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Mutualistic microalgae co-diversify with reef corals that acquire symbionts during egg development

Abstract

The application of molecular genetics has reinvigorated and improved how species are defined and investigated scientifically, especially for morphologically cryptic micro-organisms. Here we show how species recognition improves understanding of the ecology and evolution of mutualisms between reef-building corals and their mutualistic dinoflagellates (i.e. Symbiodiniaceae). A combination of genetic, ecological, and morphological evidence defines two sibling species of Cladocopium (formerly Symbiodinium Clade C), specific only to host corals in the common genus Pocillopora, which transmit their obligate symbionts during oogenesis. Cladocopium latusorum sp. nov. is symbiotic with P. grandis/meandrina while the smaller-celled C. pacificum sp. nov. associates with P. verrucosa. Both symbiont species form mutualisms with Pocillopora that brood their young. Populations of each species, like their hosts, are genetically well connected across the tropical and subtropical Pacific Ocean, indicating a capacity for long-range dispersal. A molecular clock approximates their speciation during the late Pliocene or early Pleistocene as Earth underwent cycles of precipitous cooling and warming; and corresponds to when their hosts were also diversifying. The long temporal and spatial maintenance of high host fidelity, as well as genetic connectivity across thousands of kilometers, indicates that distinct ecological attributes and close evolutionary histories will restrain the adaptive responses of corals and their specialized symbionts to rapid climate warming.

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Fig. 1: Collection locations, light micrographs, and cell sizes of symbiotic dinoflagellates from corals in the genus Pocillopora.
Fig. 2: Phylogenetic and population genetic data resolving two species of Cladocopium.
Fig. 3: High-resolution phylogenetic analysis of Cladocopium latusorum and C. pacificum.
Fig. 4: Age estimates for the co-diversification of Cladocopium with their pocilloporid hosts.

References

  1. 1.

    Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, et al. Cryptic species as a window on diversity and conservation. Trends Ecol Evol. 2007;22:148–55.

    PubMed  PubMed Central  Article  Google Scholar 

  2. 2.

    Tewksbury JJ, Anderson JGT, Bakker JD, Billo TJ, Dunwiddie PW, Groom MJ, et al. Natural history’s place in science and society. Bioscience. 2014;64:300–10.

    Article  Google Scholar 

  3. 3.

    Leliaert F, Verbruggen H, Vanormelingen P, Steen F, López-Bautista JM, Zuccarello GC, et al. DNA-based species delimitation in algae. Eur J Phycol. 2014;49:179–96.

    Article  Google Scholar 

  4. 4.

    Potter D, LaJeunesse TC, Saunders GW, Anderson RA. Convergent evolution masks extensive biodiversity among marine coccoid picoplankton. Biodivers Conserv. 1997;6:99–107.

    Article  Google Scholar 

  5. 5.

    de Vargas C, Norris R, Zaninetti L, Gibb SW, Pawlowski J. Molecular evidence of cryptic speciation in planktonic foraminifers and their relation to oceanic provinces. Proc Natl Acad Sci USA. 1999;96:2864–8.

    PubMed  Article  PubMed Central  Google Scholar 

  6. 6.

    John U, Litaker RW, Montresor M, Murray S, Brosnahan ML, Anderson DM. Formal revision of the alexandrium tamarense species complex (dinophyceae) taxonomy: the introduction of five species with emphasis on molecular-based (rDNA) classification. Protist. 2014;165:779–804.

    PubMed  PubMed Central  Article  Google Scholar 

  7. 7.

    Hoppenrath M, Reñé A, Satta CT, Yamaguchi A, Leander BS. Morphology and molecular phylogeny of a new marine, sand-dwelling dinoflagellate genus, Pachena (Dinophyceae), with descriptions of three new species. J Phycol. 2020;56:798–817.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  8. 8.

    Sproles AE, Oakley CA, Krueger T, Grossman AR, Weis VM, Meibom A, et al. Sub-cellular imaging shows reduced photosynthetic carbon and increased nitrogen assimilation by the non-native endosymbiont Durusdinium trenchii in the model cnidarian Aiptasia. Environ Microbiol. 2020;22:3741–53.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  9. 9.

