1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Genetics
  4. Volume 57, 2023
  5. Article

Annual Review of Genetics

Volume 57, 2023

Coral Reef Population Genomics in an Age of Global Change

Abstract

Coral reefs are both exceptionally biodiverse and threatened by climate change and other human activities. Here, we review population genomic processes in coral reef taxa and their importance for understanding responses to global change. Many taxa on coral reefs are characterized by weak genetic drift, extensive gene flow, and strong selection from complex biotic and abiotic environments, which together present a fascinating test of microevolutionary theory. Selection, gene flow, and hybridization have played and will continue to play an important role in the adaptation or extinction of coral reef taxa in the face of rapid environmental change, but research remains exceptionally limited compared to the urgent needs. Critical areas for future investigation include understanding evolutionary potential and the mechanisms of local adaptation, developing historical baselines, and building greater research capacity in the countries where most reef diversity is concentrated.

Keyword(s): climate change, dispersal, evolutionary rescue, fish, local adaptation, population genetics
Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-022123-102748
2023-11-27
2024-05-04
Loading full text...

Full text loading...

/deliver/fulltext/genet/57/1/annurev-genet-022123-102748.html?itemId=/content/journals/10.1146/annurev-genet-022123-102748&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Allendorf FW. 1986. Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol. 5:2181–90
     [Google Scholar]
  2. 2.
    Almany GR, Planes S, Thorrold SR, Berumen ML, Bode M et al. 2017. Larval fish dispersal in a coral-reef seascape. Nat. Ecol. Evol. 1:60148
     [Google Scholar]
  3. 3.
    Apodaca JJ, Trexler JC, Jue NK, Schrader M, Travis J, McPeek MA. 2013. Large-scale natural disturbance alters genetic population structure of the sailfin molly, Poecilia latipinna. Am. Nat. 181:2254–63
     [Google Scholar]
  4. 4.
    Ayre DJ, Hughes TP. 2004. Climate change, genotypic diversity and gene flow in reef-building corals. Ecol. Lett. 7:4273–78
     [Google Scholar]
  5. 5.
    Baeza JA, Prakash S, Frolová P, Ďuriš Z, Anker A. 2023. Unweaving a hard taxonomic knot in coral reef dwellers: Integrative systematics reveals two parallel cryptic species complexes in ‘marbled’ shrimps of the genus Saron Thallwitz 1891 (Caridea: Hippolytidae). Coral Reefs 42:157–79
     [Google Scholar]
  6. 6.
    Bairos-Novak KR, Hoogenboom MO, Oppen MJH, Connolly SR. 2021. Coral adaptation to climate change: Meta-analysis reveals high heritability across multiple traits. Glob. Change Biol. 27:225694–710
     [Google Scholar]
  7. 7.
    Barber PH, Palumbi SR, Erdmann MV, Moosa MK. 2000. A marine Wallace's line?. Nature 406:692–93
     [Google Scholar]
  8. 8.
    Barfield S, Davies SW, Matz MV. 2023. Evidence of sweepstakes reproductive success in a broadcast-spawning coral and its implications for coral metapopulation persistence. Mol. Ecol. 32:3696–702
     [Google Scholar]
  9. 9.
    Bay RA, Palumbi SR. 2014. Multilocus adaptation associated with heat resistance in reef-building corals. Curr. Biol. 24:242952–56
     [Google Scholar]
  10. 10.
    Bell G. 2013. Evolutionary rescue and the limits of adaptation. Philos. Trans. R. Soc. B 368:161020120080
     [Google Scholar]
  11. 11.
    Bell JJ, Smith D, Hannan D, Haris A, Jompa J, Thomas L. 2014. Resilience to disturbance despite limited dispersal and self-recruitment in tropical barrel sponges: implications for conservation and management. PLOS ONE 9:3e91635
     [Google Scholar]
  12. 12.
    Bellwood DR, Goatley CHR, Bellwood O. 2017. The evolution of fishes and corals on reefs: form, function and interdependence. Biol. Rev. 92:2878–901
     [Google Scholar]
  13. 13.
    Bernard AM, Feldheim KA, Nemeth R, Kadison E, Blondeau J et al. 2016. The ups and downs of coral reef fishes: the genetic characteristics of a formerly severely overfished but currently recovering Nassau grouper fish spawning aggregation. Coral Reefs 35:273–84
     [Google Scholar]
  14. 14.
    Bernardi G. 2022. Inter-island local adaptation in the Galápagos Archipelago: genomics of the Galápagos blue-banded goby, Lythrypnus gilberti. Coral Reefs 41:3625–33
     [Google Scholar]
  15. 15.
    Bode M, Williamson DH, Harrison HB, Outram N, Jones GP. 2018. Estimating dispersal kernels using genetic parentage data. Methods Ecol. Evol. 9:3490–501
     [Google Scholar]
  16. 16.
    Bors EK, Herrera S, Morris JA Jr., Shank TM. 2019. Population genomics of rapidly invading lionfish in the Caribbean reveals signals of range expansion in the absence of spatial population structure. Ecol. Evol. 9:63306–20
     [Google Scholar]
  17. 17.
    Bourne SD, Hudson J, Holman LE, Rius M. 2018. Marine invasion genomics: revealing ecological and evolutionary consequences of biological invasions. Population Genomics: Marine Organisms MF Oleksiak, OP Rajora 363–98. Cham, Switz.: Springer Int. Publ.
     [Google Scholar]
  18. 18.
    Bowen BW, Rocha LA, Toonen RJ, Karl SA. 2013. The origins of tropical marine biodiversity. Trends Ecol. Evol. 28:6359–66
     [Google Scholar]
  19. 19.
    Budd AF, Pandolfi JM. 2010. Evolutionary novelty is concentrated at the edge of coral species distributions. Science 328:59851558–61
     [Google Scholar]
  20. 20.
    Buddemeier RW, Kleypas JA, Aronson RB. 2004. Coral reefs & global climate change: potential contributions of climate change to stresses on coral reef ecosystems Rep. Pew Cent. Glob. Clim. Change Arlington, VA:
  21. 21.
    Buffalo V, Coop G. 2020. Estimating the genome-wide contribution of selection to temporal allele frequency change. PNAS 117:3420672–80
     [Google Scholar]
  22. 22.
    Burgess SC, Baskett ML, Grosberg RK, Morgan SG, Strathmann RR. 2016. When is dispersal for dispersal? Unifying marine and terrestrial perspectives. Biol. Rev. 91:3867–82
     [Google Scholar]
  23. 23.
    Burgess SC, Johnston EC, Wyatt ASJ, Leichter JJ, Edmunds PJ. 2021. Response diversity in corals: hidden differences in bleaching mortality among cryptic Pocillopora species. Ecology 102:6e03324
     [Google Scholar]
  24. 24.
    Card DC, Shapiro B, Giribet G, Moritz C, Edwards SV. 2021. Museum genomics. Annu. Rev. Genet. 55:633–59
     [Google Scholar]
  25. 25.
    Carlson SM, Cunningham CJ, Westley PAH. 2014. Evolutionary rescue in a changing world. Trends Ecol. Evol. 29:9521–30
     [Google Scholar]
  26. 26.
    Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S et al. 2008. One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:5888560–63
     [Google Scholar]
  27. 27.
    Carradec Q, Poulain J, Boissin E, Hume BCC, Voolstra CR et al. 2020. A framework for in situ molecular characterization of coral holobionts using nanopore sequencing. Sci. Rep. 10:115893
     [Google Scholar]
  28. 28.
    Case TJ, Taper ML. 2000. Interspecific competition, environmental gradients, gene flow, and the coevolution of species’ borders. Am. Nat. 155:5583–605
     [Google Scholar]
  29. 29.
    Castillo KD, Ries JB, Weiss JM, Lima FP. 2012. Decline of forereef corals in response to recent warming linked to history of thermal exposure. Nat. Clim. Change 2:10756–60
     [Google Scholar]
  30. 30.
    Catalano KA, Dedrick AG, Stuart MR, Puritz JB, Montes HR, Pinsky ML. 2021. Quantifying dispersal variability among nearshore marine populations. Mol. Ecol. 30:102366–77
     [Google Scholar]
  31. 31.
    Chakravarti LJ, Beltran VH, van Oppen MJH. 2017. Rapid thermal adaptation in photosymbionts of reef-building corals. Glob. Change Biol. 23:114675–88
     [Google Scholar]
  32. 32.
    Chakravarti LJ, van Oppen MJH. 2018. Experimental evolution in coral photosymbionts as a tool to increase thermal tolerance. Front. Mar. Sci. 5:227
     [Google Scholar]
  33. 33.
    Chan WY, Peplow LM, Menéndez P, Hoffmann AA, van Oppen MJH. 2018. Interspecific hybridization may provide novel opportunities for coral reef restoration. Front. Mar. Sci. 5:160
     [Google Scholar]
  34. 34.
    Charlesworth B. 2009. Effective population size and patterns of molecular evolution and variation. Nat. Rev. Genet. 10:3195–205
     [Google Scholar]
  35. 35.
    Chaudhary C, Richardson AJ, Schoeman DS, Costello MJ. 2021. Global warming is causing a more pronounced dip in marine species richness around the equator. PNAS 118:15e2015094118
     [Google Scholar]
  36. 36.
    Christie MR, Marine ML, French RA, Waples RS, Blouin MS. 2012. Effective size of a wild salmonid population is greatly reduced by hatchery supplementation. Heredity 109:4254–60
     [Google Scholar]
  37. 37.
    Clark RD, Aardema ML, Andolfatto P, Barber PH, Hattori A et al. 2021. Genomic signatures of spatially divergent selection at clownfish range margins. Proc. R. Soc. B 288:20210407
     [Google Scholar]
  38. 38.
    Coleman RR, Gaither MR, Kimokeo B, Stanton FG, Bowen BW, Toonen RJ. 2014. Large-scale introduction of the Indo-Pacific damselfish Abudefduf vaigiensis into Hawai'i promotes genetic swamping of the endemic congener A. abdominalis. Mol. Ecol. 23:225552–65
     [Google Scholar]
  39. 39.
    Colin L, Yesson C, Head CEI. 2021. Complete mitochondrial genomes of three reef forming Acropora corals (Acroporidae, Scleractinia) from Chagos Archipelago, Indian Ocean. Biodivers. Data J. 9:e72762
     [Google Scholar]
  40. 40.
    Colton MA, McManus LC, Schindler DE, Mumby PJ, Palumbi SR et al. 2022. Coral conservation in a warming world must harness evolutionary adaptation. Nat. Ecol. Evol. 6:1405–7
     [Google Scholar]
  41. 41.
    Concepcion GT, Crepeau MW, Wagner D, Kahng SE, Toonen RJ. 2008. An alternative to ITS, a hypervariable, single-copy nuclear intron in corals, and its use in detecting cryptic species within the octocoral genus Carijoa. Coral Reefs 27:2323–36
     [Google Scholar]
  42. 42.
    Conover DO, Clarke LM, Munch SB, Wagner GN. 2006. Spatial and temporal scales of adaptive divergence in marine fishes and the implications for conservation. J. Fish Biol. 69:sc21–47
     [Google Scholar]
  43. 43.
    Cornuet JM, Luikart G. 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–14
     [Google Scholar]
  44. 44.
    Cornwell B, Armstrong K, Walker NS, Lippert M, Nestor V et al. 2021. Widespread variation in heat tolerance and symbiont load are associated with growth tradeoffs in the coral Acropora hyacinthus in Palau. eLife 10:e64790
     [Google Scholar]
  45. 45.
    Correa AMS, Baker AC. 2009. Understanding diversity in coral-algal symbiosis: a cluster-based approach to interpreting fine-scale genetic variation in the genus Symbiodinium. Coral Reefs 28:181–93
     [Google Scholar]
  46. 46.
    Costanza R, de Groot R, Sutton P, van der Ploeg S, Anderson SJ et al. 2014. Changes in the global value of ecosystem services. Glob. Environ. Change 26:152–58
     [Google Scholar]
  47. 47.
    Counsell C, Coleman R, Lal S, Bowen B, Franklin E et al. 2022. Interdisciplinary analysis of larval dispersal for a coral reef fish: opening the black box. Mar. Ecol. Prog. Ser. 684:117–32
     [Google Scholar]
  48. 48.
    Cowen LJ, Putnam HM. 2022. Bioinformatics of corals: investigating heterogeneous omics data from coral holobionts for insight into reef health and resilience. Annu. Rev. Biomed. Data Sci. 5:205–31
     [Google Scholar]
  49. 49.
    Cowman PF, Bellwood DR. 2013. Vicariance across major marine biogeographic barriers: temporal concordance and the relative intensity of hard versus soft barriers. Proc. R. Soc. B 280:176820131541
     [Google Scholar]
  50. 50.
    Coyne JA. 1994. Ernst Mayr and the Origin of Species. Evolution 48:119–30
     [Google Scholar]
  51. 51.
    Cros A, Toonen R, Karl SA. 2020. Is post-bleaching recovery of Acropora hyacinthus on Palau via spread of local kin groups?. Coral Reefs 39:3687–99
     [Google Scholar]
  52. 52.
    Cruse-Sanders JM, Hamrick JL. 2004. Genetic diversity in harvested and protected populations of wild American ginseng, Panax quinquefolius L. (Araliaceae). Am. J. Bot. 91:4540–48
     [Google Scholar]
  53. 53.
    Culumber ZW, Anaya-Rojas JM, Booker WW, Hooks AP, Lange EC et al. 2019. Widespread biases in ecological and evolutionary studies. BioScience 69:8631–40
     [Google Scholar]
  54. 54.
    Cure K, Thomas L, Hobbs J-PA, Fairclough DV, Kennington WJ. 2017. Genomic signatures of local adaptation reveal source-sink dynamics in a high gene flow fish species. Sci. Rep. 7:18618
     [Google Scholar]
  55. 55.
    D'Aloia CC, Bogdanowicz SM, Francis RK, Majoris JE, Harrison RG, Buston PM. 2015. Patterns, causes, and consequences of marine larval dispersal. PNAS 112:4513940–45
     [Google Scholar]
  56. 56.
