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Abstract

Marine organisms’ persistence hinges on the capacity for acclimatization and adaptation to the myriad of interacting environmental stressors associated with global climate change. In this context, epigenetics—mechanisms that facilitate phenotypic variation through genotype–environment interactions—are of great interest ecologically and evolutionarily. Our comprehensive review of marine environmental epigenetics guides our recommendations of four key areas for future research: the dynamics of wash-in and wash-out of epigenetic effects, the mechanistic understanding of the interplay of different epigenetic marks and the interaction with the microbiome, the capacity for and mechanisms of transgenerational epigenetic inheritance, and the evolutionary implications of the interaction of genetic and epigenetic features. Emerging insights in marine environmental epigenetics can be applied to critical issues such as aquaculture, biomonitoring, and biological invasions, thereby improving our ability to explain and predict the responses of marine taxa to global climate change.

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2019-01-03
2024-06-16
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Literature Cited

  1. Allis CD, Jenuwein T 2016. The molecular hallmarks of epigenetic control. Nat. Rev. Genet. 17:487–500
    [Google Scholar]
  2. Anastasiadi D, Díaz N, Piferrer F 2017. Small ocean temperature increases elicit stage-dependent changes in DNA methylation and gene expression in a fish, the European sea bass. Sci. Rep. 7:12401
    [Google Scholar]
  3. Andreassen R, Worren MM, Høyheim B 2013. Discovery and characterization of miRNA genes in Atlantic salmon (Salmo salar) by use of a deep sequencing approach. BMC Genom 14:482
    [Google Scholar]
  4. Araya I, Nardocci G, Morales J, Vera M, Molina A, Alvarez M 2010. MacroH2A subtypes contribute antagonistically to the transcriptional regulation of the ribosomal cistron during seasonal acclimatization of the carp fish. Epigenet. Chromatin 3:14
    [Google Scholar]
  5. Ardura A, Zaiko A, Morán P, Planes S, Garcia-Vazquez E 2017. Epigenetic signatures of invasive status in populations of marine invertebrates. Sci. Rep. 7:42193
    [Google Scholar]
  6. Arenas-Mena C, Wong KS-Y, Arandi-Foroshani NR 2007. Histone H2A.Z expression in two indirectly developing marine invertebrates correlates with undifferentiated and multipotent cells. Evol. Dev. 9:231–43
    [Google Scholar]
  7. Baccarelli A, Bollati V 2009. Epigenetics and environmental chemicals. Curr. Opin. Pediatr. 21:243–51
    [Google Scholar]
  8. Baerwald MR, Meek MH, Stephens MR, Nagarajan RP, Goodbla AM et al. 2016. Migration-related phenotypic divergence is associated with epigenetic modifications in rainbow trout. Mol. Ecol. 25:1785–800
    [Google Scholar]
  9. Bannister AJ, Kouzarides T 2011. Regulation of chromatin by histone modifications. Cell Res 21:381–95
    [Google Scholar]
  10. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE et al. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129:823–37
    [Google Scholar]
  11. Beal A, Rodriguez-Casariego J, Rivera-Casas C, Suarez-Ulloa V, Eirin-Lopez J 2018. Environmental epigenomics and its applications in marine organisms. Population Genomics: Marine Organisms M Oleksiak, OP Rajora Cham, Switz. Springer: In press
    [Google Scholar]
  12. Bizuayehu TT, Babiak I 2014. MicroRNA in teleost fish. Genome Biol. Evol. 6:1911–37
    [Google Scholar]
  13. Bizuayehu TT, Babiak J, Norberg B, Fernandes JMO, Johansen SD, Babiak I 2012.a Sex-biased miRNA expression in Atlantic halibut (Hippoglossus hippoglossus) brain and gonads. Sex Dev 6:257–66
    [Google Scholar]
  14. Bizuayehu TT, Johansen SD, Puvanendran V, Toften H, Babiak I 2015. Temperature during early development has long-term effects on microRNA expression in Atlantic cod. BMC Genom 16:305
    [Google Scholar]
  15. Bizuayehu TT, Lanes CFC, Furmanek T, Karlsen BO, Fernandes JMO et al. 2012.b Differential expression patterns of conserved miRNAs and isomiRs during Atlantic halibut development. BMC Genom 13:11
    [Google Scholar]
  16. Bollati V, Baccarelli A 2010. Environmental epigenetics. Heredity 105:105–12
    [Google Scholar]
  17. Boltaña S, Valenzuela-Miranda D, Aguilar A, Mackenzie S, Gallardo-Escárate C 2016. Long noncoding RNAs (lncRNAs) dynamics evidence immunomodulation during ISAV-Infected Atlantic salmon (Salmo salar). Sci. Rep. 6:22698
    [Google Scholar]
  18. Buenrostro JD, Wu B, Chang HY, Greenleaf WJ 2015. ATAC-seq: a method for assaying chromatin accessibility genome-wide. Curr. Protoc. Mol. Biol. 109:21.29.1–9
    [Google Scholar]
  19. Burgerhout E, Mommens M, Johnsen H, Aunsmo A, Santi N, Andersen Ø 2017. Genetic background and embryonic temperature affect DNA methylation and expression of myogenin and muscle development in Atlantic salmon (Salmo salar). PLOS ONE 12:e0179918