    Hume BCC, Mejia-Restrepo A, Voolstra CR, Berumen ML. Fine-scale delineation of Symbiodiniaceae genotypes on a previously bleached central Red Sea reef system demonstrates a prevalence of coral host-specific associations. Coral Reefs. 2020;39:583–601.

    Article  Google Scholar 

  10. 10.

    Gabay Y, Parkinson JE, Wilkinson SP, Weis VM, Davy SK. Inter-partner specificity limits the acquisition of thermotolerant symbionts in a model cnidarian-dinoflagellate symbiosis. ISME J. 2019;13:2489–99.

    PubMed  PubMed Central  Article  Google Scholar 

  11. 11.

    Tivey TR, Parkinson JE, Weis VM. Host and symbiont cell cycle coordination is mediated by symbiotic state, nutrition, and partner identity in a model cnidarian-dinoflagellate symbiosis. MBio. 2020;11:1–17.

    Article  Google Scholar 

  12. 12.

    Lawson CA, Possell M, Seymour JR, Raina JB, Suggett DJ. Coral endosymbionts (Symbiodiniaceae) emit species-specific volatilomes that shift when exposed to thermal stress. Sci Rep. 2019;9:1–11.

    Google Scholar 

  13. 13.

    Reich HG, Rodriguez IB, LaJeunesse TC, Ho TY. Endosymbiotic dinoflagellates pump iron: differences in iron and other trace metal needs among the Symbiodiniaceae. Coral Reefs. 2020;39:915–27.

    Article  Google Scholar 

  14. 14.

    de Queiroz A, Gatesy J. The supermatrix approach to systematics. Trends Ecol Evol. 2007;22:34–41.

    PubMed  Article  PubMed Central  Google Scholar 

  15. 15.

    de Queiroz K. Species concepts and species delimitation. Syst Biol. 2007;56:879–86.

    PubMed  PubMed Central  Article  Google Scholar 

  16. 16.

    Schönrogge K, Barr B, Wardlaw JC, Napper E, Gardner MG, Breen J, et al. When rare species become endangered: Cryptic speciation in myrmecophilous hoverflies. Biol J Linn Soc. 2002;75:291–300.

    Article  Google Scholar 

  17. 17.

    Pettay DT, Wham DC, Pinzón JH, LaJeunesse TC. Genotypic diversity and spatial-temporal distribution of Symbiodinium clones in an abundant reef coral. Mol Ecol. 2011;20:5197–212.

    PubMed  PubMed Central  Article  Google Scholar 

  18. 18.

    Baums IB, Devlin-Durante MK, LaJeunesse TC. New insights into the dynamics between reef corals and their associated dinoflagellate endosymbionts from population genetic studies. Mol Ecol. 2014;23:4203–15.

    PubMed  Article  PubMed Central  Google Scholar 

  19. 19.

    Pinzón JH, LaJeunesse TC. Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology. Mol Ecol. 2011;20:311–25.

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  20. 20.

    Sampayo EM, Dove S, LaJeunesse TC. Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol. 2009;18:500–19.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  21. 21.

    Lien AY, Fukami H, Yamashita Y, Lien Y, Fukami H, Yamashita Y. Symbiodinium Clade C dominates zooxanthellate corals (Scleractinia) in the temperate region of Japan. Zool Sci. 2012;29:173–80.

    Article  Google Scholar 

  22. 22.

    LaJeunesse TC. ‘Species’ radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol. 2005;22:570–81.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  23. 23.

    Wham DC, Carmichael M, LaJeunesse TC. Microsatellite loci for Symbiodinium goreaui and other Clade C Symbiodinium. Conserv Genet Resour. 2014;6:127–9.

    Article  Google Scholar 

  24. 24.

    LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Borwn B, Obura DO, et al. Long standing environmental conditions, geographic isolation and host-symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr. 2010;11:674–5.

    Google Scholar 

  25. 25.

    Thornhill DJ, Lewis AM, Wham DC, LaJeunesse TC. Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution. 2014;68:352–67.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  26. 26.

    LaJeunesse TC, Bhagooli R, Hidaka M, DeVantier L, Done T, Schmidt GW, et al. Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser. 2004;284:147–61.

    Article  Google Scholar 

  27. 27.

