Abstract
Coral populations must be able to adapt to changing environmental conditions for coral reefs to persist under climate change. The adaptive potential of these organisms is difficult to forecast due to complex interactions between the host animal, dinoflagellate symbionts and the environment. Here we created 26 larval families from six Montipora capitata colonies from a single reef, showing significant, heritable variation in thermal tolerance. Our results indicate that 9.1% of larvae are expected to exhibit four times the thermal tolerance of the general population. Differences in larval thermotolerance were driven mainly by maternal contributions, but we found no evidence that these effects were driven by symbiont identity despite vertical transmission from the dam. We also document no evidence of reproductive incompatibility attributable to symbiont identity. These data demonstrate significant genetic variation within this population which provides the raw material upon which natural selection can act.
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Data and code are uploaded to GitHub at: https://github.com/Erikacj/Matrix_reloaded.
References
Alvarez-Filip L, Dulvy NK, Gill JA, Côté IM, Watkinson AR (2009) Flattening of Caribbean coral reefs: Region-wide declines in architectural complexity. Proc R Soc B Biol Sci 276:3019–3025
Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol Syst 40:551–571
Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689
Batstone RT, Carscadden KA, Afkhami ME, Frederickson ME (2018) Using niche breadth theory to explain generalization in mutualisms. Ecology 99:1039–1050
Baums IB, Hughes CR, Hellberg ME (2005) Mendelian microsatellite loci for the Caribbean coral Acropora palmata. Mar Ecol Prog Ser 288:115–127
Baums IB, Devlin-Durante MK, Polato NR, Xu D, Giri S, Altman NS, Ruiz D, Parkinson JE, Boulay JN (2013) Genotypic variation influences reproductive success and thermal stress tolerance in the reef building coral, Acropora palmata. Coral Reefs 32:703–717
Bay R, Palumbi S (2014) Multilocus adaptation associated with heat resistance in reef-building corals. Curr Biol 24:1–5
Bay RA, Rose NH, Logan CA, Palumbi SR (2017b) Genomic models predict successful coral adaptation if future ocean warming rates are reduced. Sci Adv 3:e1701413
Bay RA, Rose N, Barrett R, Bernatchez L, Ghalambor CK, Lasky JR, Brem RB, Palumbi SR, Ralph P (2017a) Predicting responses to contemporary environmental change using evolutionary response architectures. Am Naturalist 189:463–473
Beever EA, O’Leary J, Mengelt C, West JM, Julius S, Green N, Magness D, Petes L, Stein B, Nicotra AB, Hellmann JJ, Robertson AL, Staudinger MD, Rosenberg AA, Babij E, Brennan J, Schuurman GW, Hofmann GE (2016) Improving conservation outcomes with a new paradigm for understanding species’ fundamental and realized adaptive capacity. Conserv Lett 9:131–137
Bongaerts P, Carmichael M, Hay KB, Tonk L, Frade PR, Hoegh-Guldberg O (2015) Prevalent endosymbiont zonation shapes the depth distributions of scleractinian coral species. R Soc Open Sci 2:140297
Brown AL, Pfab F, Baxter EC, Detmer AR, Moeller HV, Nisbet RM, Cunning R (2022) Analysis of a mechanistic model of corals in association with multiple symbionts: within-host competition and recovery from bleaching. Conserv Physiol 10(1):coac066
Buerger P, Alvarez-Roa C, Coppin CW, Pearce SL, Chakravarti LJ, Oakeshott JG, Edwards OR, Van Oppen MJH (2020) Heat-evolved microalgal symbionts increase coral bleaching tolerance. Sci Adv 6:eaba2498
