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Abstract

Selective breeding of resilient organisms is an emerging topic in marine conservation. It can help us predict how species will adapt in the future and how we can help restore struggling populations effectively in the present. Scleractinian corals represent a potential tractable model system given their widescale phenotypic plasticity across fitness-related traits and a reproductive life history based on mass synchronized spawning. Here, I explore the justification for breeding in corals, identify underutilized pathways of acclimation, and highlight avenues for quantitative targeted breeding from the coral host and symbiont perspective. Specifically, the facilitation of enhanced heat tolerance by targeted breeding of plasticity mechanisms is underutilized. Evidence from theoretical genetics identifies potential pitfalls, including inattention to physical and genetic characteristics of the receiving environment. Three criteria for breeding emerge from this synthesis: selection from warm, variable reefs that have survived disturbance. This information will be essential to protect what we have and restore what we can.

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2024-02-15
2024-04-29
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Literature Cited

  1. 1.
    Pörtner H-O, Roberts DC, Poloczanska ES, Mintenbeck K, Tignor M et al. 2022. IPCC, 2022: summary for policymakers Rep. Intergov. Panel Clim. Change Geneva:
  2. 2.
    Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Péan C et al. 2021. Climate change 2021: the physical science basis Rep., Contrib. Work Group I, Sixth Assess. Rep. Intergov. Panel Clim. Change 2 Intergov. Panel Clim. Change Geneva:
  3. 3.
    Rezende EL, Bozinovic F. 2019. Thermal performance across levels of biological organization. Philos. Trans. R. Soc. B 374:177820180549
    [Google Scholar]
  4. 4.
    Blowes SA, Supp SR, Antão LH, Bates A, Bruelheide H et al. 2019. The geography of biodiversity change in marine and terrestrial assemblages. Science 366:6463339–45
    [Google Scholar]
  5. 5.
    Smith KE, Burrows MT, Hobday AJ, King NG, Moore PJ et al. 2023. Biological impacts of marine heatwaves. Annu. Rev. Mar. Sci. 15:119–45
    [Google Scholar]
  6. 6.
    Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS et al. 2017. Coral reefs in the Anthropocene. Nature 546:765682–90
    [Google Scholar]
  7. 7.
    Hillebrand H, Donohue I, Harpole WS, Hodapp D, Kucera M et al. 2020. Thresholds for ecological responses to global change do not emerge from empirical data. Nat. Ecol. Evol. 4:111502–9
    [Google Scholar]
  8. 8.
    Voolstra CR, Suggett DJ, Peixoto RS, Parkinson JE, Quigley KM et al. 2021. Extending the natural adaptive capacity of coral holobionts. Nat. Rev. Earth Environ. 2:11747–62
    [Google Scholar]
  9. 9.
    Sentinella AT, Warton DI, Sherwin WB, Offord CA, Moles AT. 2020. Tropical plants do not have narrower temperature tolerances, but are more at risk from warming because they are close to their upper thermal limits. Glob. Ecol. Biogeogr. 29:81387–98
    [Google Scholar]
  10. 10.
    Bove CB, Mudge L, Bruno JF. 2022. A century of warming on Caribbean reefs. PLOS Clim. 1:3e:0000002
    [Google Scholar]
  11. 11.
    Eladawy A, Nakamura T, Shaltout M, Mohammed A, Nadaoka K et al. 2022. Appraisal of coral bleaching thresholds and thermal projections for the northern Red Sea refugia. Front. Mar. Sci. 9: https://doi.org/10.3389/fmars.2022.938454
    [Google Scholar]
  12. 12.
    Somero GN. 2004. Adaptation of enzymes to temperature: searching for basic “strategies. Comp. Biochem. Physiol. B 139:3321–33
    [Google Scholar]
  13. 13.
    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]
  14. 14.
    Lynch M, Walsh B. 1998. Genetics and Analysis of Quantitative Traits Sunderland, MA: Sinauer Assoc
  15. 15.
    Huey RB, Kingsolver JG. 1993. Evolution of resistance to high temperature in ectotherms. Am. Nat. 142:S21–S46
    [Google Scholar]
  16. 16.