    Fitt WK, Gates RD, Hoegh-Guldberg O, Bythell JC, Jatkar A, Grottoli AG, et al. Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: The host does matter in determining the tolerance of corals to bleaching. J Exp Mar Bio Ecol. 2009;373:102–10.

    Article  Google Scholar 

  28. 28.

    Hume B, D’Angelo C, Burt J, Baker AC, Riegl B, Wiedenmann J. Corals from the Persian/Arabian Gulf as models for thermotolerant reef-builders: Prevalence of clade C3 Symbiodinium, host fluorescence and ex situ temperature tolerance. Mar Pollut Bull. 2013;72:313–22.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  29. 29.

    Hoadley KD, Lewis AM, Wham DC, Pettay DT, Grasso C, Smith R, et al. Host – symbiont combinations dictate the photo-physiological response of reef-building corals to thermal stress. Sci Rep. 2019:9:1–15.

  30. 30.

    Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg O. Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci USA. 2008;105:10444–9.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  31. 31.

    Lee SY, Jeong HJ, LaJeunesse TC. Cladocopium infistulum sp. nov. (Dinophyceae), a thermally tolerant dinoflagellate symbiotic with giant clams from the western Pacific Ocean. Phycologia. 2020;59:515–26.

    Article  Google Scholar 

  32. 32.

    LaJeunesse TC, Wham DC, Pettay DT, Parkinson JE, Keshavmurthy S, Chen CA. Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus Symbiodinium (Dinophyceae) Clade D are different species. Phycologia. 2014;53:305–19.

    Article  Google Scholar 

  33. 33.

    Lewis AM, Chan AN, LaJeunesse TC. New species of closely related endosymbiotic dinoflagellates in the greater caribbean have niches corresponding to host coral phylogeny. J Eukaryot Microbiol. 2019;66:469–82.

    PubMed  Article  PubMed Central  Google Scholar 

  34. 34.

    Veron JEN. Corals of the world. In: Stafford-Smith M, editor. Australian Institute of Marine Science; Townsville, Australia, 2000.

  35. 35.

    Richmond RH. Energetics, competency, and long-distance dispersal of planula larvae of the coral Pocillopora damicornis. Mar Biol. 1987;93:527–33.

    Article  Google Scholar 

  36. 36.

    Harrison PL, Wallace CC. A review of reproduction, larval dispersal and settlement of scleractinian corals. In: Dubinsky Z, editor. Ecosystems of the World 25 Coral Reefs; New York, NY, USA, 1990. p. 133–96

  37. 37.

    Glynn PW. Coral reef bleaching: ecological perspectives. Coral Reefs. 1993;12:1–17.

    Article  Google Scholar 

  38. 38.

    LaJeunesse TC, Smith R, Walther M, Pinzon J, Pettay DT, McGinley M, et al. Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proc R Soc B Biol Sci. 2010;277:2925–34.

    Article  Google Scholar 

  39. 39.

    Stella JS, Pratchett MS, Hutchings PA, Jones GP. Coral-associated invertebrates: diversity, ecological importance and vulnerability to disturbance. Oceanogr Mar Biol Annu Rev. 2011;49:43–104.

    Google Scholar 

  40. 40.

    Austin AD, Austin SA, Sale PF. Community structure of the fauna associated with the coral Pocillopora damicornis (L.) on the Great Barrier Reef. Mar Freshw Res. 1980;31:163–74.

    Article  Google Scholar 

  41. 41.

    Glynn PW, Maté JL, Baker AC. Coral bleaching and mortality in Panama and Ecuador during the 1997 – 1998 El Niño – southern oscillation event: spatial/temporal patterns and comparisons with the 1982 – 1983 event. Bull Mar Sci. 2001;69:79–109.

    Google Scholar 

  42. 42.

    Johnston EC, Forsman ZH, Flot J, Schmidt-Roach S, Pinzón H, Knapp ISS, et al. A genomic glance through the fog of plasticity and diversification in Pocillopora. Sci Rep. 2017;7:5991.

  43. 43.

    Iglesias-Prieto R, Beltrán VH, LaJeunesse TC, Reyes-Bonilla H, Thomé PE. Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc R Soc B Biol Sci. 2004;271:1757–63.

    CAS  Article  Google Scholar 

  44. 44.