    [Google Scholar]
  20. Burggren WW 2015. Dynamics of epigenetic phenomena: intergenerational and intragenerational phenotype “washout. J. Exp. Biol. 218:80–87
    [Google Scholar]
  21. Carthew RW, Sontheimer EJ 2009. Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–55
    [Google Scholar]
  22. Castegna A, Iacobazzi V, Infantino V 2015. The mitochondrial side of epigenetics. Physiol. Genom. 47:299–307
    [Google Scholar]
  23. Cochrane DR, Cittelly DM, Richer JK 2011. Steroid receptors and microRNAs: relationships revealed. Steroids 76:1–10
    [Google Scholar]
  24. Consuegra S, Rodríguez López CM 2016. Epigenetic-induced alterations in sex-ratios in response to climate change: an epigenetic trap. BioEssays 38:950–58
    [Google Scholar]
  25. Covelo-Soto L, Leunda PM, Pérez-Figueroa A, Morán P 2015.a Genome-wide methylation study of diploid and triploid brown trout (Salmo trutta L.). Anim. Genet. 46:280–88
    [Google Scholar]
  26. Covelo-Soto L, Saura M, Morán P 2015.b Does DNA methylation regulate metamorphosis? The case of the sea lamprey (Petromyzon marinus) as an example. Comp. Biochem. Physiol. B 185:42–46
    [Google Scholar]
  27. Dabe EC, Sanford RS, Kohn AB, Bobkova Y, Moroz LL 2015. DNA methylation in basal metazoans: insights from ctenophores. Integr. Comp. Biol. 55:1096–110
    [Google Scholar]
  28. D'Aquila P, Montesanto A, Guarasci F, Passarino G, Bellizzi D 2017. Mitochondrial genome and epigenome: two sides of the same coin. Front. Biosci. 22:888–908
    [Google Scholar]
  29. Day T, Bonduriansky R 2011. A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am. Nat. 178:E18–36
    [Google Scholar]
  30. Deans C, Maggert KA 2015. What do you mean, “epigenetic”. Genetics 199:887–96
    [Google Scholar]
  31. Dekker J 2006. The three ‘C’ s of chromosome conformation capture: controls, controls, controls. Nat. Methods 3:17–21
    [Google Scholar]
  32. Di Liegro CM, Schiera G, Di Liegro I 2017. Extracellular vesicle-associated RNA as a carrier of epigenetic information. Genes 8:E240
    [Google Scholar]
  33. Díaz-Freije E, Gestal C, Castellanos-Martínez S, Morán P 2014. The role of DNA methylation on Octopus vulgaris development and their perspectives. Front. Physiol. 5:62
    [Google Scholar]
  34. Dimond JL, Gamblewood SK, Roberts SB 2017. Genetic and epigenetic insight into morphospecies in a reef coral. Mol. Ecol. 26:5031–42
    [Google Scholar]
  35. Dimond JL, Roberts SB 2016. Germline DNA methylation in reef corals: patterns and potential roles in response to environmental change. Mol. Ecol. 25:1895–904
    [Google Scholar]
  36. Dixon GB, Bay LK, Matz MV 2010. Bimodal signatures of germline methylation are linked with gene expression plasticity in the coral Acropora millepora. BMC Genom 15:1109
    [Google Scholar]
  37. Dixon GB, Bay LK, Matz MV 2016. Evolutionary consequences of DNA methylation in a basal metazoan. Mol. Biol. Evol. 33:2285–93
    [Google Scholar]
  38. Dixon GB, Bay LK, Matz MV 2017. Patterns of gene body methylation predict coral fitness in new environments. bioRxiv 184457. https://doi.org/10.1101/184457
    [Crossref]
  39. Donelson JM, Salinas S, Munday PL, Shama LNS 2018. Transgenerational plasticity and climate change experiments: Where do we go from here. Glob. Change Biol. 24:13–34
    [Google Scholar]
  40. Donohoe DR, Bultman SJ 2012. Metaboloepigenetics: interrelationships between energy metabolism and epigenetic control of gene expression. J. Cell. Physiol. 227:3169–77
    [Google Scholar]
  41. Doskočil J, Šorm F 1962. Distribution of 5-methylcytosine in pyrimidine sequences of deoxyribonucleic acids. Biochim. Biophys. Acta 55:953–59
    [Google Scholar]
  42. Eirin-Lopez JM, Ausió J 2009. Origin and evolution of chromosomal sperm proteins. BioEssays 31:1062–70
    [Google Scholar]
  43. Eirin-Lopez JM, González-Romero R, Dryhurst D, Méndez J, Ausió J 2009. Long-term evolution of histone families: old notions and new insights into their mechanisms of diversification across eukaryotes. Evolutionary Biology P Pontarotti 139–62 Berlin: Springer
    [Google Scholar]
  44. Ellison A, Rodríguez López CM, Moran P, Breen J, Swain M et al. 2015. Epigenetic regulation of sex ratios may explain natural variation in self-fertilization rates. Proc. R. Soc. B 282:20151900
    [Google Scholar]
  45. Erdel F 2017. How communication between nucleosomes enables spreading and epigenetic memory of histone modifications. BioEssays 39:1700053
    [Google Scholar]
  46. Esteller M, Pandolfi PP 2017. The epitranscriptome of noncoding RNAs in cancer. Cancer Discov 7:359–68
    [Google Scholar]
  47. Etchegaray J-P, Mostoslavsky R 2016. Interplay between metabolism and epigenetics: a nuclear adaptation to environmental changes. Mol. Cell 62:695–711
    [Google Scholar]
  48. Feil R, Fraga MF 2012. Epigenetics and the environment: emerging patterns and implications. Nat. Rev. Genet. 13:97–109
    [Google Scholar]