    D'Angelo C, Hume BCC, Burt J, Smith EG, Achterberg EP, Wiedenmann J 2015. Local adaptation constrains the distribution potential of heat-tolerant Symbiodinium from the Persian/Arabian Gulf. ISME J. 9:122551–60
     [Google Scholar]
  57. 57.
    Davies SW, Treml EA, Kenkel CD, Matz MV. 2015. Exploring the role of Micronesian islands in the maintenance of coral genetic diversity in the Pacific Ocean. Mol. Ecol. 24:170–82
     [Google Scholar]
  58. 58.
    Dixon GB, Davies SW, Aglyamova GV, Meyer E, Bay LK, Matz MV. 2015. Genomic determinants of coral heat tolerance across latitudes. Science 348:62421460–62
     [Google Scholar]
  59. 59.
    Duffy JE. 1996. Resource-associated population subdivision in a symbiotic coral-reef shrimp. Evolution 50:1360–73
     [Google Scholar]
  60. 60.
    Duran S, Rützler K. 2006. Ecological speciation in a Caribbean marine sponge. Mol. Phylogenet. Evol. 40:1292–97
     [Google Scholar]
  61. 61.
    Eirin-Lopez JM, Putnam HM. 2018. Marine environmental epigenetics. Annu. Rev. Mar. Sci. 11:335–68
     [Google Scholar]
  62. 62.
    Eldon B, Riquet F, Yearsley J, Jollivet D, Broquet T. 2016. Current hypotheses to explain genetic chaos under the sea. Curr. Zool. 62:6551–66
     [Google Scholar]
  63. 63.
    Etterson JR, Shaw RG. 2001. Constraint to adaptive evolution in response to global warming. Science 294:5540151–54
     [Google Scholar]
  64. 64.
    Excoffier L, Ray N. 2008. Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol. Evol. 23:7347–51
     [Google Scholar]
  65. 65.
    Faucci A, Toonen RJ, Hadfield MG. 2007. Host shift and speciation in a coral-feeding nudibranch. Proc. R. Soc. B 274:1606111–19
     [Google Scholar]
  66. 66.
    Faulk C. 2023. De novo sequencing, diploid assembly, and annotation of the black carpenter ant, Camponotus pennsylvanicus, and its symbionts by one person for $1000, using nanopore sequencing. Nucleic Acids Res. 51:117–28
     [Google Scholar]
  67. 67.
    Fauvelot C, Bernardi G, Planes S. 2003. Reductions in the mitochondrial DNA diversity of coral reef fish provide evidence of population bottlenecks resulting from Holocene sea-level change. Evolution 57:71571–83
     [Google Scholar]
  68. 68.
    Ferrario F, Beck MW, Storlazzi CD, Micheli F, Shepard CC, Airoldi L. 2014. The effectiveness of coral reefs for coastal hazard risk reduction and adaptation. Nat. Commun. 5:13794
     [Google Scholar]
  69. 69.
    Fifer JE, Yasuda N, Yamakita T, Bove CB, Davies SW. 2022. Genetic divergence and range expansion in a western North Pacific coral. Sci. Total Environ. 813:152423
     [Google Scholar]
  70. 70.
    Figueira WF, Booth DJ. 2010. Increasing ocean temperatures allow tropical fishes to survive overwinter in temperate waters. Glob. Change Biol. 16:2506–16
     [Google Scholar]
  71. 71.
    Figueiredo J, Thomas CJ, Deleersnijder E, Lambrechts J, Baird AH et al. 2022. Global warming decreases connectivity among coral populations. Nat. Clim. Change 12:183–87
     [Google Scholar]
  72. 72.
    Fisher R, Radford BT, Knowlton N, Brainard RE, Michaelis FB, Caley MJ. 2011. Global mismatch between research effort and conservation needs of tropical coral reefs: global distribution of coral reef research. Conserv. Lett. 4:164–72
     [Google Scholar]
  73. 73.
    Fitz KS, Montes HR, Thompson DM, Pinsky ML. 2023. Isolation-by-distance and isolation-by-oceanography in Maroon Anemonefish (Amphiprion biaculeatus). Evol. Appl. 16:2379–92
     [Google Scholar]
  74. 74.
    Foote AD. 2018. Sympatric speciation in the Genomic Era. Trends Ecol. Evol. 33:285–95
     [Google Scholar]
  75. 75.
    Frieler K, Meinshausen M, Golly A, Mengel M, Lebek K et al. 2013. Limiting global warming to 2°C is unlikely to save most coral reefs. Nat. Clim. Change 3:165–70
     [Google Scholar]
  76. 76.
    Fuller ZL, Mocellin VJL, Morris LA, Cantin N, Shepherd J et al. 2020. Population genetics of the coral Acropora millepora: toward genomic prediction of bleaching. Science 369:6501eaba4674
     [Google Scholar]
  77. 77.
    García-Dorado A, Caballero A. 2021. Neutral genetic diversity as a useful tool for conservation biology. Conserv. Genet. 22:541–45
     [Google Scholar]
  78. 78.
    Gardiner NM, Munday PL, Nilsson GE. 2010. Counter-gradient variation in respiratory performance of coral reef fishes at elevated temperatures. PLOS ONE 5:10e13299
     [Google Scholar]
  79. 79.
    Gattuso J-P, Hoegh-Guldberg O, Pörtner HO 2014. Cross-chapter box on coral reefs. Climate Change 2014: Impacts, Adaptation, and Vulnerability, Part A: Global and Sectoral Aspects CB Field, VR Barros, DJ Dokken, KJ Mach, MD Mastrandrea, et al. 97–100. Cambridge, UK: Cambridge Univ. Press
     [Google Scholar]
  80. 80.
    Glasby CJ, Wei N-WV, Gibb KS. 2013. Cryptic species of Nereididae (Annelida: Polychaeta) on Australian coral reefs. Invertebr. Syst. 27:3245–64
     [Google Scholar]
  81. 81.
    Gomez Cabrera MdC, Young JM, Roff G, Staples T, Ortiz JC et al. 2019. Broadening the taxonomic scope of coral reef palaeoecological studies using ancient DNA. Mol. Ecol. 28:102636–52
     [Google Scholar]
  82. 82.
    Gómez-Corrales M, Prada C. 2020. Cryptic lineages respond differently to coral bleaching. Mol. Ecol. 29:224265–73
     [Google Scholar]
  83. 83.
    Gomulkiewicz R, Holt RD. 1995. When does evolution by natural selection prevent extinction?. Evolution 49:1201–7
     [Google Scholar]
  84. 84.
    Grabenstein KC, Taylor SA. 2018. Breaking barriers: causes, consequences, and experimental utility of human-mediated hybridization. Trends Ecol. Evol. 33:3198–212
     [Google Scholar]
  85. 85.
    Grealy A, Douglass K, Haile J, Bruwer C, Gough C, Bunce M. 2016. Tropical ancient DNA from bulk archaeological fish bone reveals the subsistence practices of a historic coastal community in southwest Madagascar. J. Archaeol. Sci. 75:82–88
     [Google Scholar]
  86. 86.
    Greiner A, Andrello M, Darling E, Krkošek M, Fortin M. 2022. Limited spatial rescue potential for coral reefs lost to future climate warming. Glob. Ecol. Biogeogr. 31:112245–58
     [Google Scholar]
  87. 87.
