1932

Abstract

Experimental evolution and the associated theory are underutilized in marine microbial studies; the two fields have developed largely in isolation. Here, we review evolutionary tools for addressing four key areas of ocean global change biology: linking plastic and evolutionary trait changes, the contribution of environmental variability to determining trait values, the role of multiple environmental drivers in trait change, and the fate of populations near their tolerance limits. Wherever possible, we highlight which data from marine studies could use evolutionary approaches and where marine model systems can advance our understanding of evolution. Finally, we discuss the emerging field of marine microbial experimental evolution. We propose a framework linking changes in environmental quality (defined as the cumulative effect on population growth rate) with population traits affecting evolutionary potential, in order to understand which evolutionary processes are likely to be most important across a range of locations for different types of marine microbes.

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2020-01-03
2024-12-04
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Literature Cited

  1. Ajani PA, Larsson ME, Woodcock S, Rubio A, Farrell H et al. 2018. Bloom drivers of the potentially harmful dinoflagellate Prorocentrum minimum (Pavillard) Schiller in a south eastern temperate Australian estuary. Estuar. Coast. Shelf Sci. 215:161–71
    [Google Scholar]
  2. Baker KG, Robinson CM, Radford DT, McInnes AS, Evenhuis C, Doblin MA 2016. Thermal performance curves of functional traits aid understanding of thermally induced changes in diatom-mediated biogeochemical fluxes. Front. Mar. Sci. 3:2605
    [Google Scholar]
  3. Barshis DJ. 2015. Genomic potential for coral survival of climate change. Coral Reefs in the Anthropocene C Birkeland 133–46 Dordrecht, Neth.: Springer
    [Google Scholar]
  4. Bay RA, Rose N, Barrett R, Bernatchez L, Ghalambor CK et al. 2017. Predicting responses to contemporary environmental change using evolutionary response architectures. Am. Nat. 189:463–73
    [Google Scholar]
  5. Beaumont HJE, Gallie J, Kost C, Ferguson GC, Rainey PB 2009. Experimental evolution of bet hedging. Nature 462:90–93
    [Google Scholar]
  6. Bell G. 2017. Evolutionary rescue. Annu. Rev. Ecol. Evol. Syst. 48:605–27
    [Google Scholar]
  7. Bennett AF, Lenski RE. 1993. Evolutionary adaptation to temperature II. Thermal niches of experimental lines of Escherichia coli. . Evolution 47:1–12
    [Google Scholar]
  8. Bernhardt JR, Sunday JM, Thompson PL, O'Connor MI 2018. Nonlinear averaging of thermal experience predicts population growth rates in a thermally variable environment. Proc. R. Soc. B 285:20181076
    [Google Scholar]
  9. Bestion E, García‐Carreras B, Schaum C, Pawar S, Yvon‐Durocher G 2018. Metabolic traits predict the effects of warming on phytoplankton competition. Ecol. Lett 21:655–64
    [Google Scholar]
  10. Blanchard JL, Heneghan RF, Everett JD, Trebilco R, Richardson AJ 2017. From bacteria to whales: using functional size spectra to model marine ecosystems. Trends Ecol. Evol. 32:174–86
    [Google Scholar]
  11. Blundell JR, Schwartz K, Francois D, Fisher DS, Sherlock G, Levy SF 2019. The dynamics of adaptive genetic diversity during the early stages of clonal evolution. Nat. Ecol. Evol. 3:293–301
    [Google Scholar]
  12. Botero CA, Weissing FJ, Wright J, Rubenstein DR 2015. Evolutionary tipping points in the capacity to adapt to environmental change. PNAS 112:184–89