    Diamond SE, Martin RA. 2021. Physiological adaptation to cities as a proxy to forecast global-scale responses to climate change. J. Exp. Biol. 224:Suppl. 1jeb229336
    [Google Scholar]
  17. 17.
    Visscher PM, Hill WG, Wray NR. 2008. Heritability in the genomics era—concepts and misconceptions. Nat. Rev. Genet. 9:4255–66
    [Google Scholar]
  18. 18.
    Kiessling W. 2009. Geologic and biologic controls on the evolution of reefs. Annu. Rev. Ecol. Evol. Syst. 40:173–92
    [Google Scholar]
  19. 19.
    Neufeldt H, Christiansen L, Dale TW. 2021. Adaptation gap report 2020 Rep. UN Environ. Progr. Nairobi:
  20. 20.
    LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD et al. 2018. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28:162570–80
    [Google Scholar]
  21. 21.
    Quigley KM, Willis BL, Bay LK. 2017. Heritability of the Symbiodinium community in vertically- and horizontally-transmitting broadcast spawning corals. Sci. Rep. 7:8219
    [Google Scholar]
  22. 22.
    Jokiel PL, Coles SL. 1990. Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8:4155–62
    [Google Scholar]
  23. 23.
    Fitt WK, McFarland FK, Warner ME, Chilcoat GC. 2000. Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol. Oceanogr. 45:3677–85
    [Google Scholar]
  24. 24.
    Loya Y, Sakai K, Nakano Y, van Woesik R. 2001. Coral bleaching: the winners and the losers. Ecol. Lett. 4:2122–31
    [Google Scholar]
  25. 25.
    Oakley CA, Davy SK. 2018. Cell biology of coral bleaching. In Coral Bleaching MJH van Oppen, JM Lough 189–211 Cham, Switz: Springer
    [Google Scholar]
  26. 26.
    Hoegh-Guldberg O. 1999. Climate change, coral bleaching and the future of the world's coral reefs. Aust. J. Mar. Freshw. Res. 50:8839–66
    [Google Scholar]
  27. 27.
    Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P et al. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318:58571737–42
    [Google Scholar]
  28. 28.
    Bieri T, Onishi M, Xiang T, Grossman AR, Pringle JR. 2016. Relative contributions of various cellular mechanisms to loss of algae during cnidarian bleaching. PLOS ONE 11:4e0152693
    [Google Scholar]
  29. 29.
    Bonnet T, Morrissey MB, de Villemereuil P, Alberts SC, Arcese P et al. 2022. Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals. Science 376:65961012–16
    [Google Scholar]
  30. 30.
    Lambert MR, Brans KI, des Roches S, Donihue CM, Diamond SE. 2021. Adaptive evolution in cities: progress and misconceptions. Trends Ecol. Evol. 36:3239–57
    [Google Scholar]
  31. 31.
    Kao KC, Sherlock G. 2008. Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat. Genet. 40:121499–504
    [Google Scholar]
  32. 32.
    Messer PW, Petrov DA. 2013. Population genomics of rapid adaptation by soft selective sweeps. Trends Ecol. Evol. 28:11659–69
    [Google Scholar]
  33. 33.
    Radchuk V, Reed T, Teplitsky C, van de Pol M, Charmantier A et al. 2019. Adaptive responses of animals to climate change are most likely insufficient. Nat. Commun. 10:13109
    [Google Scholar]
  34. 34.
    Pollock FJ, Katz SM, van de Water JAJM, Davies SW, Hein M et al. 2017. Coral larvae for restoration and research: a large-scale method for rearing Acropora millepora larvae, inducing settlement, and establishing symbiosis. PeerJ 5:e3732
    [Google Scholar]
  35. 35.
    Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, Willis BL. 1984. Mass spawning in tropical reef corals. Science 223:46411186–89
    [Google Scholar]
  36. 36.
    Baird AH, Guest JR, Edwards AJ, Bauman AG, Bouwmeester J et al. 2021. An Indo-Pacific coral spawning database. Sci. Data 8:35
    [Google Scholar]
  37. 37.
    Willis BL, Babcock RC, Harrison PL, Wallace CC. 1997. Experimental hybridization and breeding incompatibilities within the mating systems of mass spawning reef corals. Coral Reefs 16:1S53–S65
    [Google Scholar]
  38. 38.