    Hager ER, Harringmeyer OS, Wooldridge TB, Theingi S, Gable JT et al. 2022. A chromosomal inversion contributes to divergence in multiple traits between deer mouse ecotypes. Science 377:6604399–405
     [Google Scholar]
  88. 88.
    Hallatschek O, Nelson DR. 2008. Gene surfing in expanding populations. Theor. Popul. Biol. 73:1158–70
     [Google Scholar]
  89. 89.
    Harrison HB, Berumen ML, Saenz-Agudelo P, Salas E, Williamson DH, Jones GP. 2017. Widespread hybridization and bidirectional introgression in sympatric species of coral reef fish. Mol. Ecol. 26:205692–704
     [Google Scholar]
  90. 90.
    Harrisson KA, Pavlova A, Telonis-Scott M, Sunnucks P. 2014. Using genomics to characterize evolutionary potential for conservation of wild populations. Evol. Appl. 7:91008–25
     [Google Scholar]
  91. 91.
    Hausfather Z, Peters GP. 2020. Emissions—the ‘business as usual’ story is misleading. Nature 577:7792618–20
     [Google Scholar]
  92. 92.
    Hays CG, Hanley TC, Hughes AR, Truskey SB, Zerebecki RA, Sotka EE. 2021. Local adaptation in marine foundation species at microgeographic scales. Biol. Bull. 241:116–29
     [Google Scholar]
  93. 93.
    Hedgecock D. 1994. Does variance in reproductive success limit effective population sizes of marine organisms?. Genetics and Evolution of Aquatic Organisms A Beaumont 122–34. London: Chapman & Hall
     [Google Scholar]
  94. 94.
    Hemond EM, Vollmer SV. 2010. Genetic diversity and connectivity in the threatened staghorn coral (Acropora cervicornis) in Florida. PLOS ONE 5:1e8652
     [Google Scholar]
  95. 95.
    Hench K, Helmkampf M, McMillan WO, Puebla O. 2022. Rapid radiation in a highly diverse marine environment. PNAS 119:4e2020457119
     [Google Scholar]
  96. 96.
    Hobbs J-PA, Richards ZT, Popovic I, Lei C, Staeudle TM et al. 2022. Hybridisation and the evolution of coral reef biodiversity. Coral Reefs 41:3535–49
     [Google Scholar]
  97. 97.
    Hodge JR, Bellwood DR. 2016. The geography of speciation in coral reef fishes: the relative importance of biogeographical barriers in separating sister-species. J. Biogeogr. 43:71324–35
     [Google Scholar]
  98. 98.
    Hoegh-Guldberg O, Beal D, Chaudhry T, Elhaj H, Abdullat A et al. 2015. Reviving the Ocean Economy: The Case for Action Gland, Switz: WWF Int.
  99. 99.
    Hoegh-Guldberg O, Hughes L, Lindenmayer DB, McIntyre S, Parmesan C et al. 2008. Assisted colonization and rapid climate change. Science 321:345–46
     [Google Scholar]
  100. 100.
    Hoegh-Guldberg O, Ortiz JC, Dove S. 2011. The future of coral reefs. Science 334:60621494–95
     [Google Scholar]
  101. 101.
    Hofreiter M, Paijmans JLA, Goodchild H, Speller CF, Barlow A et al. 2015. The future of ancient DNA: technical advances and conceptual shifts. BioEssays 37:3284–93
     [Google Scholar]
  102. 102.
    Hopkinson BM, King AC, Owen DP, Johnson-Roberson M, Long MH, Bhandarkar SM. 2020. Automated classification of three-dimensional reconstructions of coral reefs using convolutional neural networks. PLOS ONE 15:3e0230671
     [Google Scholar]
  103. 103.
    Howells EJ, Abrego D, Liew YJ, Burt JA, Meyer E, Aranda M. 2021. Enhancing the heat tolerance of reef-building corals to future warming. Sci. Adv. 7:34eabg6070
     [Google Scholar]
  104. 104.
    Howells EJ, Abrego D, Meyer E, Kirk NL, Burt JA. 2016. Host adaptation and unexpected symbiont partners enable reef-building corals to tolerate extreme temperatures. Glob. Change Biol. 22:82702–14
     [Google Scholar]
  105. 105.
    Hubert N, Meyer CP, Bruggemann HJ, Guérin F, Komeno RJL et al. 2012. Cryptic diversity in Indo-Pacific coral-reef fishes revealed by DNA-barcoding provides new support to the centre-of-overlap hypothesis. PLOS ONE 7:3e28987
     [Google Scholar]
  106. 106.
    Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT et al. 2018. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 5:8080–83
     [Google Scholar]
  107. 107.
    Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS et al. 2017. Coral reefs in the Anthropocene. Nature 546:765682–90
     [Google Scholar]
  108. 108.
    Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD et al. 2017. Global warming and recurrent mass bleaching of corals. Nature 543:7645373–77
     [Google Scholar]
  109. 109.
    IPCC 2022. Global Warming of 1.5°C Cambridge, UK: Cambridge Univ. Press
  110. 110.
    Johnson JA, Bellinger MR, Toepfer JE, Dunn P. 2004. Temporal changes in allele frequencies and low effective population size in greater prairie-chickens. Mol. Ecol. 13:92617–30
     [Google Scholar]
  111. 111.
    Kawecki TJ, Ebert D. 2004. Conceptual issues in local adaptation. Ecol. Lett. 7:121225–41
     [Google Scholar]
  112. 112.
    Kenkel CD, Almanza AT, Matz MV. 2015. Fine-scale environmental specialization of reef-building corals might be limiting reef recovery in the Florida Keys. Ecology 96:123197–212
     [Google Scholar]
  113. 113.
    Kenton MI. 2021. A test of rad capture sequencing on ethanol-preserved centennial and contemporary specimens of Philippine fishes MS Thesis Old Dominion Univ. Norfolk, VA:
  114. 114.
    Keyse J, Crandall ED, Toonen RJ, Meyer CP, Treml EA, Riginos C. 2014. The scope of published population genetic data for Indo-Pacific marine fauna and future research opportunities in the region. Bull. Mar. Sci. 90:147–78
     [Google Scholar]
  115. 115.
    Kim E, Lasker HR, Coffroth MA, Kim K. 2004. Morphological and genetic variation across reef habitats in a broadcast-spawning octocoral. Hydrobiologia 530:423–32
     [Google Scholar]
  116. 116.
    Kinlan BP, Gaines SD. 2003. Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:82007–20
     [Google Scholar]
  117. 117.
    Kirkpatrick M, Peischl S. 2013. Evolutionary rescue by beneficial mutations in environments that change in space and time. Philos. Trans. R. Soc. B. 368:161020120082
     [Google Scholar]
  118. 118.
    Kleypas JA, Thompson DM, Castruccio FS, Curchitser EN, Pinsky ML, Watson JR. 2016. Larval connectivity across temperature gradients and its potential effect on heat tolerance in coral populations. Glob. Change Biol. 22:113539–49
     [Google Scholar]
  119. 119.
    Knowlton N, Leray M. 2015. Exploring coral reefs using the tools of molecular genetics. Coral Reefs in the Anthropocene117–32. Dordrecht, Neth.: Springer
     [Google Scholar]
  120. 120.