  49. Fellous A, Favrel P, Riviere G 2015. Temperature influences histone methylation and mRNA expression of the Jmj-C histone-demethylase orthologues during the early development of the oyster Crassostrea gigas. Mar. Genom. 19:23–30
    [Google Scholar]
  50. Feng S, Cokus SJ, Zhang X, Chen P-Y, Bostick M et al. 2010. Conservation and divergence of methylation patterning in plants and animals. PNAS 107:8689–94
    [Google Scholar]
  51. Flusberg BA, Webster DR, Lee JH, Travers KJ, Olivares EC et al. 2010. Direct detection of DNA methylation during single-molecule, real-time sequencing. Nat. Methods 7:461–65
    [Google Scholar]
  52. Ford EE, Grimmer MR, Stolzenburg S, Bogdanovic O, de Mendoza A et al. 2017. Frequent lack of repressive capacity of promoter DNA methylation identified through genome-wide epigenomic manipulation. bioRxiv 170506. https://doi.org/10.1101/170506
    [Crossref]
  53. Gallardo-Escárate C, Valenzuela-Muñoz V, Boltaña S, Nuñez-Acuña G, Valenzuela-Miranda D et al. 2017. The Caligus rogercresseyi miRNome: discovery and transcriptome profiling during the sea lice ontogeny. Agri Gene 4:8–22
    [Google Scholar]
  54. García-Fernández P, García-Souto D, Almansa E, Morán P, Gestal C 2017. Epigenetic DNA methylation mediating Octopus vulgaris early development: effect of essential fatty acids enriched diet. Front. Physiol. 8:292
    [Google Scholar]
  55. García-Giménez JL, Seco-Cervera M, Tollefsbol TO, Romá-Mateo C, Peiró-Chova L et al. 2017. Epigenetic biomarkers: current strategies and future challenges for their use in the clinical laboratory. Crit. Rev. Clin. Lab. Sci. 54:529–50
    [Google Scholar]
  56. Gardiner-Garden M, Frommer M 1987. CpG islands in vertebrate genomes. J. Mol. Biol. 196:261–82
    [Google Scholar]
  57. Gavery MR, Roberts SB 2010. DNA methylation patterns provide insight into epigenetic regulation in the Pacific oyster (Crassostrea gigas). BMC Genom 11:483
    [Google Scholar]
  58. Gavery MR, Roberts SB 2013. Predominant intragenic methylation is associated with gene expression characteristics in a bivalve mollusc. PeerJ 1:e215
    [Google Scholar]
  59. Gavery MR, Roberts SB 2014. A context dependent role for DNA methylation in bivalves. Brief. Funct. Genom. 13:217–22
    [Google Scholar]
  60. Gavery MR, Roberts SB 2017. Epigenetic considerations in aquaculture. PeerJ 5:e4147
    [Google Scholar]
  61. Geay F, Zambonino-Infante J, Reinhardt R, Kuhl H, Santigosa E et al. 2012. Characteristics of fads2 gene expression and putative promoter in European sea bass (Dicentrarchus labrax): comparison with salmonid species and analysis of CpG methylation. Mar. Genom. 5:7–13
    [Google Scholar]
  62. Gertz J, Varley KE, Reddy TE, Bowling KM, Pauli F et al. 2011. Analysis of DNA methylation in a three-generation family reveals widespread genetic influence on epigenetic regulation. PLOS Genet 7:e1002228
    [Google Scholar]
  63. Geurden I, Borchert P, Balasubramanian MN, Schrama JW, Dupont-Nivet M et al. 2013. The positive impact of the early-feeding of a plant-based diet on its future acceptance and utilisation in rainbow trout. PLOS ONE 8:e83162
    [Google Scholar]
  64. Ghosh S, Sengupta S, Scaria V 2014. Comparative analysis of human mitochondrial methylomes shows distinct patterns of epigenetic regulation in mitochondria. Mitochondrion 18:58–62
    [Google Scholar]
  65. Gibbin EM, Chakravarti LJ, Jarrold MD, Christen F, Turpin V et al. 2017. Can multi-generational exposure to ocean warming and acidification lead to the adaptation of life history and physiology in a marine metazoan. J. Exp. Biol. 220:551–63
    [Google Scholar]
  66. Gibson G, Hart C, Pierce R, Lloyd V 2012. Ontogenetic survey of histone modifications in an annelid. Genet. Res. Int. 2012:392903
    [Google Scholar]
  67. González-Romero R, Rivera-Casas C, Frehlick LJ, Méndez J, Ausió J, Eirin-Lopez JM 2012. Histone H2A (H2A.X and H2A.Z) variants in molluscs: molecular characterization and potential implications for chromatin dynamics. PLOS ONE 7:e30006
    [Google Scholar]
  68. González-Romero R, Suarez-Ulloa V, Rodriguez-Casariego J, Garcia-Souto D, Diaz G et al. 2017. Effects of Florida Red Tides on histone variant expression and DNA methylation in the Eastern oyster Crassostrea virginica. Aquat. Toxicol 186:196–204
    [Google Scholar]
  69. Gu H, Smith ZD, Bock C, Boyle P, Gnirke A, Meissner A 2011. Preparation of reduced representation bisulfite sequencing libraries for genome-scale DNA methylation profiling. Nat. Protoc. 6:468–81
    [Google Scholar]
  70. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR 2009. Distinctive chromatin in human sperm packages genes for embryo development. Nature 460:473–78
    [Google Scholar]
  71. Harris RA, Wang T, Coarfa C, Nagarajan RP, Hong C et al. 2010. Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nat. Biotechnol. 28:1097–105
    [Google Scholar]
  72. Hawes NA, Fidler AE, Tremblay LA, Pochon X, Dunphy BJ, Smith KF 2018. Understanding the role of DNA methylation in successful biological invasions: a review. Biol. Invasions 20:2285–300