    Willis BI, Babcock RC, Harrison PL, Wallace CC. 1997. Mating systems, hybridization and species concepts in mass spawning reef corals. Coral Reefs 16:Suppl.S53–S65
    [Google Scholar]
  39. 39.
    Drury C, Caruso C, Quigley K. 2022. Selective breeding to enhance the adaptive potential of corals. Coral Reef Conservation and Restoration in the Omics Age MJH van Oppen, MA Lastra 71–84 Cham, Switz.: Springer
    [Google Scholar]
  40. 40.
    Quigley KM, Hein M, Suggett DJ. 2022. Translating the ten golden rules of reforestation for coral reef restoration. Conserv. Biol. 36:e13890
    [Google Scholar]
  41. 41.
    Aitken SN, Whitlock MC. 2013. Assisted gene flow to facilitate local adaptation to climate change. Annu. Rev. Ecol. Evol. Syst. 44:367–88
    [Google Scholar]
  42. 42.
    MacPherson A, Wang S, Yamaguchi R, Rieseberg LH, Otto SP. 2022. Parental population range expansion before secondary contact promotes heterosis. Am. Nat. 200:1E1–15
    [Google Scholar]
  43. 43.
    Hoffmann AA, Weeks AR, Sgrò CM. 2021. Opportunities and challenges in assessing climate change vulnerability through genomics. Cell 184:61420–25
    [Google Scholar]
  44. 44.
    Hoffmann AA, Miller AD, Weeks AR. 2021. Genetic mixing for population management: from genetic rescue to provenancing. Evol. Appl. 14:3634–52
    [Google Scholar]
  45. 45.
    Quigley KM, Bay LK, van Oppen MJH. 2019. The active spread of adaptive variation for reef resilience. Ecol. Evol. 9:1911122–35
    [Google Scholar]
  46. 46.
    Anthony K, Bay LK, Costanza R, Firn J, Gunn J et al. 2017. New interventions are needed to save coral reefs. Nat. Ecol. Evol. 1:1420–22
    [Google Scholar]
  47. 47.
    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]
  48. 48.
    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]
  49. 49.
    Quigley KM, Bay LK, van Oppen MJH. 2020. Genome-wide SNP analysis reveals an increase in adaptive genetic variation through selective breeding of coral. Mol. Ecol. 29:2176–88
    [Google Scholar]
  50. 50.
    Humanes A, Bythell J, Beauchamp E, Carl M, Craggs J et al. 2021. An experimental framework for selectively breeding corals for assisted evolution. Front. Mar. Sci. 8:669995
    [Google Scholar]
  51. 51.
    Baird AH, Guest JR, Willis BL. 2009. Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu. Rev. Ecol. Evol. Syst. 40:551–71
    [Google Scholar]
  52. 52.
    Torda G, Quigley KM. 2022. Drivers of adaptive capacity in wild populations: implications for genetic interventions. Front. Mar. Sci. 9:947989
    [Google Scholar]
  53. 53.
    Weeriyanun P, Collins RB, Macadam A, Kiff H, Randle JL, Quigley KM. 2021. Predicting selection-response gradients of heat tolerance in a wide-ranging reef-building coral. J. Exp. Biol. 225:Suppl. 1jeb243344
    [Google Scholar]
  54. 54.
    Quigley KM, Randall CJ, van Oppen MJH, Bay LK. 2020. Assessing the role of historical temperature regime and algal symbionts on the heat tolerance of coral juveniles. Biol. Open 9:bio047316
    [Google Scholar]
  55. 55.
    Quigley KM, van Oppen MJH. 2022. Predictive models for the selection of thermally tolerant corals based on offspring survival. Nat. Commun. 13:1543
    [Google Scholar]
  56. 56.
    Vinton AC, Gascoigne SJL, Sepil I, Salguero-Gómez R. 2022. Plasticity's role in adaptive evolution depends on environmental change components. Trends Ecol. Evol. 37:121067–78
    [Google Scholar]
  57. 57.
    Gaitán-Espitia JD, Hobday AJ. 2021. Evolutionary principles and genetic considerations for guiding conservation interventions under climate change. Glob. Change Biol. 27:3475–88
    [Google Scholar]
  58. 58.