    Bahr KD, Tran T, Jury CP, Toonen RJ. Abundance, size, and survival of recruits of the reef coral Pocillopora acuta under ocean warming and acidification. PLoS ONE. 2020;15:1–13.

    Article  CAS  Google Scholar 

  45. 45.

    Flot JF, Tillier S. The mitochondrial genome of Pocillopora (Cnidaria: Scleractinia) contains two variable regions: The putative D-loop and a novel ORF of unknown function. Gene. 2007;401:80–7.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  46. 46.

    LaJeunesse TC, Loh WKW, Van Woesik R, Schmidt GW, Fitt WK. Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol Oceanogr. 2003;48:2046–54.

    Article  Google Scholar 

  47. 47.

    Tonk L, Sampayo EM, LaJeunesse TC, Schrameyer V, Hoegh-Guldberg O. Symbiodinium (Dinophyceae) diversity in reef-invertebrates along an offshore to inshore reef gradient near Lizard Island, Great Barrier Reef. J Phycol. 2014;50:552–63.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  48. 48.

    Magalon H, Baudry E, Husté A, Adjeroud M, Veuille M. High genetic diversity of the symbiotic dinoflagellates in the coral Pocillopora meandrina from the South Pacific. Mar Biol. 2006;148:913–22.

    Article  Google Scholar 

  49. 49.

    Pinzón JH, Sampayo E, Cox E, Chauka LJ, Chen CA, Voolstra CR, et al. Blind to morphology: genetics identifies several widespread ecologically common species and few endemics among Indo-Pacific cauliflower corals (Pocillopora, Scleractinia). J Biogeogr. 2013;40:1595–608.

    Article  Google Scholar 

  50. 50.

    Silverstein RN, Correa AMS, LaJeunesse TC, Baker AC. Novel algal symbiont (Symbiodinium spp.) diversity in reef corals of Western Australia. Mar Ecol Prog Ser. 2011;422:63–75.

    Article  Google Scholar 

  51. 51.

    Wham DC, LaJeunesse TC. Symbiodinium population genetics: testing for species boundaries and analysing samples with mixed genotypes. Mol Ecol. 2016;25:2699–712.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  52. 52.

    Baums IB, Devlin-durante M, Laing BAA, Feingold J, Smith T, Bruckner A, et al. Marginal coral populations: the densest known aggregation of Pocillopora in the Galápagos Archipelago is of asexual origin. Front Mar Sci. 2014;1:1–11.

    Article  Google Scholar 

  53. 53.

    McGinley MP, Aschaffenburg MD, Pettay DT, Smith RT, LaJeunesse TC, Warner ME. Symbiodinium spp. in colonies of eastern Pacific Pocillopora spp. are highly stable despite the prevalence of low-abundance background populations. Mar Ecol Prog Ser. 2012;462:1–7.

    Article  Google Scholar 

  54. 54.

    Camp EF, Nitschke MR, Rodolfo-metalpa R, Gardner SG, Smith DJ, Zampighi M, et al. Reef-building corals thrive within hot-acidic and deoxygenated waters. Sci Rep. 2017;7:2434.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  55. 55.

    LaJeunesse TC, Trench RK. Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull. 2000;199:126–34.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  56. 56.

    LaJeunesse TC. Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the its region: In search of a “species” level marker. J Phycol. 2001;880:866–80.

    Article  Google Scholar 

  57. 57.

    Moore RB, Ferguson KM, Loh WKW, Hoegh-Guldberg O, Carter DA. Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium. Int J Syst Evol Microbiol. 2003;53:1725–34.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  58. 58.

    LaJeunesse TC, Thornhill DJ. Improved resolution of reef-coral endosymbiont (Symbiodinium) species diversity, ecology, and evolution through psbA non-coding region genotyping. PLoS ONE. 2011;6:e29013.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  59. 59.

    Swofford D. PAUP 4.0: Phylogenetic analysis using parsimony. Washington DC, USA: Smithson Inst.; 2014.

  60. 60.

    Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, et al. Mrbayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539–42.

    PubMed  PubMed Central  Article  Google Scholar 

  61. 61.

    Nylander JAA. MrModeltest v2. Uppsala, Sweden: Progr Distrib by author Evol Biol Centre, Uppsala Univ.; 2004.

  62. 62.

    Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu CH, Xie D, et al. BEAST 2: a software platform for bayesian evolutionary analysis. PLoS Comput Biol. 2014;10:1–6.