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:e03324
Camp EF, Schoepf V, Mumby PJ, Hardtke LA, Rodolfo-Metalpa R, Smith DJ, Suggett DJ (2018) The future of coral reefs subject to rapid climate change: Lessons from natural extreme environments. Front Mar Sci 5:4
Caruso C, Rocha de Souza M, Ruiz-Jones L, Conetta D, Hancock J, Hobbs C, Hobbs C, Kahkejian V, Kitchen R, Marin C, Monismith S, Madin J, Gates R, Drury C (2022) Genetic patterns in Montipora capitata across an environmental mosaic in Kāne’ohe Bay, O’ahu, Hawai’i. Mol Ecol 31:5201–5213
Chamberland VF, Latijnhouwers KRW, Huisman J, Hartmann AC, Vermeij MJA (2017) Costs and benefits of maternally inherited algal symbionts in coral larvae. Proc R Soc B Biol Sci 284:20170852
Chille E, Strand E, Neder M, Schmidt V, Sherman M, Mass T, Putnam H (2021) Developmental series of gene expression clarifies maternal mRNA provisioning and maternal-to-zygotic transition in a reef-building coral. BMC Genomics 22:815
Colton MA, McManus LC, Schindler DE, Mumby PJ, Palumbi SR, Webster MM, Essington TE, Fox HE, Forrest DL, Schill SR, Pollock FJ, DeFilippo LB, Tekwa EW, Walsworth TE, Pinsky ML (2022) Coral conservation in a warming world must harness evolutionary adaptation. Nat Ecol Evol 6:1405–1407
Cooke I, Ying H, Forêt S, Bongaerts P, Strugnell JM, Simakov O, Zhang J, Field MA, Rodriguez-Lanetty M, Bell SC, Bourne DG, van Oppen MJH, Ragan MA, Miller DJ (2020) Genomic signatures in the coral holobiont reveal host adaptations driven by Holocene climate change and reef specific symbionts. Sci Adv 6:eabc6318
Cox EF (2007) Continuation of sexual reproduction in Montipora capitata following bleaching. Coral Reefs 26:721–724
Cunning R, Ritson-Williams R, Gates RD (2016) Patterns of bleaching and recovery of Montipora capitata in Kane’ohe Bay, Hawai’i, USA. Mar Ecol Prog Ser 551:131–139
Dana JD (1846) Zoophytes. United States Exploring Expedition during the years 1838-1842. Lea and Blanchard, Philadelphia 7:709–720
Darwin CR (1876) The effects of cross and self-fertilisation in the vegetable kingdom. London: John Murray
Díaz-Almeyda EM, Prada C, Ohdera AH, Moran H, Civitello DJ, Iglesias-Prieto R, Carlo TA, Lajeunesse TC, Medina M (2017) Intraspecific and interspecific variation in thermotolerance and photoacclimation in Symbiodinium dinoflagellates. Proc R Soc B Biol Sci 284:20171767
Dietzel A, Bode M, Connolly SR, Hughes TP (2021) The population sizes and global extinction risk of reef-building coral species at biogeographic scales. Nat Ecol Evol 5:663–669
Dilworth J, Caruso C, Kahkejian VA, Baker AC, Drury C (2021) Host genotype and stable differences in algal symbiont communities explain patterns of thermal stress response of Montipora capitata following thermal pre-exposure and across multiple bleaching events. Coral Reefs 40:151–163
Dixon GB, Davies SW, Aglyamova GA, Meyer E, Bay LK, Matz MV (2015) Genomic determinants of coral heat tolerance across latitudes. Science 348:1460–1462
Drury C (2020) Resilience in reef-building corals: The ecological and evolutionary importance of the host response to thermal stress. Mol Ecol 29:448–465
Drury C, Dilworth J, Majerová E, Caruso C, Greer JB (2022b) Expression plasticity regulates intraspecific variation in the acclimatization potential of a reef-building coral. Nat Commun 13:4790
Drury C, Bean NK, Harris CI, Hancock JR, Huckeba J, Christian Martin H, Roach TNF, Quinn RA, Gates RD (2022a) Intrapopulation adaptive variance supports thermal tolerance in a reef-building coral. Commun Biol 5:486