    Prudic KL, Stoehr AM, Wasik BR, Monteiro A. 2015. Eyespots deflect predator attack increasing fitness and promoting the evolution of phenotypic plasticity. Proc. R. Soc. B 282:179820141531
    [Google Scholar]
  59. 59.
    Oomen RA, Hutchings JA. 2022. Genomic reaction norms inform predictions of plastic and adaptive responses to climate change. J. Anim. Ecol. 91:61073–87
    [Google Scholar]
  60. 60.
    Ancel LW. 2000. Undermining the Baldwin expediting effect: Does phenotypic plasticity accelerate evolution?. Theor. Popul. Biol. 58:4307–19
    [Google Scholar]
  61. 61.
    Fox RJ, Donelson JM, Schunter C, Ravasi T, Gaitán-Espitia JD. 2019. Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Philos. Trans. R. Soc. B 374:176820180174
    [Google Scholar]
  62. 62.
    Torda G, Donelson JM, Aranda M, Barshis DJ, Bay L et al. 2017. Rapid adaptive responses to climate change in corals. Nat. Clim. Change 7:9627–36
    [Google Scholar]
  63. 63.
    Pottier P, Burke S, Zhang RY, Noble DWA, Schwanz LE et al. 2022. Developmental plasticity in thermal tolerance: ontogenetic variation, persistence, and future directions. Ecol. Lett. 25:102245–68
    [Google Scholar]
  64. 64.
    Logan ML, Cox CL. 2020. Genetic constraints, transcriptome plasticity, and the evolutionary response to climate change. Front. Genet. 11:538226
    [Google Scholar]
  65. 65.
    Franklin CE, Hoppeler HH. 2021. Elucidating mechanism is important in forecasting the impact of a changing world on species survival. J. Exp. Biol. 224:Suppl. 1jeb242284
    [Google Scholar]
  66. 66.
    Allen AP, Brown JH, Gillooly JF. 2002. Global biodiversity, biochemical kinetics, and the energetic-equivalence rule. Science 297:55861545–48
    [Google Scholar]
  67. 67.
    O'Connor MI, Bruno JF, Gaines SD, Halpern BS, Lester SE et al. 2007. Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. PNAS 104:41266–71
    [Google Scholar]
  68. 68.
    Marshall DJ, Pettersen AK, Bode M, White CR. 2020. Developmental cost theory predicts thermal environment and vulnerability to global warming. Nat. Ecol. Evol. 4:3406–11
    [Google Scholar]
  69. 69.
    Deutsch C, Penn JL, Seibel B. 2020. Metabolic trait diversity shapes marine biogeography. Nature 585:7826557–62
    [Google Scholar]
  70. 70.
    Bennett JM, Sunday J, Calosi P, Villalobos F, Martínez B et al. 2021. The evolution of critical thermal limits of life on Earth. Nat. Commun. 12:1198
    [Google Scholar]
  71. 71.
    Liggins L, Treml EA, Riginos C. 2020. Seascape genomics: contextualizing adaptive and neutral genomic variation in the ocean environment. Population Genomics: Marine Organisms MF Oleksiak, OP Rajora 171–218 Cham, Switz.: Springer Nat.
    [Google Scholar]
  72. 72.
    Donner SD. 2009. Coping with commitment: projected thermal stress on coral reefs under different future scenarios. PLOS ONE 4:6e5712
    [Google Scholar]
  73. 73.
    Reusch TBH. 2014. Climate change in the oceans: evolutionary versus phenotypically plastic responses of marine animals and plants. Evol. Appl. 7:1104–22
    [Google Scholar]
  74. 74.
    Morgan R, Finnøen MH, Jensen H, Pélabon C, Jutfelt F. 2020. Low potential for evolutionary rescue from climate change in a tropical fish. PNAS 117:5233365–72
    [Google Scholar]
  75. 75.
    Baldwin JM. 1896. A new factor in evolution (continued). Am. Nat. 30:355536–53
    [Google Scholar]
  76. 76.
    Kolodny O, Schulenburg H. 2020. Microbiome-mediated plasticity directs host evolution along several distinct time scales. Philos. Trans. R. Soc. B 375:180820190589
    [Google Scholar]
  77. 77.