    Article  CAS  Google Scholar 

  63. 63.

    Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Syst Biol. 2018;67:901–4.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. 64.

    Jackson JBC, O’Dea A. Timing of the oceanographic and biological isolation of the Caribbean sea from the tropical eastern pacific ocean. Bull Mar Sci. 2013;89:779–800.

    Google Scholar 

  65. 65.

    Haug G, Tiedemann R. Effect of the formation of the Isthmus of Panama on Atlantic Ocean thermohaline circulation. Nature. 1998;394:1699–701.

    Google Scholar 

  66. 66.

    O’Dea A, Lessios HA, Coates AG, Eytan RI, Restrepo-Moreno SA, Cione AL, et al. Formation of the Isthmus of Panama. Sci Adv. 2016;2:1–12.

    Article  Google Scholar 

  67. 67.

    Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 2007;7:214.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  68. 68.

    Bouckaert R, Heled J DensiTree 2: seeing trees through the forest. 2014. https://www.biorxiv.org/content/10.1101/012401v1.

  69. 69.

    Bay LK, Howells EJ, van Oppen MJH. Isolation, characterisation and cross amplification of thirteen microsatellite loci for coral endo-symbiotic dinoflagellates (Symbiodinium clade C). Conserv Genet Resour. 2009;1:199–203.

    Article  Google Scholar 

  70. 70.

    Peakall R, Smouse PE. GenALEx 6.5: genetic analysis in excel. population genetic software for teaching and research-an update. Bioinformatics. 2012;28:2537–9.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  71. 71.

    Davies SW, Moreland KN, Wham DC, Kanke MR, Matz MV. Cladocopium community divergence in two Acropora coral hosts across multiple spatial scales. Mol Ecol. 2020;29:4559–72.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  72. 72.

    Earl DA, vonHoldt BM. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour. 2012;4:359–61.

    Article  Google Scholar 

  73. 73.

    Liu H, Stephens TG, González-Pech RA, Beltran VH, Lapeyre B, Bongaerts P, et al. Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis. Commun Biol. 2018;1:95.

    PubMed  PubMed Central  Article  Google Scholar 

  74. 74.

    Raymond M, Rousset F. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity. 1995:248–9.

  75. 75.

    Rousset F. GENEPOP’007: A complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour. 2008;86:103–6.

    PubMed  PubMed Central  Article  Google Scholar 

  76. 76.

    Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–59.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  77. 77.

    van der Maaten L, Hinton G. Visualizing data using t-SNE. J Mach Learn Res. 2008;9:2579–605.

    Google Scholar 

  78. 78.

    LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol. 2018;28:2570–2580.e6.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  79. 79.

    LaJeunesse TC, Bonilla HR, Warner ME, Wills M, Schmidt GW, Fitt WK. Specificity and stability in high latitude eastern Pacific coral-algal symbioses. Limnol Oceanogr. 2008;53:719–27.

    Article  Google Scholar 

  80. 80.

    Ramsby BD, Hill MS, Thornhill DJ, Steenhuizen SF, Achlatis M, Lewis AM, et al. Sibling species of mutualistic Symbiodinium Clade G from bioeroding sponges in the western Pacific and western Atlantic oceans. J Phycol. 2017;53:951–60.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  81. 81.

    Prada C, McIlroy SE, Beltrán DM, Valint DJ, Ford SA, Hellberg ME, et al. Cryptic diversity hides host and habitat specialization in a gorgonian-algal symbiosis. Mol Ecol. 2014;23:3330–40.

    PubMed  Article  PubMed Central  Google Scholar 

  82. 82.

    Wham DC, Ning G, LaJeunesse TC. Symbiodinium glynnii sp. nov., a species of stress-tolerant symbiotic dinoflagellates from pocilloporid and montiporid corals in the Pacific Ocean. Phycologia. 2017;56:396–409.

    CAS  Article  Google Scholar 

  83. 83.

    Mayr E. The growth of biological thought: Diversity, evolution, and inheritance. Cambridge, MA, USA: Belknap Press of Harvard University Press; 1982.

  84. 84.

    Arnaud-Haond S, Duarte CM, Alberto F, Serrão EA. Standardizing methods to address clonality in population studies. Mol Ecol. 2007;16:5115–39.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  85. 85.