    [Google Scholar]
  13. Boyd PW, Collins S, Dupont S, Fabricius K, Gattuso J-P et al. 2018. Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change—a review. Glob. Change Biol. 24:2239–61
    [Google Scholar]
  14. Boyd PW, Cornwall CE, Davison A, Doney SC, Fourquez M et al. 2016a. Biological responses to environmental heterogeneity under future ocean conditions. Glob. Change Biol. 22:2633–50
    [Google Scholar]
  15. Boyd PW, Dillingham PW, McGraw CM, Armstrong EA, Cornwall CE et al. 2016b. Physiological responses of a Southern Ocean diatom to complex future ocean conditions. Nat. Clim. Change 6:207–13
    [Google Scholar]
  16. Boyd PW, Doney SC, Stzepek R, Dusenberry J, Lindsay K, Fung I 2008. Climate-mediated changes to mixed-layer properties in the Southern Ocean: assessing the phytoplankton response. Biogeosciences 5:847–64
    [Google Scholar]
  17. Boyd PW, Lennartz ST, Glover DM, Doney SC 2014. Biological ramifications of climate-change-mediated oceanic multi-stressors. Nat. Clim. Change 5:71–79
    [Google Scholar]
  18. Boyd PW, Rynearson TA, Armstrong EA, Fu F, Hayashi K et al. 2013. Marine phytoplankton temperature versus growth responses from polar to tropical waters – outcome of a scientific community-wide study. PLOS ONE 8:e63091
    [Google Scholar]
  19. Brennan GL, Colegrave N, Collins S 2017. Evolutionary consequences of multidriver environmental change in an aquatic primary producer. PNAS 114:9930–35
    [Google Scholar]
  20. Brennan GL, Collins S. 2015. Growth responses of a green alga to multiple environmental drivers. Nat. Clim. Change 5:892–97
    [Google Scholar]
  21. Burggren WW. 2017. Epigenetics in insects: mechanisms, phenotypes and ecological and evolutionary implications. Adv. Insect Physiol. 53:1–30
    [Google Scholar]
  22. Burke MK, Liti G, Long AD 2014. Standing genetic variation drives repeatable experimental evolution in outcrossing populations of Saccharomyces cerevisiae. Mol. Biol. Evol 31:3228–39
    [Google Scholar]
  23. Carlson SM, Cunningham CJ, Westley PAH 2014. Evolutionary rescue in a changing world. Trends Ecol. Evol. 29:521–30
    [Google Scholar]
  24. Chevin LM, Hoffmann AA. 2017. Evolution of phenotypic plasticity in extreme environments. Philos. Trans. R. Soc. B 372:20160138
    [Google Scholar]
  25. Chevin LM, Lande R, Mace GM 2010. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLOS Biol 8:e1000357
    [Google Scholar]
  26. Coles VJ, Stukel MR, Brooks MT, Burd A, Crump BC et al. 2017. Ocean biogeochemistry modeled with emergent trait-based genomics. Science 358:1149–54
    [Google Scholar]
  27. Collins S. 2011. Many possible worlds: expanding the ecological scenarios in experimental evolution. Evol. Biol. 38:3–14
    [Google Scholar]
  28. Collins S. 2016. Growth rate evolution in improved environments under Prodigal Son dynamics. Evol. Appl. 9:1179–88
    [Google Scholar]
  29. Collins S, Bell G. 2004. Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature 431:566–69
    [Google Scholar]
  30. Collins S, Bell G. 2006. Evolution of natural algal populations at elevated CO2. Ecol. Lett. 9:129–35
    [Google Scholar]
  31. Collins S, de Meaux J 2009. Adaptation to different rates of environmental change in Chlamydomonas. Evol. Biol 63:2952–65
    [Google Scholar]
  32. Collins S, de Meaux J, Acquisti C 2007. Adaptive walks toward a moving optimum. Genetics 176:1089–99
    [Google Scholar]
  33. Collins S, Rost B, Rynearson TA 2013. Evolutionary potential of marine phytoplankton under ocean acidification. Evol. Appl. 7:140–55