    [Google Scholar]
  73. Helm M, Motorin Y 2017. Detecting RNA modifications in the epitranscriptome: predict and validate. Nat. Rev. Genet. 18:275–91
    [Google Scholar]
  74. Herman JG, Graff JR, Myöhänen S, Nelkin BD, Baylin SB 1996. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. PNAS 93:9821–26
    [Google Scholar]
  75. Hochachka PW, Somero GN 2002. Biochemical Adaptation, Mechanism and Process in Physiological Evolution New York: Oxford Univ. Press
    [Google Scholar]
  76. Hoegh-Guldberg O, Bruno JF 2010. The impact of climate change on the world's marine ecosystems. Science 328:1523–28
    [Google Scholar]
  77. Hofmann GE 2017. Ecological epigenetics in marine metazoans. Front. Mar. Sci. 4:4
    [Google Scholar]
  78. Holoch D, Moazed D 2015. RNA-mediated epigenetic regulation of gene expression. Nat. Rev. Genet. 16:71–84
    [Google Scholar]
  79. Huang X, Li S, Ni P, Gao Y, Jiang B et al. 2017. Rapid response to changing environments during biological invasions: DNA methylation perspectives. Mol. Ecol. 26:6621–33
    [Google Scholar]
  80. IPCC (Intergov. Panel Clim. Change). 2014. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change Core Writ. Team, RK Pachauri, LA Meyer Geneva, Switz.: IPCC
    [Google Scholar]
  81. Ito S, Shen L, Dai Q, Wu SC, Collins LB et al. 2011. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333:1300–3
    [Google Scholar]
  82. Iwasaki YW, Siomi MC, Siomi H 2015. PIWI-interacting RNA: its biogenesis and functions. Annu. Rev. Biochem. 84:405–33
    [Google Scholar]
  83. Jablonka E, Lamb MJ 2002. The changing concept of epigenetics. Ann. N.Y. Acad. Sci. 981:82–96
    [Google Scholar]
  84. Jablonka E, Raz G 2009. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q. Rev. Biol. 84:131–76
    [Google Scholar]
  85. Jacinto FV, Ballestar E, Esteller M 2008. Methyl-DNA immunoprecipitation (MeDIP): hunting down the DNA methylome. Biotechniques 44:35, 37, 39 passim
    [Google Scholar]
  86. Jeltsch A 2002. Beyond Watson and Crick: DNA methylation and molecular enzymology of DNA methyltransferases. ChemBioChem 3:274–93
    [Google Scholar]
  87. Jeltsch A, Jurkowska RZ 2014. New concepts in DNA methylation. Trends Biochem. Sci. 39:310–18
    [Google Scholar]
  88. Jensen N, Allen RM, Marshall DJ 2013. Adaptive maternal and paternal effects: gamete plasticity in response to parental stress. Funct. Ecol. 28:724–33
    [Google Scholar]
  89. Jiang Q, Li Q, Yu H, Kong L-F 2013. Genetic and epigenetic variation in mass selection populations of Pacific oyster Crassostrea gigas. Genes Genom. 35:641–47
    [Google Scholar]
  90. Jiang Q, Li Q, Yu H, Kong L-F 2016. Inheritance and variation of genomic DNA methylation in diploid and triploid Pacific Oyster (Crassostrea gigas). Mar. Biotechnol. 18:124–32
    [Google Scholar]
  91. Karch KR, Denizio JE, Black BE, Garcia BA 2013. Identification and interrogation of combinatorial histone modifications. Front. Genet. 4:264
    [Google Scholar]
  92. Kashi K, Henderson L, Bonetti A, Carninci P 2016. Discovery and functional analysis of lncRNAs: methodologies to investigate an uncharacterized transcriptome. Biochim. Biophys. Acta 1859:3–15
    [Google Scholar]
  93. Kimmins S, Sassone-Corsi P 2005. Chromatin remodelling and epigenetic features of germ cells. Nature 434:583–89
    [Google Scholar]
  94. Kota SK, Feil R 2010. Epigenetic transitions in germ cell development and meiosis. Dev. Cell. 19:675–86
    [Google Scholar]
  95. Kronholm I, Bassett A, Baulcombe D, Collins S 2017. Epigenetic and genetic contributions to adaptation in Chlamydomonas. Mol. Biol. Evol. 34:2285–306
    [Google Scholar]
  96. Kronholm I, Collins S 2016. Epigenetic mutations can both help and hinder adaptive evolution. Mol. Ecol. 25:1856–68
    [Google Scholar]
  97. Kuc C, Richard DJ, Johnson S, Bragg L, Servos MR et al. 2017. Rainbow trout exposed to benzo[a]pyrene yields conserved microRNA binding sites in DNA methyltransferases across 500 million years of evolution. Sci. Rep. 7:16843
    [Google Scholar]
  98. Kuo KC, McCune RA, Gehrke CW, Midgett R, Ehrlich M 1980. Quantitative reversed-phase high performance liquid chromatographic determination of major and modified deoxyribonucleosides in DNA. Nucleic Acids Res 8:4763–76
    [Google Scholar]
  99. Kurdyukov S, Bullock M 2016. DNA methylation analysis: choosing the right method. Biology 5:E3
    [Google Scholar]
  100. Laird PW 2010. Principles and challenges of genomewide DNA methylation analysis. Nat. Rev. Genet. 11:191–203
    [Google Scholar]
  101. Lau K, Lai KP, Bao JYJ, Zhang N, Tse A et al. 2014. Identification and expression profiling of microRNAs in the brain, liver and gonads of marine medaka (Oryzias melastigma) and in response to hypoxia. PLOS ONE 9:e110698
    [Google Scholar]