    Sørensen JG, Kristensen TN, Overgaard J. 2016. Evolutionary and ecological patterns of thermal acclimation capacity in Drosophila: Is it important for keeping up with climate change?. Curr. Opin. Insect Sci. 17:98–104
    [Google Scholar]
  78. 78.
    Corl A, Bi K, Luke C, Challa AS, Stern AJ et al. 2018. The genetic basis of adaptation following plastic changes in coloration in a novel environment. Curr. Biol. 28:182970–77
    [Google Scholar]
  79. 79.
    Corl A, Lancaster LT, Sinervo B. 2012. Rapid formation of reproductive isolation between two populations of side-blotched lizards, Uta stansburiana. Copeia 2012:4593–602
    [Google Scholar]
  80. 80.
    Selkoe KA, Henzler CM, Gaines SD. 2008. Seascape genetics and the spatial ecology of marine populations. Fish Fish. 9:4363–77
    [Google Scholar]
  81. 81.
    Strader ME, Quigley KM. 2022. The role of gene expression and symbiosis in reef-building coral acquired heat tolerance. Nat. Commun. 13:4513
    [Google Scholar]
  82. 82.
    Kenkel CD, Matz MV. 2016. Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nat. Ecol. Evol. 1:0014
    [Google Scholar]
  83. 83.
    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]
  84. 84.
    Van Woesik R, Shlesinger T, Grottoli AG, Toonen RJ, Vega Thurber R et al. 2022. Coral-bleaching responses to climate change across biological scales. Glob. Change Biol. 28:144229–50
    [Google Scholar]
  85. 85.
    Hoegh-Guldberg O, Fine M. 2004. Low temperatures cause coral bleaching. Coral Reefs 23:3444
    [Google Scholar]
  86. 86.
    Woolsey ES, Keith SA, Byrne M, Schmidt-Roach S, Baird AH. 2015. Latitudinal variation in thermal tolerance thresholds of early life stages of corals. Coral Reefs 34:2471–78
    [Google Scholar]
  87. 87.
    Jurriaans S, Hoogenboom MO. 2019. Thermal performance of scleractinian corals along a latitudinal gradient on the Great Barrier Reef. Philos. Trans. R. Soc. B 374:177820180546
    [Google Scholar]
  88. 88.
    Baskett ML, Gaines SD, Nisbet RM. 2009. Symbiont diversity may help coral reefs survive moderate climate change. Ecol. Appl. 19:13–17
    [Google Scholar]
  89. 89.
    Whiteley AR, Fitzpatrick SW, Funk WC, Tallmon DA. 2015. Genetic rescue to the rescue. Trends Ecol. Evol. 30:142–49
    [Google Scholar]
  90. 90.
    Baker DM, Freeman CJ, Wong JCY, Fogel ML, Knowlton N. 2018. Climate change promotes parasitism in a coral symbiosis. ISME J. 12:3921–30
    [Google Scholar]
  91. 91.
    Srivastava DS, Coristine L, Angert AL, Bontrager M, Amundrud SL et al. 2021. Wildcards in climate change biology. Ecol. Monogr. 91:4e01471
    [Google Scholar]
  92. 92.
    van Woesik R, Sakai K, Ganase A, Loya Y. 2011. Revisiting the winners and the losers a decade after coral bleaching. Mar. Ecol. Prog. Ser. 434:67–76
    [Google Scholar]
  93. 93.
    Hoogenboom MO, Frank GE, Chase TJ, Jurriaans S, Álvarez-Noriega M et al. 2017. Environmental drivers of variation in bleaching severity of Acropora species during an extreme thermal anomaly. Front. Mar. Sci. 4:376
    [Google Scholar]
  94. 94.
    Baums IB, Devlin-Durante MK, Polato NR, Xu D, Giri S et al. 2013. Genotypic variation influences reproductive success and thermal stress tolerance in the reef building coral, Acropora palmata. Coral Reefs 32:3703–17
    [Google Scholar]
  95. 95.
    Drury C, Manzello D, Lirman D. 2017. Genotype and local environment dynamically influence growth, disturbance response and survivorship in the threatened coral, Acropora cervicornis. PLOS ONE 12:3e0174000
    [Google Scholar]
  96. 96.