    Kurihara H, Watanabe A, Tsugi A, Mimura I, Hongo C et al. 2021. Potential local adaptation of corals at acidified and warmed Nikko Bay, Palau. Sci. Rep. 11:111192
     [Google Scholar]
  121. 121.
    Lacson JM, Morizot DC. 1991. Temporal genetic variation in subpopulations of bicolor damselfish (Stegastes partitus) inhabiting coral reefs in the Florida Keys. Mar. Biol. 110:353–57
     [Google Scholar]
  122. 122.
    Ladner JT, Palumbi SR. 2012. Extensive sympatry, cryptic diversity and introgression throughout the geographic distribution of two coral species complexes: geographic patterns of diversity and introgression. Mol. Ecol. 21:92224–38
     [Google Scholar]
  123. 123.
    Leis JM, Wright KJ, Johnson RN. 2007. Behaviour that influences dispersal and connectivity in the small, young larvae of a reef fish. Mar. Biol. 153:1103–17
     [Google Scholar]
  124. 124.
    Leprieur F, Colosio S, Descombes P, Parravicini V, Kulbicki M et al. 2016. Historical and contemporary determinants of global phylogenetic structure in tropical reef fish faunas. Ecography 39:9825–35
     [Google Scholar]
  125. 125.
    Leray M, Beldade R, Holbrook SJ, Schmitt RJ, Planes S, Bernardi G. 2010. Allopatric divergence and speciation in coral reef fish: the three-spot dascyllus, Dascyllus trimaculatus, species complex. Evolution 64:51218–30
     [Google Scholar]
  126. 126.
    Lesser MP, Stat M, Gates RD. 2013. The endosymbiotic dinoflagellates (Symbiodinium sp.) of corals are parasites and mutualists. Coral Reefs 32:3603–11
     [Google Scholar]
  127. 127.
    Levene H. 1953. Genetic equilibrium when more than one ecological niche is available. Am. Nat. 87:836331–33
     [Google Scholar]
  128. 128.
    Levin RA, Voolstra CR, Agrawal S, Steinberg PD, Suggett DJ, van Oppen MJH. 2017. Engineering strategies to decode and enhance the genomes of coral symbionts. Front. Microbiol. 8:1220
     [Google Scholar]
  129. 129.
    Leydet KP, Grupstra CGB, Coma R, Ribes M, Hellberg ME. 2018. Host-targeted RAD-Seq reveals genetic changes in the coral Oculina patagonica associated with range expansion along the Spanish Mediterranean coast. Mol. Ecol. 27:112529–43
     [Google Scholar]
  130. 130.
    Li J, Knapp DE, Fabina NS, Kennedy EV, Larsen K et al. 2020. A global coral reef probability map generated using convolutional neural networks. Coral Reefs 39:61805–15
     [Google Scholar]
  131. 131.
    Liggins L, Treml EA, Riginos C. 2020. Seascape genomics: contextualizing adaptive and neutral genomic variation in the ocean environment. Population Genomics: Marine Organisms171–217. Cham, Switz: Springer Int. Publ.
     [Google Scholar]
  132. 132.
    Llorens TM, Tapper S-L, Coates DJ, McArthur S, Hankinson M, Byrne M. 2017. Does population distribution matter? Influence of a patchy versus continuous distribution on genetic patterns in a wind-pollinated shrub. J. Biogeogr. 44:2361–74
     [Google Scholar]
  133. 133.
    Lo-Yat A, Simpson SD, Meekan M, Lecchini D, Martinez E, Clark R. 2011. Extreme climatic events reduce ocean productivity and larval supply in a tropical reef ecosystem. Glob. Change Biol. 17:41695–702
     [Google Scholar]
  134. 134.
    Ludt WB, Rocha LA. 2015. Shifting seas: the impacts of Pleistocene sea-level fluctuations on the evolution of tropical marine taxa. J. Biogeogr. 42:125–38
     [Google Scholar]
  135. 135.
    Majoris JE, Catalano KA, Scolaro D, Atema J, Buston PM. 2019. Ontogeny of larval swimming abilities in three species of coral reef fishes and a hypothesis for their impact on the spatial scale of dispersal. Mar. Biol. 166:12159
     [Google Scholar]
  136. 136.
    Majoris JE, Foretich MA, Hu Y, Nickles KR, Di Persia CL et al. 2021. An integrative investigation of sensory organ development and orientation behavior throughout the larval phase of a coral reef fish. Sci. Rep. 11:112377
     [Google Scholar]
  137. 137.
    Malay MCMD, Paulay G. 2010. Peripatric speciation drives diversification and distributional pattern of reef hermit crabs (Decapoda: Diogenidae: Calcinus). Evolution 64:3634–62
     [Google Scholar]
  138. 138.
    Mao Y. 2020. Genomic insights into hybridization of reef corals. Coral Reefs 39:161–67
     [Google Scholar]
  139. 139.
    Marhaver KL, Vermeij MJA, Rohwer F, Sandin SA. 2013. Janzen-Connell effects in a broadcast-spawning Caribbean coral: distance-dependent survival of larvae and settlers. Ecology 94:1146–60
     [Google Scholar]
  140. 140.
    Marshall DJ, Monro K, Bode M, Keough MJ, Swearer SE. 2010. Phenotype–environment mismatches reduce connectivity in the sea. Ecol. Lett. 13:1128–40
     [Google Scholar]
  141. 141.
    Matz MV, Treml EA, Haller BC. 2020. Estimating the potential for coral adaptation to global warming across the Indo-West Pacific. Glob. Change Biol. 26:63473–81
     [Google Scholar]
  142. 142.
    McManus LC, Forrest DL, Tekwa EW, Schindler DE, Colton MA et al. 2021. Evolution and connectivity influence the persistence and recovery of coral reefs under climate change in the Caribbean, Southwest Pacific, and Coral Triangle. Glob. Change Biol. 27:184307–21
     [Google Scholar]
  143. 143.
    McManus LC, Tekwa EW, Schindler DE, Walsworth TE, Colton MA et al. 2021. Evolution reverses the effect of network structure on metapopulation persistence. Ecology 102:7e03381
     [Google Scholar]
  144. 144.
    Moberg F, Folke C. 1999. Ecological goods and services of coral reef ecosystems. Ecol. Econ. 29:2215–33
     [Google Scholar]
  145. 145.
    Molina AN, Pulgar JM, Rezende EL, Carter MJ. 2023. Heat tolerance of marine ectotherms in a warming Antarctica. Glob. Change Biol. 29:1179–88
     [Google Scholar]
  146. 146.
    Montanari SR, Hobbs J-PA, Pratchett MS, Bay LK, Van Herwerden L. 2014. Does genetic distance between parental species influence outcomes of hybridization among coral reef butterflyfishes?. Mol. Ecol. 23:112757–70
     [Google Scholar]
  147. 147.
    Montano S, Maggioni D, Galli P, Hoeksema BW. 2017. A cryptic species in the Pteroclava krempfi species complex (Hydrozoa, Cladocorynidae) revealed in the Caribbean. Mar. Biodivers 47:183–89
     [Google Scholar]
  148. 148.