  102. Le Luyer J, Laporte M, Beacham TD, Kaukinen KH, Withler RE et al. 2017. Parallel epigenetic modifications induced by hatchery rearing in a Pacific salmon. PNAS 114:12964–69
    [Google Scholar]
  103. Lee TM, Zucker I 1988. Vole infant development is influenced perinatally by maternal photoperiodic history. Am. J. Physiol. 255:R831–38
    [Google Scholar]
  104. Li M, Leatherland JF 2012. The implications for aquaculture practice of epigenomic programming of components of the endocrine system of teleostean embryos: lessons learned from mammalian studies. Fish Fish 14:528–53
    [Google Scholar]
  105. Li S, He F, Wen H, Li J, Si Y et al. 2017.a Low salinity affects cellularity, DNA methylation, and mRNA expression of igf1 in the liver of half smooth tongue sole (Cynoglossus semilaevis). Fish Physiol. Biochem. 43:1587–602
    [Google Scholar]
  106. Li S, Wen H, Li J, Si Y, Liu M et al. 2017.b Analysis of DNA methylation level by methylation-sensitive amplification polymorphism in half smooth tongue sole (Cynoglossus semilaevis) subjected to salinity stress. J. Ocean Univ. China 16:269–78
    [Google Scholar]
  107. Li X, Xiong X, Yi C 2016. Epitranscriptome sequencing technologies: decoding RNA modifications. Nat. Methods 14:23–31
    [Google Scholar]
  108. Li Y, Liew YJ, Cui G, Cziesielski MJ, Zahran N et al. 2018. DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia. bioRxiv 213066. https://doi.org/10.1101/213066
    [Crossref]
  109. Liew YJ, Howells EJ, Wang X, Michell CT, Burt JA et al. 2018.a Intergenerational epigenetic inheritance in reef-building corals. bioRxiv 269076. https://doi.org/10.1101/269076
    [Crossref]
  110. Liew YJ, Zoccola D, Li Y, Tambutté E, Venn AA et al. 2018.b Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral. Sci. Adv. 4:eaar8028
    [Google Scholar]
  111. Lin X, Tirichine L, Bowler C 2012. Protocol: chromatin immunoprecipitation (ChIP) methodology to investigate histone modifications in two model diatom species. Plant Methods 8:48
    [Google Scholar]
  112. Lorincz AT 2011. The promise and the problems of epigenetic biomarkers in cancer. Expert Opin. Med. Diagn. 5:375–79
    [Google Scholar]
  113. Lotze HK, Lenihan HS, Bourque BJ, Bradbury RH, Cooke RG et al. 2006. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312:1806–9
    [Google Scholar]
  114. Ma H, Hostuttler M, Wei H, Rexroad CE III, Yao J 2012. Characterization of the rainbow trout egg microRNA transcriptome. PLOS ONE 7:e39649
    [Google Scholar]
  115. Manev H, Dzitoyeva S 2013. Progress in mitochondrial epigenetics. Biomol. Concepts 4:381–89
    [Google Scholar]
  116. Maresca A, Zaffagnini M, Caporali L, Carelli V, Zanna C 2015. DNA methyltransferase 1 mutations and mitochondrial pathology: Is mtDNA methylated. Front. Genet. 6:90
    [Google Scholar]
  117. Marsh AG, Pasqualone AA 2014. DNA methylation and temperature stress in an Antarctic polychaete, Spiophanes tcherniai. Front. Physiol. 5:173
    [Google Scholar]
  118. Marshall DJ 2008. Transgenerational plasticity in the sea: context-dependent maternal effects across the life history. Ecology 89:418–27
    [Google Scholar]
  119. McVicker G, van de Geijn B, Degner JF, Cain CE, Banovich NE et al. 2013. Identification of genetic variants that affect histone modifications in human cells. Science 342:747–49
    [Google Scholar]
  120. Mechta M, Ingerslev LR, Fabre O, Picard M, Barrès R 2017. Evidence suggesting absence of mitochondrial DNA methylation. Front. Genet. 8:166
    [Google Scholar]
  121. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J et al. 2008. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454:766–70
    [Google Scholar]
  122. Mennigen JA, Skiba-Cassy S, Panserat S 2013. Ontogenetic expression of metabolic genes and microRNAs in rainbow trout alevins during the transition from the endogenous to the exogenous feeding period. J. Exp. Biol. 216:1597–608
    [Google Scholar]
  123. Metzger DCH, Schulte PM 2016. Epigenomics in marine fishes. Mar. Genom. 30:43–54
    [Google Scholar]
  124. Metzger DCH, Schulte PM 2017. Persistent and plastic effects of temperature on DNA methylation across the genome of threespine stickleback (Gasterosteus aculeatus). Proc. R. Soc. B 284:20171667
    [Google Scholar]
  125. Metzger DCH, Schulte PM 2018. The DNA methylation landscape of stickleback reveals patterns of sex chromosome evolution and effects of environmental salinity. Genome Biol. Evol. 10:775–85
    [Google Scholar]
  126. Mirbahai L, Chipman JK 2014. Epigenetic memory of environmental organisms: a reflection of lifetime stressor exposures. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 764–65:10–17
    [Google Scholar]
  127. Mirbahai L, Southam AD, Sommer U, Williams TD, Bignell JP et al. 2013. Disruption of DNA methylation via S-adenosylhomocysteine is a key process in high incidence liver carcinogenesis in fish. J. Proteome Res. 12:2895–904
    [Google Scholar]
  128. Mirbahai L, Yin G, Bignell JP, Li N, Williams TD, Chipman JK 2011. DNA methylation in liver tumorigenesis in fish from the environment. Epigenetics 6:1319–33