Ellner S, Hairston NG (1994) Role of overlapping generations in maintaining genetic variation in a fluctuating environment. Am Nat 143:403–417
Evans JP, Sherman CDH (2013) Sexual selection and the evolution of egg-sperm interactions in broadcast-spawning invertebrates. Biol Bull 224:166–183
Fuller ZL, Mocellin VJL, Morris L, Cantin N, Shepherd J, Sarre L, Peng J, Liao Y, Pickrell J, Andolfatto P, Matz M, Bay LK, Przeworski M (2019) Population genetics of the coral Acropora millepora: Towards a genomic predictor of bleaching. Science 369:6501
Gaither MR, Szabó Z, Crepeau MW, Bird CE, Toonen RJ (2011) Preservation of corals in salt-saturated DMSO buffer is superior to ethanol for PCR experiments. Coral Reefs 30:329–333
Glynn PW, Perez M, Gilchrist SL (1985) Lipid decline in stressed corals and their crustacean symbionts. Ref Biol Bull 168:276–284
Goulet TL, Erill I, Ascunce MS, Finley SJ, Javan GT (2020) Conceptualization of the holobiont paradigm as it pertains to corals. Front Physiol 11:566968
Hancock JR, Barrows AR, Roome TC, Huffmyer AS, Matsuda SB, Munk NJ, Rahnke SA, Drury C (2021) Coral husbandry for ocean futures: Leveraging abiotic factors to increase survivorship, growth, and resilience in juvenile Montipora capitata. Mar Ecol Prog Ser 657:123–133
Harii S, Yamamoto M, Hoegh-Guldberg O (2010) The relative contribution of dinoflagellate photosynthesis and stored lipids to the survivorship of symbiotic larvae of the reef-building corals. Mar Biol 157:1215–1224
Harris CI, Bean NK, Baker AC, Gates RD, Drury C (2022) Stable symbiont communities persist in parents, gametes, and larvae of Montipora capitata across historical bleaching phenotypes. Coral Reefs 41:1627–1636
Hartfield M, Bataillon T, Glémin S (2017) The evolutionary interplay between adaptation and self-fertilization. Trends Genet 33:420–431
Henley EM, Quinn M, Bouwmeester J, Daly J, Zuchowicz N, Lager C, Bailey DW, Hagedorn M (2021) Reproductive plasticity of Hawaiian Montipora corals following thermal stress. Sci Rep. 11:1–17
Hoegh-Guldberg O, Kennedy EV, Beyer HL, McClennen C, Possingham HP (2018) Securing a long-term future for coral reefs. Trends Ecol Evol 33:936–944
Howe-Kerr LI, Bachelot B, Wright RM, Kenkel CD, Bay LK, Correa AMS (2020) Symbiont community diversity is more variable in corals that respond poorly to stress. Glob Chang Biol 26:2220–2234
Howells EJ, Abrego D, Meyer E, Kirk NL, Burt JA (2016a) Host adaptation and unexpected symbiont partners enable reef-building corals to tolerate extreme temperatures. Glob Chang Biol 22:2702–2714
Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, van Oppen MJH (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Chang 2:116–120
Howells EJ, Ketchum RN, Bauman AG, Mustafa Y, Watkins KD, Burt JA (2016b) Species-specific trends in the reproductive output of corals across environmental gradients and bleaching histories. Mar Pollut Bull 105:532–539
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:eabg6070
Huffmyer AS, Wong KH, Becker DM, Strand E, Mass T, Putnam HM (2023) Nutritional exchange between reef-building corals and algal endosymbionts buffers the energetic demand of larval development and metamorphosis. bioRxiv: https://doi.org/10.1101/2023.03.20.533475
Hume BCC, Smith EG, Ziegler M, Warrington HJM, Burt JA, LaJeunesse TC, Wiedenmann J, Voolstra CR (2019) SymPortal: A novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Mol Ecol Resour 19:1063–1080