    Jeong HJ, Lee SY, Kang NS, Yoo YD, Lim AS, Lee MJ, et al. Genetics and morphology characterize the dinoflagellate Symbiodinium voratum, n. sp., (dinophyceae) as the sole representative of Symbiodinium Clade E. J Eukaryot Microbiol. 2014;61:75–94.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  86. 86.

    Blank RJ, Trench RK. Speciation and symbiotic dinoflagellates. Science. 1985;229:656–8.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  87. 87.

    Suggett DJ, Moore CM, Hickman AE, Geider RJ. Interpretation of fast repetition rate (FRR) fluorescence: Signatures of phytoplankton community structure versus physiological state. Mar Ecol Prog Ser. 2009;376:1–19.

    Article  Google Scholar 

  88. 88.

    Suggett DJ, Goyen S, Evenhuis C, Szabó M, Pettay DT, Warner ME, et al. Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation. New Phytol. 2015;208:370–81.

    PubMed  Article  PubMed Central  Google Scholar 

  89. 89.

    Geider R, Piatt T, Raven J. Size dependence of growth and photosynthesis in diatoms: a synthesis. Mar Ecol Prog Ser. 1986;30:93–104.

    CAS  Article  Google Scholar 

  90. 90.

    Finkel ZV. Light absorption and size scaling of light-limited metabolism in marine diatoms. Limnol Oceanogr. 2001;46:86–94.

    CAS  Article  Google Scholar 

  91. 91.

    Irwin AJ, Finkel ZV, Schofield OME, Falkowski PG. Scaling-up from nutrient physiology to the size-structure of phytoplankton communities. J Plankton Res. 2006;28:459–71.

    Article  Google Scholar 

  92. 92.

    Wu Y, Campbell DA, Irwin AJ, Suggett DJ, Finkel ZV. Ocean acidification enhances the growth rate of larger diatoms. Limnol Oceanogr. 2014;59:1027–34.

    CAS  Article  Google Scholar 

  93. 93.

    Rowan R. Coral bleaching: thermal adaptation in reef coral symbionts. Nature. 2004;430:742.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  94. 94.

    Berkelmans R, Van, Oppen MJH. The role of zooxanthellae in the thermal tolerance of corals: a “nugget of hope” for coral reefs in an era of climate change. Proc R Soc B Biol Sci. 2006;273:2305–12.

    Article  Google Scholar 

  95. 95.

    Abrego D, Ulstrup KE, Willis BL, Van Oppen MJH. Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proc R Soc B Biol Sci. 2008;275:2273–82.

    CAS  Article  Google Scholar 

  96. 96.

    Schluter D. Evidence for ecological speciation and its alternative. Science. 2009;323:737–41.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  97. 97.

    Hendry AP, Nosil P, Rieseberg LH. The speed of ecological speciation. Funct Ecol. 2007;21:455–64.

    PubMed  PubMed Central  Article  Google Scholar 

  98. 98.

    Glynn PW, Gassman NJ, Eakin CM, Cortes J, Smith DB, Guzman HM. Reef coral reproduction in the eastern Pacific: Costa Rica, Panama, and Galapagos Islands (Ecuador). Mar Biol. 1991;109:355–68.

    Article  Google Scholar 

  99. 99.

    Hirose M, Kinzie RA, Hidaka M. Early development of zooxanthella-containing eggs of the corals Pocillopora verrucosa and P. eydouxi with special reference to the distribution of zooxanthellae. Biol Bull. 2000;199:68–75.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  100. 100.

    Chavez-Romo H. Sexual reproduction of the coral Pocillopora damicornis in the southern Gulf of California. Mex Cienc Mar. 2007;33:495–501.

    Article  Google Scholar 

  101. 101.

    Russell SL, Chappell L, Sullivan W. A symbiont’s guide to the germline. 1st ed. In: Current topics in developmental biology. Vol 135. Amsterdam, The Netherlands: Elsevier Inc.; 2019. p. 351.

  102. 102.

    LaJeunesse TC, Thornhill DJ, Cox EF, Stanton FG, Fitt WK, Schmidt GW. High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs. 2004;23:596–603.

    Google Scholar 

  103. 103.