    Muir PR, Wallace CC, Done TJ, Aguirre JD. 2015. Limited scope for latitudinal extension of reef corals. Science 348:62391135–38
     [Google Scholar]
  149. 149.
    Mullen SP, Little K, Draud M, Brozek J, Itzkowitz M. 2012. Hybridization among Caribbean damselfish species correlates with habitat degradation. J. Exp. Mar. Biol. Ecol. 416–417:221–29
     [Google Scholar]
  150. 150.
    Munday PL, Jones GP, Pratchett MS, Williams AJ. 2008. Climate change and the future for coral reef fishes. Fish. 9:3261–85
     [Google Scholar]
  151. 151.
    Munday PL, van Herwerden L, Dudgeon CL. 2004. Evidence for sympatric speciation by host shift in the sea. Curr. Biol. 14:161498–504
     [Google Scholar]
  152. 152.
    Muñoz MM. 2022. The Bogert effect, a factor in evolution. Evolution 76:S149–66
     [Google Scholar]
  153. 153.
    Nakabayashi A, Yamakita T, Nakamura T, Aizawa H, Kitano YF et al. 2019. The potential role of temperate Japanese regions as refugia for the coral Acropora hyacinthus in the face of climate change. Sci. Rep. 9:11892
     [Google Scholar]
  154. 154.
    Nakamura Y, Feary DA, Kanda M, Yamaoka K. 2013. Tropical fishes dominate temperate reef fish communities within western Japan. PLOS ONE 8:12e81107
     [Google Scholar]
  155. 155.
    NASEM 2019. A Research Review of Interventions to Increase the Persistence and Resilience of Coral Reefs Washington, DC: Natl. Acad. Press
  156. 156.
    Natl. Acad. Sci. Eng. Med 2019. A Decision Framework for Interventions to Increase the Persistence and Resilience of Coral Reefs Washington, DC: Natl. Acad. Press
  157. 157.
    Norberg J, Urban MC, Vellend M, Klausmeier CA, Loeuille N. 2012. Eco-evolutionary responses of biodiversity to climate change. Nat. Clim. Change 2:10747–51
     [Google Scholar]
  158. 158.
    Nunes FLD, Norris RD, Knowlton N. 2011. Long distance dispersal and connectivity in amphi-Atlantic corals at regional and basin scales. PLOS ONE 6:7e22298
     [Google Scholar]
  159. 159.
    Nunney L. 1993. The influence of mating system and overlapping generations on effective population size. Evolution 47:51329–41
     [Google Scholar]
  160. 160.
    O'Dea A, Lessios HA, Coates AG, Eytan RI, Restrepo-Moreno SA et al. 2016. Formation of the Isthmus of Panama. Sci. Adv. 2:8e1600883
     [Google Scholar]
  161. 161.
    Paez S, Kraus RHS, Shapiro B, Gilbert MTP, Jarvis ED et al. 2022. Reference genomes for conservation. Science 377:6604364–66
     [Google Scholar]
  162. 162.
    Palstra FP, Ruzzante DE. 2008. Genetic estimates of contemporary effective population size: What can they tell us about the importance of genetic stochasticity for wild population persistence?. Mol. Ecol. 17:153428–47
     [Google Scholar]
  163. 163.
    Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA. 2014. Mechanisms of reef coral resistance to future climate change. Science 344:6186895–98
     [Google Scholar]
  164. 164.
    Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL. 2011. Projecting coral reef futures under global warming and ocean acidification. Science 333:6041418–22
     [Google Scholar]
  165. 165.
    Pandolfi JM, Kiessling W. 2014. Gaining insights from past reefs to inform understanding of coral reef response to global climate change. Curr. Opin. Environ. Sustain 7:52–58
     [Google Scholar]
  166. 166.
    Parkinson JE, Baker AC, Baums IB. 2020. Molecular tools for coral reef restoration: beyond biomarker discovery. Conserv. Lett. 13:e12687
     [Google Scholar]
  167. 167.
    Pease CM, Lande R, Bull JJ. 1989. A model of population growth, dispersal and evolution in a changing environment. Ecology 70:61657–64
     [Google Scholar]
  168. 168.
    Peischl S, Dupanloup I, Kirkpatrick M, Excoffier L. 2013. On the accumulation of deleterious mutations during range expansions. Mol. Ecol. 22:245972–82
     [Google Scholar]
  169. 169.
    Penn JL, Deutsch C. 2022. Avoiding ocean mass extinction from climate warming. Science 376:6592524–26
     [Google Scholar]
  170. 170.
    Picq S, McMillan WO, Puebla O. 2016. Population genomics of local adaptation versus speciation in coral reef fishes (Hypoplectrus spp, Serranidae). Ecol. Evol. 6:72109–24
     [Google Scholar]
  171. 171.
    Pini J, Planes S, Rochel E, Lecchini D, Fauvelot C 2011. Genetic diversity loss associated to high mortality and environmental stress during the recruitment stage of a coral reef fish. Coral Reefs 30:399–404
     [Google Scholar]
  172. 172.
    Pino Del Carpio D, Lozano R, Wolfe MD, Jannink J-L. 2019. Genome-wide association studies and heritability estimation in the functional genomics era. Population Genomics: Concepts, Approaches and Applications OP Rajora Cham, Switz.: Springer Int. Publ.
     [Google Scholar]
  173. 173.
    Pinsky ML, Palumbi SR. 2014. Meta-analysis reveals lower genetic diversity in overfished populations. Mol. Ecol. 23:129–39
     [Google Scholar]
  174. 174.
    Pinsky ML, Saenz-Agudelo P, Salles OC, Almany GR, Bode M et al. 2017. Marine dispersal scales are congruent over evolutionary and ecological time. Curr. Biol. 27:1149–54
     [Google Scholar]
  175. 175.
    Plaisance L, Caley MJ, Brainard RE, Knowlton N. 2011. The diversity of coral reefs: What are we missing?. PLOS ONE 6:10e25026
     [Google Scholar]
  176. 176.
    Prada C, Hellberg ME. 2013. Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral. PNAS 110:103961–66
     [Google Scholar]
  177. 177.
    Puebla O, Bermingham E, McMillan WO. 2012. On the spatial scale of dispersal in coral reef fishes. Mol. Ecol. 21:235675–88
     [Google Scholar]
  178. 178.
    Ravigné V, Dieckmann U, Olivieri I. 2009. Live where you thrive: Joint evolution of habitat choice and local adaptation facilitates specialization and promotes diversity. Am. Nat. 174:4E141–69
     [Google Scholar]
  179. 179.
    Reaka-Kudla ML. 1997. The global biodiversity of coral reefs: a comparison with rain forests. Biodiversity II: Understanding and Protecting Our Biological Resources ML Reaka-Kudla, DE Wilson, EO Wilson 83–108. Washington, DC: Joseph Henry Press
     [Google Scholar]
  180. 180.
    Reiskind MOB, Reed EMX, Elias A, Giacomini JJ, McNear AF et al. 2019. The genomics of invasion: characterization of red lionfish (Pterois volitans) populations from the native and introduced ranges. Biol. Invasions 21:72471–83
     [Google Scholar]
  181. 181.
    Reusch TBH, Baums IB, Werner B. 2021. Evolution via somatic genetic variation in modular species. Trends Ecol. Evol. 36:121083–92
     [Google Scholar]
  182. 182.