    Quigley KM, Willis BL, Bay LK. 2016. Maternal effects and Symbiodinium community composition drive differential patterns in juvenile survival in the coral Acropora tenuis R. . Soc. Open Sci. 3:160471
    [Google Scholar]
  97. 97.
    Darling ES, Côté IM. 2018. Seeking resilience in marine ecosystems. Science 359:6379986–87
    [Google Scholar]
  98. 98.
    Morikawa MK, Palumbi SR. 2019. Using naturally occurring climate resilient corals to construct bleaching-resistant nurseries. PNAS 116:2110586–91
    [Google Scholar]
  99. 99.
    Bay RA, Palumbi SR. 2014. Multilocus adaptation associated with heat resistance in reef-building corals. Curr. Biol. 24:242952–56
    [Google Scholar]
  100. 100.
    Quigley KM, Marzonie M, Ramsby B, Abrego D, Milton G et al. 2021. Variability in fitness trade-offs amongst coral juveniles with mixed genetic backgrounds held in the wild. Front. Mar. Sci. 8:161
    [Google Scholar]
  101. 101.
    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]
  102. 102.
    Henry LP, Bruijning M, Forsberg SKG, Ayroles JF. 2021. The microbiome extends host evolutionary potential. Nat Commun. 12:5141
    [Google Scholar]
  103. 103.
    Fabina NS, Putnam HM, Franklin EC, Stat M, Gates RD. 2012. Transmission mode predicts specificity and interaction patterns in coral-Symbiodinium networks. PLOS ONE 7:944970
    [Google Scholar]
  104. 104.
    Davy SK, Allemand D, Weis VM. 2012. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76:2229–61
    [Google Scholar]
  105. 105.
    Quigley KM, Warner PA, Bay LK, Willis BL. 2018. Unexpected mixed-mode transmission and moderate genetic regulation of Symbiodinium communities in a brooding coral. Heredity 121:524–36
    [Google Scholar]
  106. 106.
    Thornhill DJ, Lewis AM, Wham DC, Lajeunesse TC. 2014. Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution 68:2352–67
    [Google Scholar]
  107. 107.
    Muller-Parker G, D'Elia CF, Cook CB. 2015. Interactions between corals and their symbiotic algae. Coral Reefs in the Anthropocene C Birkeland 99–116 Dordrecht, Neth.: Springer
    [Google Scholar]
  108. 108.
    Quigley KM, Davies SW, Kenkel CD, Willis BL, Matz MV, Bay LK. 2014. Deep-sequencing method for quantifying background abundances of Symbiodinium types: exploring the rare Symbiodinium biosphere in reef-building corals. PLOS ONE 9:4e94297
    [Google Scholar]
  109. 109.
    Ziegler M, Stone E, Colman D, Takacs-Vesbach C, Shepherd U. 2018. Patterns of Symbiodinium (Dinophyceae) diversity and assemblages among diverse hosts and the coral reef environment of Lizard Island, Australia. J. Phycol. 54:4447–60
    [Google Scholar]
  110. 110.
    Thornhill DJ, Howells EJ, Wham DC, Steury TD, Santos SR. 2017. Population genetics of reef coral endosymbionts (Symbiodinium, Dinophyceae). Mol. Ecol. 26:102640–59
    [Google Scholar]
  111. 111.
    Davies S, Gamache MH, Howe-Kerr LI, Kriefall NG, Baker AC et al. 2022. Building consensus around the assessment and interpretation of Symbiodiniaceae diversity. PeerJ 11:e15023
    [Google Scholar]
  112. 112.
    Martignoni MM, Hart MM, Garnier J, Tyson RC. 2020. Parasitism within mutualist guilds explains the maintenance of diversity in multi-species mutualisms. Theor. Ecol. 13:615–27
    [Google Scholar]
  113. 113.
    Quigley KM, Bay LK, Willis BL. 2018. Leveraging new knowledge of Symbiodinium community regulation in corals for conservation and reef restoration. Mar. Ecol. Prog. Ser. 600:245–53
    [Google Scholar]
  114. 114.
    Salsbery ME, DeLong JP. 2021. Thermal adaptation in a holobiont accompanied by phenotypic changes in an endosymbiont. Evolution 75:82074–84
    [Google Scholar]
  115. 115.