    [Google Scholar]
  129. Mischke M, Plösch T 2013. More than just a gut instinct—the potential interplay between a baby's nutrition, its gut microbiome, and the epigenome. Am. J. Physiol. Regul. Integr. Comp. Physiol. 304:R1065–69
    [Google Scholar]
  130. Moosmann A, Campsteijn C, Jansen PW, Nasrallah C, Raasholm M et al. 2011. Histone variant innovation in a rapidly evolving chordate lineage. BMC Evol. Biol. 11:208
    [Google Scholar]
  131. Morán P, Pérez-Figueroa A 2011. Methylation changes associated with early maturation stages in the Atlantic salmon. BMC Genet 12:86
    [Google Scholar]
  132. Moran Y, Praher D, Fredman D, Technau U 2013. The evolution of microRNA pathway protein components in Cnidaria. Mol. Biol. Evol. 30:2541–52
    [Google Scholar]
  133. Morley SA, Nguyen KD, Peck LS, Lai C-H, Tan KS 2017. Can acclimation of thermal tolerance, in adults and across generations, act as a buffer against climate change in tropical marine ectotherms. J. Therm. Biol. 68:195–99
    [Google Scholar]
  134. Navarro-Martín L, Viñas J, Ribas L, Díaz N, Gutiérrez A et al. 2011. DNA methylation of the gonadal aromatase (cyp19a) promoter is involved in temperature-dependent sex ratio shifts in the European sea bass. PLOS Genet 7:e1002447
    [Google Scholar]
  135. O'Geen H, Echipare L, Farnham PJ 2011. Using ChIP-seq technology to generate high-resolution profiles of histone modifications. Methods Mol. Biol. 791:265–86
    [Google Scholar]
  136. Olova N, Krueger F, Andrews S, Oxley D, Berrens RV et al. 2018. Comparison of whole-genome bisulfite sequencing library preparation strategies identifies sources of biases affecting DNA methylation data. Genome Biol 19:33
    [Google Scholar]
  137. Olson CE, Roberts SB 2014. Genome-wide profiling of DNA methylation and gene expression in Crassostrea gigas male gametes. Front. Physiol. 5:224
    [Google Scholar]
  138. Ozsolak F, Milos PM 2011. RNA sequencing: advances, challenges and opportunities. Nat. Rev. Genet. 12:87–98
    [Google Scholar]
  139. Paneru B, Al-Tobasei R, Palti Y, Wiens GD, Salem M 2016. Differential expression of long non-coding RNAs in three genetic lines of rainbow trout in response to infection with Flavobacterium psychrophilum. Sci. Rep. 6:36032
    [Google Scholar]
  140. Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP 2010. Phenotypic plasticity's impacts on diversification and speciation. Trends Ecol. Evol. 25:459–67
    [Google Scholar]
  141. Pierron F, Baillon L, Sow M, Gotreau S, Gonzalez P 2014. Effect of low-dose cadmium exposure on DNA methylation in the endangered European eel. Environ. Sci. Technol. 48:797–803
    [Google Scholar]
  142. Polanowski AM, Robbins J, Chandler D, Jarman SN 2014. Epigenetic estimation of age in humpback whales. Mol. Ecol. Resour. 14:976–87
    [Google Scholar]
  143. Putnam HM, Davidson JM, Gates RD 2016. Ocean acidification influences host DNA methylation and phenotypic plasticity in environmentally susceptible corals. Evol. Appl. 9:1165–78
    [Google Scholar]
  144. Putnam HM, Gates RD 2015. Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions. J. Exp. Biol. 218:2365–72
    [Google Scholar]
  145. Putnam HM, Ritson-Williams R, Cruz JA, Davidson JM, Gates RD 2018. Nurtured by nature: considering the role of environmental and parental legacies in coral ecological performance. bioRxiv 317453. https://doi.org/10.1101/317453
    [Crossref]
  146. Putnam HM, Roberts S, Spencer LH 2017. Capacity for adaptation and acclimatization to ocean acidification in geoduck through epigenetic mechanisms. Poster, Figshare. https://doi.org/10.6084/m9.figshare.4990889.v1
    [Crossref]
  147. Reddy PC, Ubhe S, Sirwani N, Lohokare R, Galande S 2017. Rapid divergence of histones in Hydrozoa (Cnidaria) and evolution of a novel histone involved in DNA damage response in hydra. Zoology 123:53–63
    [Google Scholar]
  148. Resch AM, Palakodeti D 2012. Small RNA pathways in Schmidtea mediterranea. Int. J. Dev. Biol. 56:67–74
    [Google Scholar]
  149. Rey O, Danchin E, Mirouze M, Loot C, Blanchet S 2016. Adaptation to global change: a transposable element-epigenetics perspective. Trends Ecol. Evol. 31:514–26
    [Google Scholar]
  150. Richards CL, Alonso C, Becker C, Bossdorf O, Bucher E et al. 2017. Ecological plant epigenetics: evidence from model and non-model species, and the way forward. Ecol. Lett. 20:1576–90
    [Google Scholar]
  151. Rivera-Casas C, González-Romero R, Cheema MS, Ausió J, Eirin-Lopez JM 2016. The characterization of macroH2A beyond vertebrates supports an ancestral origin and conserved role for histone variants in chromatin. Epigenetics 11:415–25
    [Google Scholar]
  152. Rivera-Casas C, González-Romero R, Garduño RA, Cheema MS, Ausio J, Eirin-Lopez JM 2017. Molecular and biochemical methods useful for the epigenetic characterization of chromatin-associated proteins in bivalve molluscs. Front. Physiol. 8:490