    Richards ZT, Hobbs J-PA. 2015. Hybridisation on coral reefs and the conservation of evolutionary novelty. Curr. Zool. 61:1132–45
     [Google Scholar]
  183. 183.
    Richardson JL, Urban MC, Bolnick DI, Skelly DK. 2014. Microgeographic adaptation and the spatial scale of evolution. Trends Ecol. Evol. 29:3165–76
     [Google Scholar]
  184. 184.
    Riegl BM, Purkis SJ, Al-Cibahy AS, Abdel-Moati MA, Hoegh-Guldberg O 2011. Present limits to heat-adaptability in corals and population-level responses to climate extremes. PLOS ONE 6:9e24802
     [Google Scholar]
  185. 185.
    Ritson-Williams R, Arnold S, Fogarty N, Steneck RS, Vermeij M, Paul VJ 2009. New perspectives on ecological mechanisms affecting coral recruitment on reefs. Smithson. Contrib. Mar. Sci. 38:437–57
     [Google Scholar]
  186. 186.
    Roberts CM, Hawkins JP. 1999. Extinction risk in the sea. Trends Ecol. Evol. 14:6241–46
     [Google Scholar]
  187. 187.
    Roberts CM, McClean CJ, Veron JEN, Hawkins JP, Allen GR et al. 2002. Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:55581280–84
     [Google Scholar]
  188. 188.
    Rocha LA, Bowen BW. 2008. Speciation in coral-reef fishes. J. Fish Biol. 72:51101–21
     [Google Scholar]
  189. 189.
    Rocha LA, Lindeman KC, Rocha CR, Lessios HA. 2008. Historical biogeography and speciation in the reef fish genus Haemulon (Teleostei: Haemulidae). Mol. Phylogenet. Evol. 48:3918–28
     [Google Scholar]
  190. 190.
    Rose NH, Bay RA, Morikawa MK, Palumbi SR. 2018. Polygenic evolution drives species divergence and climate adaptation in corals. Evolution 72:182–94
     [Google Scholar]
  191. 191.
    Rose NH, Bay RA, Morikawa MK, Thomas L, Sheets EA, Palumbi SR. 2021. Genomic analysis of distinct bleaching tolerances among cryptic coral species. Proc. R. Soc. B 288:196020210678
     [Google Scholar]
  192. 192.
    Rummer JL, Munday PL. 2017. Climate change and the evolution of reef fishes: past and future. Fish Fish. 18:122–39
     [Google Scholar]
  193. 193.
    Sanford E, Kelly MW. 2011. Local adaptation in marine invertebrates. Annu. Rev. Mar. Sci. 3:509–35
     [Google Scholar]
  194. 194.
    Sayers EW, Beck J, Bolton EE, Bourexis D, Brister JR et al. 2021. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 49:D1D10–17
     [Google Scholar]
  195. 195.
    Schoepf V, Carrion SA, Pfeifer SM, Naugle M, Dugal L et al. 2019. Stress-resistant corals may not acclimatize to ocean warming but maintain heat tolerance under cooler temperatures. Nat. Commun. 10:14031
     [Google Scholar]
  196. 196.
    Schunter C, Pascual M, Raventos N, Garriga J, Garza JC et al. 2019. A novel integrative approach elucidates fine-scale dispersal patchiness in marine populations. Sci. Rep. 9:10796
     [Google Scholar]
  197. 197.
    Scott CB, Cárdenas A, Mah M, Narasimhan VM, Rohland N et al. 2022. Millennia-old coral holobiont DNA provides insight into future adaptive trajectories. Mol. Ecol. 31:194979–90
     [Google Scholar]
  198. 198.
    Selkoe KA, D'Aloia CC, Crandall ED, Iacchei M, Liggins L et al. 2016. A decade of seascape genetics: contributions to basic and applied marine connectivity. Mar. Ecol. Prog. Ser. 554:1–19
     [Google Scholar]
  199. 199.
    Selkoe KA, Gaggiotti OE, Treml EA, Wren JLK, Donovan MK, Toonen RJ. 2016. The DNA of coral reef biodiversity: predicting and protecting genetic diversity of reef assemblages. Proc. R. Soc. B 283:182920160354
     [Google Scholar]
  200. 200.
    Selwyn JD, Hogan JD, Downey-Wall AM, Gurski LM, Portnoy DS, Heath DD. 2016. Kin-aggregations explain chaotic genetic patchiness, a commonly observed genetic pattern, in a marine fish. PLOS ONE 11:4e0153381
     [Google Scholar]
  201. 201.
    Semmens BX, Buhle ER, Salomon AK, Pattengill-Semmens CV. 2004. A hotspot of non-native marine fishes: evidence for the aquarium trade as an invasion pathway. Mar. Ecol. Prog. Ser. 266:239–44
     [Google Scholar]
  202. 202.
    Shanks AL. 2009. Pelagic larval duration and dispersal distance revisited. Biol. Bull. 216:373–85
     [Google Scholar]
  203. 203.
    Siegel DA, Mitarai S, Costello CJ, Gaines SD, Kendall BE et al. 2008. The stochastic nature of larval connectivity among nearshore marine populations. PNAS 105:268974–79
     [Google Scholar]
  204. 204.
    Simon T, Pinheiro HT, Santos S, Macieira RM, Ferreira YSS et al. 2022. Comparative phylogeography of reef fishes indicates seamounts as stepping stones for dispersal and diversification. Coral Reefs 41:3551–61
     [Google Scholar]
  205. 205.
    Smith EG, Hazzouri KM, Choi JY, Delaney P, Al-Kharafi M et al. 2022. Signatures of selection underpinning rapid coral adaptation to the world's warmest reefs. Sci. Adv. 8:2eabl7287
     [Google Scholar]
  206. 206.
    Snead AA, Clark RD. 2022. The biological hierarchy, time, and temporal ‘omics in evolutionary biology: a perspective. Integr. Comp. Biol. 62:61872–86
     [Google Scholar]
  207. 207.
    Sotka EE. 2012. Natural selection, larval dispersal, and the geography of phenotype in the sea. Integr. Comp. Biol. 52:4538–45
     [Google Scholar]
  208. 208.
    Souter D, Planes S, Wicquart J, Logan M, Obura D, Staub F. 2020. Status of coral reefs of the world: 2020 report Rep. Glob. Coral Reef Monit. Netw./Int. Coral Reef Initiat https://gcrmn.net/2020-report/
  209. 209.
    Souter P, Willis BL, Bay LK, Caley MJ, Muirhead A, van Oppen MJH. 2010. Location and disturbance affect population genetic structure in four coral species of the genus Acropora on the Great Barrier Reef. Mar. Ecol. Prog. Ser. 416:35–45
     [Google Scholar]
  210. 210.
    Spalding MD, Brown BE. 2015. Warm-water coral reefs and climate change. Science 350:6262769–71
     [Google Scholar]
  211. 211.
    Swaegers J, Mergeay J, Van Geystelen A, Therry L, Larmuseau MHD, Stoks R. 2015. Neutral and adaptive genomic signatures of rapid poleward range expansion. Mol. Ecol. 24:246163–76
     [Google Scholar]
  212. 212.