Innis T, Cunning R, Ritson-Williams R, Wall CB, Gates RD (2018) Coral color and depth drive symbiosis ecology of Montipora capitata in Kāne’ohe Bay, O’ahu, Hawai’i. Coral Reefs 37:423–430
Jarne P, Auld JR (2006) Animals mix it up too: The distribution of self-fertilization among hermaphroditic animals. Evolution 60:1816–1824
Johnston EC, Cunning R, Burgess SC (2022) Cophylogeny and specificity between cryptic coral species (Pocillopora spp.) at Mo′orea and their symbionts (Symbiodiniaceae). Mol Ecol 31:5368–5385
Johnston EC, Counsell CW, Sale TL, Burgess SC, Toonen RJ (2020) The legacy of stress: Coral bleaching impacts reproduction years later. Funct Ecol 34:2315–2325
Jokiel P, Hampton Bigger C (1983) Clonal population structure of two sympatric species of the reef coral Montipora. Bull Mar Sci 33:181–187
Kassambara A, Kosinski M, Biecek P, Fabian S (2021) survminer: Drawing survival curves using “ggplot2.” https://CRAN.R-project.org/package=survminer
Kessel GM, Phillips NE (2018) Global change scenarios trigger carry-over effects across life stages and generations of the intertidal limpet, Siphonaria australis. PLoS One 13:e0194645
Kolinski SP, Cox EF (2003) An update on modes and timing of gamete and planula release in Hawaiian scleractinian corals with implications for conservation and management. Pac Sci Univ Hawai’i Press 57:17–27
Lagerstrom KM, Vance S, Cornwell BH, Ruffley M, Bellagio T, Exposito-Alonso M, Palumbi SR, Hadly EA (2022) From coral reefs to Joshua trees: What ecological interactions teach us about the adaptive capacity of biodiversity in the Anthropocene. Philos Trans R Soc B Biol Sci 377:20210389
LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580
Lewis C, Neely K, 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
Matsuda SB, Chakravarti LJ, Cunning R, Huffmyer AS, Nelson CE, Gates RD, van Oppen MJH (2022) Temperature-mediated acquisition of rare heterologous symbionts promotes survival of coral larvae under ocean warming. Glob Chang Biol 28:2006–2025
Matthews JL, Cunning R, Witson-Williams R, Oakley CA, Lutz A, Roessner U, Grossman AR, Weis VM, Gates RD, Davy SK (2022) The metabolic significance of symbiont community composition in the coral-algal symbiosis. Applied Environmental Metabolomics: Community Insights and Guidance from the Field, Elsevier pp 211–229
Matz MV, Treml EA, Aglyamova GV, Bay LK (2018) Potential and limits for rapid genetic adaptation to warming in a Great Barrier Reef coral. PLoS Genet 14(4):e1007220–19
Mauritsen T, Pincus R (2017) Committed warming inferred from observations. Nat Clim Chang 7:652–655
McIlroy SE, Cunning R, Baker AC, Coffroth MA (2019) Competition and succession among coral endosymbionts. Ecol Evol 9:12767–12778
McLachlan RH, Price JT, Solomon SL, Grottoli AG (2020) Thirty years of coral heat-stress experiments: a review of methods. Coral Reefs 39:885–902
Meyer E, Davies S, Wang S, Willis B, Abrego D, Juenger T, Matz M (2009) Genetic variation in responses to a settlement cue and elevated temperature in the reef-building coral Acropora millepora. Mar Ecol Prog Ser 392:81–92
Michalek-Wagner K, Willis BL (2001a) Impacts of bleaching on the soft coral Lobophytum compactum. I. Fecundity, fertilization and offspring viability. Coral Reefs 19:231–239
Michalek-Wagner K, Willis BL (2001b) Impacts of bleaching on the soft coral Lobophytum compactum. II. Biochemical changes in adults and their eggs. Coral Reefs 19:240–246