    [Google Scholar]
  153. Riviere G, He Y, Tecchio S, Crowell E, Gras M et al. 2017. Dynamics of DNA methylomes underlie oyster development. PLOS Genet 13:e1006807
    [Google Scholar]
  154. Riviere G, Wu G-C, Fellous A, Goux D, Sourdaine P, Favrel P 2013. DNA methylation is crucial for the early development in the oyster C. gigas. Mar. Biotechnol 15:739–53
    [Google Scholar]
  155. Roberts SB, Gavery MR 2012. Is there a relationship between DNA methylation and phenotypic plasticity in invertebrates. Front. Physiol. 2:116
    [Google Scholar]
  156. Robledo D, Martin AP, Álvarez-Dios JA, Bouza C, Pardo BG, Martínez P 2017. First characterization and validation of turbot microRNAs. Aquaculture 472:76–83
    [Google Scholar]
  157. Rodriguez-Casariego J, Ladd M, Shantz A, Lopes C, Cheema M et al. 2018. Epigenetic modifications in the staghorn coral Acropora cervicornis during exposure to nutrient stress: impaired histone H2A.X phosphorylation and changes in DNA methylation trends. Mol. Ecol. In review
    [Google Scholar]
  158. Rondon R, Grunau C, Fallet M, Charlemagne N, Sussarellu R et al. 2017. Effects of a parental exposure to diuron on Pacific oyster spat methylome. Environ. Epigenet. 3:dvx004
    [Google Scholar]
  159. Rosani U, Pallavicini A, Venier P 2016. The miRNA biogenesis in marine bivalves. PeerJ 4:e1763
    [Google Scholar]
  160. Ross PM, Parker L, Byrne M 2016. Transgenerational responses of molluscs and echinoderms to changing ocean conditions. ICES J. Mar. Sci. 73:537–49
    [Google Scholar]
  161. Ryu T, Veilleux HD, Donelson JM, Munday PL, Ravasi T 2018. The epigenetic landscape of transgenerational acclimation to ocean warming. Nat. Clim. Change 8:504–9
    [Google Scholar]
  162. Saint-Carlier E, Riviere G 2015. Regulation of Hox orthologues in the oyster Crassostrea gigas evidences a functional role for promoter DNA methylation in an invertebrate. FEBS Lett 589:1459–66
    [Google Scholar]
  163. Salinas S, Munch SB 2012. Thermal legacies: transgenerational effects of temperature on growth in a vertebrate. Ecol. Lett. 15:159–63
    [Google Scholar]
  164. Schield DR, Walsh MR, Card DC, Andrew AL, Adams RH, Castoe TA 2016. EpiRADseq: scalable analysis of genomewide patterns of methylation using next-generation sequencing. Methods Ecol. Evol. 7:60–69
    [Google Scholar]
  165. Schlichting CD, Wund MA 2014. Phenotypic plasticity and epigenetic marking: an assessment of evidence for genetic accommodation. Evolution 68:656–72
    [Google Scholar]
  166. Serre D, Lee BH, Ting AH 2010. MBD-isolated genome sequencing provides a high-throughput and comprehensive survey of DNA methylation in the human genome. Nucleic Acids Res 38:391–99
    [Google Scholar]
  167. Shao C, Li Q, Chen S, Zhang P, Lian J et al. 2014. Epigenetic modification and inheritance in sexual reversal of fish. Genome Res 24:604–15
    [Google Scholar]
  168. Simonet NG, Reyes M, Nardocci G, Molina A, Alvarez M 2013. Epigenetic regulation of the ribosomal cistron seasonally modulates enrichment of H2A.Z and H2A.Zub in response to different environmental inputs in carp (Cyprinus carpio). Epigenet. Chromatin 6:22
    [Google Scholar]
  169. Sogin EM, Putnam HM, Nelson CE, Anderson P, Gates RD 2017. Correspondence of coral holobiont metabolome with symbiotic bacteria, archaea and Symbiodinium communities. Environ. Microbiol. Rep. 9:310–15
    [Google Scholar]
  170. Song K, Li L, Zhang G 2017. The association between DNA methylation and exon expression in the Pacific oyster Crassostrea gigas. PLOS ONE 12:e0185224
    [Google Scholar]
  171. Song L, James SR, Kazim L, Karpf AR 2005. Specific method for the determination of genomic DNA methylation by liquid chromatography-electrospray ionization tandem mass spectrometry. Anal. Chem. 77:504–10
    [Google Scholar]
  172. Strahl BD, Allis CD 2000. The language of covalent histone modifications. Nature 403:41–45
    [Google Scholar]
  173. Suarez-Ulloa V, González-Romero R, Eirin-Lopez JM 2015. Environmental epigenetics: a promising venue for developing next-generation pollution biomonitoring tools in marine invertebrates. Mar. Pollut. Bull. 98:5–13
    [Google Scholar]
  174. Suzuki MM, Bird A 2008. DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 9:465–76
    [Google Scholar]
  175. Talbert PB, Ahmad K, Almouzni G, Ausió J, Berger F et al. 2012. A unified phylogeny-based nomenclature for histone variants. Epigenet. Chromatin 5:7
    [Google Scholar]
  176. Talbert PB, Henikoff S 2014. Environmental responses mediated by histone variants. Trends Cell Biol 24:642–50
    [Google Scholar]
  177. Taudt A, Colomé-Tatché M, Johannes F 2016. Genetic sources of population epigenomic variation. Nat. Rev. Genet. 17:319–32
    [Google Scholar]
  178. Terova G, Díaz N, Rimoldi S, Ceccotti C, Gliozheni E, Piferrer F 2016. Effects of sodium butyrate treatment on histone modifications and the expression of genes related to epigenetic regulatory mechanisms and immune response in European sea bass (Dicentrarchus labrax) fed a plant-based diet. PLOS ONE 11:e0160332