    Quigley KM, Alvarez Roa C, Beltran VH, Leggat B, Willis BL. 2021. Experimental evolution of the coral algal endosymbiont, Cladocopium goreaui: lessons learnt across a decade of stress experiments to enhance coral heat tolerance. Restor. Ecol. 29:3e13342
    [Google Scholar]
  116. 116.
    Baker AC. 2003. Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 34:661–89
    [Google Scholar]
  117. 117.
    White JF, Kingsley KL, Zhang Q, Verma R, Obi N et al. 2019. Endophytic microbes and their potential applications in crop management. Pest Manag. Sci. 75:102558–65
    [Google Scholar]
  118. 118.
    Logan CA, Dunne JP, Ryan JS, Baskett ML, Donner SD. 2021. Quantifying global potential for coral evolutionary response to climate change. Nat. Clim. Change 11:537–42
    [Google Scholar]
  119. 119.
    Quigley K, Ramsby B, Laffy P, Harris J, Mocellin V, Bay L. 2022. Symbioses are restricted by repeated mass coral bleaching. Sci. Adv. 8:49eabq8349
    [Google Scholar]
  120. 120.
    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]
  121. 121.
    Camp EF, Nitschke MR, Rodolfo-Metalpa R, Houlbreque F, Gardner SG et al. 2017. Reef-building corals thrive within hot-acidified and deoxygenated waters. Sci. Rep. 7:2434
    [Google Scholar]
  122. 122.
    Oliver T, Palumbi S. 2011. Do fluctuating temperature environments elevate coral thermal tolerance?. Coral Reefs 30:2429–40
    [Google Scholar]
  123. 123.
    Sgrò CM, Lowe AJ, Hoffmann AA. 2011. Building evolutionary resilience for conserving biodiversity under climate change. Evol. Appl. 4:2326–37
    [Google Scholar]
  124. 124.
    Voolstra CR, Buitrago-López C, Perna G, Cárdenas A, Hume BCC et al. 2020. Standardized short-term acute heat stress assays resolve historical differences in coral thermotolerance across microhabitat reef sites. Glob. Change Biol. 26:84328–43
    [Google Scholar]
  125. 125.
    Ainsworth TD, Heron SF, Ortiz JC, Mumby PJ, Grech A et al. 2016. Climate change disables coral bleaching protection on the Great Barrier Reef. Science 352:6283338–42
    [Google Scholar]
  126. 126.
    Beyer HL, Kennedy EV, Beger M, Chen CA, Cinner JE et al. 2018. Risk-sensitive planning for conserving coral reefs under rapid climate change. Conserv. Lett. 11:6e12587
    [Google Scholar]
  127. 127.
    Tenaillon O. 2014. The utility of Fisher's geometric model in evolutionary genetics. Annu. Rev. Ecol. Evol. Syst. 45:179–201
    [Google Scholar]
  128. 128.
    Shaver EC, McLeod E, Hein MY, Palumbi SR, Quigley K et al. 2022. A roadmap to integrating resilience into the practice of coral reef restoration. Glob. Change Biol. 28:164751–64
    [Google Scholar]
  129. 129.
    Walsworth TE, Schindler DE, Colton MA, Webster MS, Palumbi SR et al. 2019. Management for network diversity speeds evolutionary adaptation to climate change. Nat. Clim. Change 9:8632–36
    [Google Scholar]
  130. 130.
    Sully S, Burkepile DE, Donovan MK, Hodgson G, van Woesik R. 2019. A global analysis of coral bleaching over the past two decades. Nat. Commun. 10:1264
    [Google Scholar]
  131. 131.
    Safaie A, Silbiger NJ, McClanahan TR, Pawlak G, Barshis DJ et al. 2018. High frequency temperature variability reduces the risk of coral bleaching. Nat. Commun. 9:1671
    [Google Scholar]
  132. 132.
    Kenkel CD, Goodbody-Gringley G, Caillaud D, Davies SW, Bartels E, Matz MV. 2013. Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol. Ecol. 22:164335–48
    [Google Scholar]
  133. 133.
    Schoepf V, Grottoli AG, Levas SJ, Aschaffenburg MD, Baumann JH et al. 2015. Annual coral bleaching and the long-term recovery capacity of coral. Proc. R. Soc. B 282:181920151887
    [Google Scholar]
  134. 134.