Minuti JJ, Byrne M, Campbell H, Hemraj DA, Russell BD (2022) Live-fast-die-young: Carryover effects of heatwave-exposed adult urchins on the development of the next generation. Glob Chang Biol 28:5781–5792
Mohamed AR, Ochsenkühn MA, Kazlak A, Moustafa A, Amin SA (2023) The coral microbiome: Towards an understanding of the molecular mechanisms of coral-microbiota interactions. FEMS Microbiol Rev 47(2):fuad005
Muir PR, Obura DO, Hoeksema BW, Sheppard C, Pichon M, Richards ZT (2022) Conclusions of low extinction risk for most species of reef-building corals are premature. Nat Ecol Evol 6:357–358
Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: An integrated framework for good genes and compatible genes. Mol Ecol 14:19–38
Nitschke M, Rosset S, Oakley C, Gardner S, Camp E, Suggett D, Davey S (2022) The diversity and ecology of Symbiodiniaceae: A traits-based review. Adv Marine Biol 92:55–109
Oliver J, Berkelmans R, Eakin C (2018) Coral Bleaching in Space and Time. In: van Oppen M.J.H & Lough J.M (eds), Coral Bleaching: Patterns, Processes, Causes and Consequences 2nd Edition. Ecological Studies, Chapter 3, 233, Springer, Berlin, 356 pp
Olsen KC, Ryan WH, Winn AA, Kosman ET, Moscoso JA, Krueger-Hadfield SA, Burgess SC, Carlon DB, Grosberg RK, Kalisz S, Levitan DR (2020) Inbreeding shapes the evolution of marine invertebrates. Evolution 74:871–882
van Oppen MJH, Blackall LL (2019) Coral microbiome dynamics, functions and design in a changing world. Nat Rev Microbiol 17:557–567
Padilla-Gamiño JL, Pochon X, Bird C, Concepcion GT, Gates RD (2012) From parent to gamete: Vertical transmission of Symbiodinium (Dinophyceae) ITS2 sequence assemblages in the reef building coral Montipora capitata. PLoS One 7(6):e38440
Parkinson JE, Baums IB (2014) The extended phenotypes of marine symbioses: Ecological and evolutionary consequences of intraspecific genetic diversity in coral-algal associations. Front Microbiol 5:1–19
Parkinson JE, Banaszak AT, Altman NS, LaJeunesse TC, Baums IB (2015) Intraspecific diversity among partners drives functional variation in coral symbioses. Sci Rep 5:15667
Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139:1069–1078
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
Quigley KM, Willis BL, Kenkel CD (2019) Transgenerational inheritance of shuffled symbiont communities in the coral Montipora digitata. Sci Rep. 9:13328
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
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(3):e13342
Rahnke SA, Hancock JR, Munk NJ, Caruso C, Drury C (2022) Optimizing sexual reproduction of Montipora capitata for restoration: effects of abiotic conditions and light acclimation on juvenile survival and growth. Mar Ecol Prog Ser 691:41–54
Roach TNF, Dilworth J, Christian Martin H, Jones AD, Quinn RA, Drury C (2021) Metabolomic signatures of coral bleaching history. Nat Ecol Evol 5:495–503
Rocha de Souza M, Caruso C, Ruiz-Jones L, Drury C, Gates R, Toonen RJ (2022) Community composition of coral-associated Symbiodiniaceae differs across fine-scale environmental gradients in Kāne’ohe Bay. R Soc Open Sci 9:212042
Rodrigues LJ, Padilla-Gamiño JL (2022) Trophic provisioning and parental trade-offs lead to successful reproductive performance in corals after a bleaching event. Sci Rep 12:18702
Rose NH, Bay RA, Morikawa MK, Palumbi SR (2018) Polygenic evolution drives species divergence and climate adaptation in corals. Evolution 72:82–94
Sanford E, Kelly MW (2011) Local adaptation in marine invertebrates. Ann Rev Mar Sci 3:509–535