    [Google Scholar]
  179. Torda G, Donelson JM, Aranda M, Barshis DJ, Bay L et al. 2017. Rapid adaptive responses to climate change in corals. Nat. Clim. Change 7:627–36
    [Google Scholar]
  180. Trautner JH, Reiser S, Blancke T, Unger K, Wysujack K 2017. Metamorphosis and transition between developmental stages in European eel (Anguilla anguilla, L.) involve epigenetic changes in DNA methylation patterns. Comp. Biochem. Physiol. D 22:139–45
    [Google Scholar]
  181. Trucchi E, Mazzarella AB, Gilfillan GD, Lorenzo MT, Schönswetter P, Paun O 2016. BsRADseq: screening DNA methylation in natural populations of non-model species. Mol. Ecol. 25:1697–713
    [Google Scholar]
  182. Turner BM 2007. Defining an epigenetic code. Nat. Cell Biol. 9:2–6
    [Google Scholar]
  183. Ulitsky I, Bartel DP 2013. lincRNAs: genomics, evolution, and mechanisms. Cell 154:26–46
    [Google Scholar]
  184. van Holde KE 1989. Chromatin New York: Springer
    [Google Scholar]
  185. van Oppen MJH, Oliver JK, Putnam HM, Gates RD 2015. Building coral reef resilience through assisted evolution. PNAS 112:2307–13
    [Google Scholar]
  186. Varriale A, Bernardi G 2006. DNA methylation and body temperature in fishes. Gene 385:111–21
    [Google Scholar]
  187. Veluchamy A, Rastogi A, Lin X, Lombard B, Murik O et al. 2015. An integrative analysis of post-translational histone modifications in the marine diatom Phaeodactylum tricornutum. Genome Biol 16:102
    [Google Scholar]
  188. Venegas D, Marmolejo-Valencia A, Valdes-Quezada C, Govenzensky T, Recillas-Targa F, Merchant-Larios H 2016. Dimorphic DNA methylation during temperature-dependent sex determination in the sea turtle Lepidochelys olivacea. Gen. Comp. Endocrinol 236:35–41
    [Google Scholar]
  189. Vogt G 2017. Facilitation of environmental adaptation and evolution by epigenetic phenotype variation: insights from clonal, invasive, polyploid, and domesticated animals. Environ Epigenet 3:dvx002
    [Google Scholar]
  190. Wang X, Li Q, Lian J, Li L, Jin L et al. 2014. Genome-wide and single-base resolution DNA methylomes of the Pacific oyster Crassostrea gigas provide insight into the evolution of invertebrate CpG methylation. BMC Genom 15:1119
    [Google Scholar]
  191. Watson RGA, Baldanzi S, Pérez-Figueroa A, Gouws G, Porri F 2018. Morphological and epigenetic variation in mussels from contrasting environments. Mar. Biol. 165:50
    [Google Scholar]
  192. Webster NS, Reusch TBH 2017. Microbial contributions to the persistence of coral reefs. ISME J 11:2167–74
    [Google Scholar]
  193. Wheeler HL, Johnson TB 1904. Researches on pyrimidine derivatives: 5-methylcytosine. Am. Chem. J. 31:591–606
    [Google Scholar]
  194. Yaish MW, Peng M, Rothstein SJ 2014. Global DNA methylation analysis using methyl-sensitive amplification polymorphism (MSAP). Methods Mol. Biol. 1062:285–98
    [Google Scholar]
  195. Yu D-H, Gadkari M, Zhou Q, Yu S, Gao N et al. 2015. Postnatal epigenetic regulation of intestinal stem cells requires DNA methylation and is guided by the microbiome. Genome Biol 16:211
    [Google Scholar]
  196. Yu H, Zhao X, Li Q 2016. Genome-wide identification and characterization of long intergenic noncoding RNAs and their potential association with larval development in the Pacific oyster. Sci. Rep. 6:20796
    [Google Scholar]
  197. Zhang J, Li S, Li L, Li M, Guo C et al. 2015. Exosome and exosomal microRNA: trafficking, sorting, and function. Genom. Proteom. Bioinform. 13:17–24
    [Google Scholar]
  198. Zhao JL, Si YF, He F, Wen HS, Li JF et al. 2015. Polymorphisms and DNA methylation level in the CpG site of the GHR1 gene associated with mRNA expression, growth traits and hormone level of half-smooth tongue sole (Cynoglossus semilaevis). Fish Physiol. Biochem. 41:853–65
    [Google Scholar]
  199. Zhao X, Yu H, Kong L, Liu S, Li Q 2016. High throughput sequencing of small RNAs transcriptomes in two Crassostrea oysters identifies microRNAs involved in osmotic stress response. Sci. Rep. 6:22687
    [Google Scholar]
  200. Zhao Y, Chen M, Storey KB, Sun L, Yang H 2015. DNA methylation levels analysis in four tissues of sea cucumber Apostichopus japonicus based on fluorescence-labeled methylation-sensitive amplified polymorphism (F-MSAP) during aestivation. Comp. Biochem. Physiol. B 181:26–32
    [Google Scholar]
  201. Zou H, Lan Z, Zhou M, Lu W 2018. Promoter methylation and Hoxd4 regulate UII mRNA tissue-specific expression in olive flounder (Paralichthys olivaceus). Gen. Comp. Endocrinol. 262:36–43
    [Google Scholar]
  202. Zuo Z, Cai J, Wang X, Li B, Wang C, Chen Y 2009. Acute administration of tributyltin and trimethyltin modulate glutamate and N-methyl-d-aspartate receptor signaling pathway in Sebastiscus marmoratus. Aquat. Toxicol 92:44–49
    [Google Scholar]
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