Time Series. Package at https://cran.r-project.org/package=xts (2018).LaJeunesse, T. C. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar. Biol. 141, 387–400 (2002).Article
Google Scholar
LaJeunesse, T. C. & Trench, R. K. Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol. Bull. 199, 126–134 (2000).Article
CAS
Google Scholar More