    Taylor MS, Hellberg ME. 2005. Marine radiations at small geographic scales: speciation in neotropical reef gobies (Elacatinus). Evolution 59:2374–85
     [Google Scholar]
  213. 213.
    Teh LSL, Teh LCL, Sumaila UR. 2013. A global estimate of the number of coral reef fishers. PLOS ONE 8:6e65397
     [Google Scholar]
  214. 214.
    Teixeira JC, Huber CD. 2021. The inflated significance of neutral genetic diversity in conservation genetics. PNAS 118:10e2015096118
     [Google Scholar]
  215. 215.
    Thomas L, Rose NH, Bay RA, López EH, Morikawa MK et al. 2018. Mechanisms of thermal tolerance in reef-building corals across a fine-grained environmental mosaic: lessons from Ofu, American Samoa. Front. Mar. Sci. 4:434
     [Google Scholar]
  216. 216.
    Thomas L, Underwood JN, Rose NH, Fuller ZL, Richards ZT et al. 2022. Spatially varying selection between habitats drives physiological shifts and local adaptation in a broadcast spawning coral on a remote atoll in Western Australia. Sci. Adv. 8:17eabl9185
     [Google Scholar]
  217. 217.
    Tigano A, Friesen VL. 2016. Genomics of local adaptation with gene flow. Mol. Ecol. 25:102144–64
     [Google Scholar]
  218. 218.
    Tisthammer KH, Timmins-Schiffman E, Seneca FO, Nunn BL, Richmond RH. 2021. Physiological and molecular responses of lobe coral indicate nearshore adaptations to anthropogenic stressors. Sci. Rep. 11:3423
     [Google Scholar]
  219. 219.
    Todesco M, Owens GL, Bercovich N, Légaré J-S, Soudi S et al. 2020. Massive haplotypes underlie ecotypic differentiation in sunflowers. Nature 584:7822602–7
     [Google Scholar]
  220. 220.
    Toth LT, Precht WF, Modys AB, Stathakopoulos A, Robbart ML et al. 2021. Climate and the latitudinal limits of subtropical reef development. Sci. Rep. 11:113044
     [Google Scholar]
  221. 221.
    Trisos CH, Auerbach J, Katti M. 2021. Decoloniality and anti-oppressive practices for a more ethical ecology. Nat. Ecol. Evol. 5:1205–12
     [Google Scholar]
  222. 222.
    Tsang LM, Chan BKK, Shih F-L, Chu KH, Chen CA. 2009. Host-associated speciation in the coral barnacle Wanella milleporae (Cirripedia: Pyrgomatidae) inhabiting the Millepora coral. Mol. Ecol. 18:71463–75
     [Google Scholar]
  223. 223.
    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. 16:4771–84
     [Google Scholar]
  224. 224.
    Uthicke S, Deshpande NP, Liddy M, Patel F, Lamare M, Wilkins MR. 2019. Little evidence of adaptation potential to ocean acidification in sea urchins living in “Future Ocean” conditions at a CO2 vent. Ecol. Evol. 9:1710004–16
     [Google Scholar]
  225. 225.
    van Oppen MJH, Oliver JK, Putnam HM, Gates RD. 2015. Building coral reef resilience through assisted evolution. PNAS 112:82307–13
     [Google Scholar]
  226. 226.
    Van Oppen MJH, Peplow LM, Kininmonth S, Berkelmans R. 2011. Historical and contemporary factors shape the population genetic structure of the broadcast spawning coral, Acropora millepora, on the Great Barrier Reef. Mol. Ecol. 20:234899–914
     [Google Scholar]
  227. 227.
    Vasquez Kuntz KL, Kitchen SA, Conn TL, Vohsen SA, Chan AN et al. 2022. Inheritance of somatic mutations by animal offspring. Sci. Adv. 8:35eabn0707
     [Google Scholar]
  228. 228.
    Veron JEN, Hoegh-Guldberg O, Lenton TM, Lough JM, Obura DO et al. 2009. The coral reef crisis: the critical importance of <350 ppm CO2. Mar. Pollut. Bull. 58:101428–36
     [Google Scholar]
  229. 229.
    Viard F, Riginos C, Bierne N. 2020. Anthropogenic hybridization at sea: three evolutionary questions relevant to invasive species management. Philos. Trans. R. Soc. B 375:180620190547
     [Google Scholar]
  230. 230.
    Wainwright BJ, Arlyza IS, Karl SA. 2020. Population genetics of the banded coral shrimp, Stenopus hispidus (Olivier, 1811), in the Indonesian archipelago. J. Exp. Mar. Biol. Ecol. 525:151325
     [Google Scholar]
  231. 231.
    Waples RS. 2016. Tiny estimates of the Ne/N ratio in marine fishes: Are they real?. J. Fish Biol. 89:62479–504
     [Google Scholar]
  232. 232.
    Willi Y, Van Buskirk J, Hoffmann AA. 2006. Limits to the adaptive potential of small populations. Annu. Rev. Ecol. Evol. Syst. 37:433–58
     [Google Scholar]
  233. 233.
    Williamson DH, Harrison HB, Almany GR, Berumen ML, Bode M et al. 2016. Large-scale, multidirectional larval connectivity among coral reef fish populations in the Great Barrier Reef Marine Park. Mol. Ecol. 25:246039–54
     [Google Scholar]
  234. 234.
    Willis BL, van Oppen MJH, Miller DJ, Vollmer SV, Ayre DJ. 2006. The role of hybridization in the evolution of reef corals. Annu. Rev. Ecol. Evol. Syst. 37:489–517
     [Google Scholar]
  235. 235.
    Wood R. 1998. The ecological evolution of reefs. Annu. Rev. Ecol. Syst. 29:179–206
     [Google Scholar]
  236. 236.
    Yaakub SM, Bellwood DR, van Herwerden L, Walsh FM. 2006. Hybridization in coral reef fishes: introgression and bi-directional gene exchange in Thalassoma (family Labridae). Mol. Phylogenet. Evol. 40:184–100
     [Google Scholar]
  237. 237.
    Yamano H, Sugihara K, Nomura K. 2011. Rapid poleward range expansion of tropical reef corals in response to rising sea surface temperatures. Geophys. Res. Lett. 38:4L04601
     [Google Scholar]
  238. 238.
    Yang J, Bakshi A, Zhu Z, Hemani G, Vinkhuyzen AAE et al. 2015. Genetic variance estimation with imputed variants finds negligible missing heritability for human height and body mass index. Nat. Genet. 47:101114–20
     [Google Scholar]
  239. 239.
    Yeaman S. 2015. Local adaptation by alleles of small effect. Am. Nat. 186:S1S74–89
     [Google Scholar]
  240. 240.
    Yeaman S, Whitlock MC. 2011. The genetic architecture of adaptation under migration–selection balance. Evolution 65:71897–911
     [Google Scholar]
/content/journals/10.1146/annurev-genet-022123-102748
Loading
Coral Reef Population Genomics in an Age of Global Change
Annual Review of Genetics 57, 87 (2023); https://doi.org/10.1146/annurev-genet-022123-102748
/content/journals/10.1146/annurev-genet-022123-102748
/content/journals/10.1146/annurev-genet-022123-102748
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error