    Hughes TP, Kerry JT, Connolly SR, Baird AH, Eakin CM et al. 2019. Ecological memory modifies the cumulative impact of recurrent climate extremes. Nat. Clim. Change 9:140–43
    [Google Scholar]
  135. 135.
    Claar DC, Starko S, Tietjen KL, Epstein HE, Cunning R et al. 2020. Dynamic symbioses reveal pathways to coral survival through prolonged heatwaves. Nat. Commun. 11:6097
    [Google Scholar]
  136. 136.
    Osman EO, Smith DJ, Ziegler M, Kürten B, Conrad C et al. 2018. Thermal refugia against coral bleaching throughout the northern Red Sea. Glob. Change Biol. 24:2e474–84
    [Google Scholar]
  137. 137.
    Camp E, Schoepf V, Suggett D. 2018. How can “Super Corals” facilitate global coral reef survival under rapid environmental and climatic change?. Glob. Change Biol. 24:72755–57
    [Google Scholar]
  138. 138.
    Banc-Prandi G, Evensen NR, Barshis DJ, Perna G, Moussa Omar Y, Fine M. 2022. Assessment of temperature optimum signatures of corals at both latitudinal extremes of the Red Sea. Conserv. Physiol. 10:1coac002
    [Google Scholar]
  139. 139.
    Rivera HE, Cohen AL, Thompson JR, Baums IB, Fox MD, Meyer-Kaiser KS. 2022. Palau's warmest reefs harbor thermally tolerant corals that thrive across different habitats. Commun. Biol. 5:1394
    [Google Scholar]
  140. 140.
    Coulson T, Kendall BE, Barthold J, Plard F, Schindler S et al. 2017. Modeling adaptive and nonadaptive responses of populations to environmental change. Am. Nat. 190:3313–36
    [Google Scholar]
  141. 141.
    Brown KT, Eyal G, Dove SG, Barott KL. 2022. Fine-scale heterogeneity reveals disproportionate thermal stress and coral mortality in thermally variable reef habitats during a marine heatwave. Coral Reefs 42:131–42
    [Google Scholar]
  142. 142.
    Lewis CL, Neely KL, Rodriguez-Lanetty M. 2019. Recurring episodes of thermal stress shift the balance from a dominant host-specialist to a background host-generalist zooxanthella in the threatened pillar coral, Dendrogyra cylindrus. Front. Mar. Sci. 6:5
    [Google Scholar]
  143. 143.
    Selmoni O, Rochat E, Lecellier G, Berteaux-Lecellier V, Joost S 2020. Seascape genomics as a new tool to empower coral reef conservation strategies: an example on north-western Pacific Acropora digitifera. Evol. Appl. 13:81923–38
    [Google Scholar]
  144. 144.
    Hereford J. 2009. A quantitative survey of local adaptation and fitness trade-offs. Am. Nat. 173:5579–88
    [Google Scholar]
  145. 145.
    Quigley K, Donelson J. 2023. Selective breeding and promotion of naturally heat-tolerant coral reef species. Oceanographic Processes of Coral Reefs: Physical and Biological Links in The Great Barrier Reef Boca Raton, FL: CRC Press, 2nd ed.. In press
    [Google Scholar]
  146. 146.
    Bitter MC, Wong JM, Dam HG, Donelan SC, Kenkel CD et al. 2021. Fluctuating selection and global change: a synthesis and review on disentangling the roles of climate amplitude, predictability and novelty. Proc. R. Soc. B 288:195720210727
    [Google Scholar]
  147. 147.
    Slatkin M. 1985. Gene flow in natural populations. Annu. Rev. Ecol. Syst. 16:393–430
    [Google Scholar]
  148. 148.
    van Belleghem SM, Cole JM, Montejo-Kovacevich G, Bacquet CN, McMillan WO et al. 2021. Selection and isolation define a heterogeneous divergence landscape between hybridizing Heliconius butterflies. Evolution 75:92251–68
    [Google Scholar]
  149. 149.
    Moore JW, Schindler DE. 2022. Getting ahead of climate change for ecological adaptation and resilience. Science 376:66001421–26
    [Google Scholar]
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