    Rowan ROB, Powers DA. A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science. 1991;251:1348–51.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  104. 104.

    Zachos JC, Dickens GR, Zeebe RE. An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature. 2008;451:279–83.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  105. 105.

    LaJeunesse TC, Parkinson JE, Reimer JD. A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (dinophyceae), two dinoflagellates symbiotic with cnidaria. J Phycol. 2012;48:1380–91.

    PubMed  Article  PubMed Central  Google Scholar 

  106. 106.

    Pettay DT, LaJeunesse TC. Long-range dispersal and high-latitude environments influence the population structure of a “stress-tolerant” dinoflagellate endosymbiont. PLoS ONE. 2013;8:1–12.

    Article  CAS  Google Scholar 

  107. 107.

    Wicks LC, Sampayo E, Gardner JPA, Davy SK. Local endemicity and high diversity characterise high-latitude coral- Symbiodinium partnerships. Coral Reefs. 2010;29:989–1003.

    Article  Google Scholar 

  108. 108.

    Sampayo EM, Franceschinis L, Hoegh-Guldberg O, Dove S. Niche partitioning of closely related symbiotic dinoflagellates. Mol Ecol. 2007;16:3721–33.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  109. 109.

    Thompson JN. The geographic mosaic of coevolution. Chicago, IL, USA: University of Chicago Press; 2005.

  110. 110.

    Sampayo EM, Ridgway T, Franceschinis L, Roff G, Hoegh-Guldberg O, Dove S. Coral symbioses under prolonged environmental change: living near tolerance range limits. Sci Rep. 2016;6:36271.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  111. 111.

    Janis CM. Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events. Annu Rev Ecol Syst. 1993;24:467–500.

    Article  Google Scholar 

  112. 112.

    Willeit M, Ganopolski A, Calov R, Brovkin V. Mid-Pleistocene transition in glacial cycles explained by declining CO2 and regolith removal. Sci Adv. 2019;5:eaav7337.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  113. 113.

    Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA. Mechanisms of reef coral resistance to future climate change. Science. 2014;344:895–8.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  114. 114.

    Pandolfi JM, Jackson JBC, Geister J. Geologically sudden extinction of two widespread late Pleistocene Caribbean reef corals. In: Evolutionary patterns: growth, form and tempo in the fossil record. Chicago, IL, USA: University of Chicago Press; 2001. p. 120–58.

  115. 115.

    Toth LT, Aronson RB, Cobb KM, Cheng H, Edwards RL, Grothe PR, et al. Climatic and biotic thresholds of coral-reef shutdown. Nat Clim Chang. 2015;5:369–74.

    Article  Google Scholar 

  116. 116.

    Baums IB, Baker AC, Davies SW, Grottoli AG, Kenkel CD, Kitchen SA, et al. Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic. Ecol Appl. 2019;29:1–23.

    Article  Google Scholar 

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Acknowledgements

The authors wish to thank Jorge Pinzon, Andie Chan, Chaolun Allen Chen, Linda Tonk, Iliana Baums, Rachel Silverstein, Sarah Davies, David Suggett’s lab, and Adrienne Correa’s lab, who contributed Pocillopora samples, as well as Ove Hoegh-Guldberg and Allison M. Lewis for photos of Pocillopora. We are grateful to Allison M. Lewis and Scott R. Santos and for assistance with data analysis. We are grateful for the valuable feedback from Adrienne Correa and two anonymous reviewers, which improved the paper. We would like to also thank Palau International Coral Reef Center (PICRC) for providing support during sample collections, which were made possible with permission from the Ministry of Natural Resources, Environment and Tourism, Palau, and from the Koror State Government, Department of Conservation and Law Enforcement. This project was supported by the USA National Science Foundation (IOS-1258058 and OCE-1636022 to TCL), NTRGP Australian Biodiversity Resources Study (ID 4-EHOJ1F5) to ES and TCL, the Society of Systematic Biologists (to KET), and the Pennsylvania State University.

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Correspondence to Kira E. Turnham or Todd C. LaJeunesse.

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Turnham, K.E., Wham, D.C., Sampayo, E. et al. Mutualistic microalgae co-diversify with reef corals that acquire symbionts during egg development. ISME J (2021). https://doi.org/10.1038/s41396-021-01007-8

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