Sgrò CM, Lowe AJ, Hoffmann AA (2011) Building evolutionary resilience for conserving biodiversity under climate change. Evol Appl 4:326–337
Shah S, Dougan KE, Bhattacharya D, Chan CX (2022) Coral conservation from the genomic perspective onSymbiodiniaceae diversity and function in the holobiont. In: Coral Reef Conservation and Restoration in the ‘Omics’Age” [van Oppen M, Aranda M (eds), Springer. https://doi.org/10.1007/978-3-031-07055-6_6
Smith EG, Hazzouri KM, Choi JY, Delaney P, Al-Kharafi M, Howells EJ, Aranda M, Burt JA (2022) Signatures of selection underpinning rapid coral adaptation to the world’s warmest reefs. Sci Adv 8:eabl7287
Stat M, Pochon X, Cowie ROM, Gates RD (2009) Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar Ecol Prog Ser 386:83–96
Therneau TM (2023) A Package for Survival Analysis in R. https://cran.r-project.org/web/packages/survival/vignettes/survival.pdf
Thomas L, Rose NH, Bay RA, López EH, Morikawa MK, Ruiz-Jones L, Palumbi SR (2018) Mechanisms of thermal tolerance in reef-building corals across a fine-grained environmental mosaic: Lessons from Ofu. Am Samoa Front Mar Sci 4:434
Torda G, Donelson JM, Aranda M, Barshis DJ, Bay L, Berumen ML, Bourne DG, Cantin N, Foret S, Matz M, Miller DJ, Moya A, Putnam HM, Ravasi T, van Oppen MJH, Thurber RV, Vidal-Dupiol J, Voolstra CR, Watson SA, Whitelaw E, Willis BL, Munday PL (2017) Rapid adaptive responses to climate change in corals. Nat Clim Chang 7:627–636
Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: Invited review. Mol Ecol 9:1013–1027
Turnham KE, Wham DC, Sampayo E, LaJeunesse TC (2021) Mutualistic microalgae co-diversify with reef corals that acquire symbionts during egg development. ISME J 15:3271–3285
Voolstra CR, Suggett DJ, Peixoto RS, Parkinson JE, Quigley KM, Silveira CB, Sweet M, Muller EM, Barshis DJ, Bourne DG, Aranda M (2021) Extending the natural adaptive capacity of coral holobionts. Nat Rev Earth Environ 2:747–762
Wall CB, Kaluhiokalani M, Popp BN, Donahue MJ, Gates RD (2020) Divergent symbiont communities determine the physiology and nutrition of a reef coral across a light-availability gradient. ISME J 14:945–958
Ward S, Harrison P (2002) Coral bleaching reduces reproduction of scleractinian corals andincreases susceptibility to future stress. Paper presented at the Proceedings of the Ninth International Coral Reef Symposium, Bali, 23–27 October 2000
Acknowledgements
We gratefully acknowledge Hanalei Hoʻopai-Sylva, Khalil Smith, Josh Hancock, Madeleine Sherman, Maile Villablanca, Jasmine Chang, Ninah Munk, and the Coral Resilience Lab for spawning assistance. We also thank three anonymous reviewers for their edits and suggestions that improved this manuscript. This work was funded by the Paul G. Allen Family Foundation, NOAA Award NA20NMF4820290, and DARPA. Coral fragments and gamete bundles were collected under Hawaii DLNR permit SAP 2023-31 to HIMB. This is HIMB contribution 1949 and SOEST contribution 11780.
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CC, ECJ and CD conceived the experiment. All authors collected data. ECJ and CD analyzed data. ECJ wrote the manuscript. All authors edited the manuscript and approved the final version.
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Johnston, E.C., Caruso, C., Mujica, E. et al. Complex parental effects impact variation in larval thermal tolerance in a vertically transmitting coral. Heredity (2024). https://doi.org/10.1038/s41437-024-00681-6
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DOI: https://doi.org/10.1038/s41437-024-00681-6