    [Google Scholar]
  34. Collins S, Sültemeyer D, Bell G 2006a. Changes in C uptake in populations of Chlamydomonas reinhardtii selected at high CO2. Plant Cell Environ 29:1812–19
    [Google Scholar]
  35. Collins S, Sültemeyer D, Bell G 2006b. Rewinding the tape: selection of algae adapted to high CO2 at current and pleistocene levels of CO2. Evolution 60:1392–401
    [Google Scholar]
  36. Constable AJ, Thomas JM, Corney SP, Arrigo KR, Barbraud C et al. 2014. Climate change and Southern Ocean ecosystems I: how changes in physical habitats directly affect marine biota. Glob. Change Biol. 20:3004–25
    [Google Scholar]
  37. Cooper TF. 2007. Recombination speeds adaptation by reducing competition between beneficial mutations in populations of Escherichia coli. . PLOS Biol 5:e225
    [Google Scholar]
  38. Crawfurd KJ, Raven JA, Wheeler GL, Baxter EJ, Joint I 2011. The response of Thalassiosira pseudonana to long-term exposure to increased CO2 and decreased pH. PLOS ONE 6:e26695
    [Google Scholar]
  39. de Visser JAGM, Krug J 2014. Empirical fitness landscapes and the predictability of evolution. Nat. Rev. Genet. 15:480–90
    [Google Scholar]
  40. Denman KL. 2003. Modelling planktonic ecosystems: parameterizing complexity. Prog. Oceanogr. 57:429–52
    [Google Scholar]
  41. Denman KL. 2017. A model simulation of the adaptive evolution through mutation of the coccolithophore Emiliania huxleyi based on a published laboratory study. Front. Mar. Sci. 3:487
    [Google Scholar]
  42. Doblin MA, Van Sebille E 2016. Drift in ocean currents impacts intergenerational microbial exposure to temperature. PNAS 113:5700–5
    [Google Scholar]
  43. Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F et al. 2012. Climate change impacts on marine ecosystems. Annu. Rev. Mar. Sci. 4:11–37
    [Google Scholar]
  44. Draghi JA, Whitlock MC. 2012. Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evol. Biol. 66:2891–902
    [Google Scholar]
  45. Dutkiewicz S, Morris JJ, Follows MJ, Scott J, Levitan O et al. 2015. Impact of ocean acidification on the structure of future phytoplankton communities. Nat. Clim. Change 5:10026
    [Google Scholar]
  46. Dutkiewicz S, Scott JR, Follows MJ 2013. Winners and losers: ecological and biogeochemical changes in a warming ocean. Glob. Biogeochem. Cycles 27:463–77
    [Google Scholar]
  47. Ehrenreich IM, Pfennig DW. 2016. Genetic assimilation: a review of its potential proximate causes and evolutionary consequences. Ann. Bot. 117:769–79
    [Google Scholar]
  48. Elena SF, Lenski RE. 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat. Rev. Genet. 4:457–69
    [Google Scholar]
  49. Falkowski PG, Fenchel T, DeLong EF 2008. The microbial engines that drive Earth's biogeochemical cycles. Science 320:1034–39
    [Google Scholar]
  50. Flombaum P, Gallegos JL, Gordillo RA, Rincón J, Zabala LL et al. 2013. Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. . PNAS 110:9824–29
    [Google Scholar]
  51. Follows MJ, Dutkiewicz S, Grant S, Chisholm SW 2007. Emergent biogeography of microbial communities in a model ocean. Science 315:1843–46
    [Google Scholar]
  52. Ghalambor CK, Hoke KL, Ruell EW, Fischer EK, Reznick DN, Hughes KA 2015. Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature 525:372–75
    [Google Scholar]
  53. Ghalambor CK, McKay JK, Carroll SP, Reznick DN 2007. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21:394–407
    [Google Scholar]
  54. Gillespie AR, Gardner A, West SA, Griffin AS 2015. Frequency dependence and cooperation: theory and a test with bacteria. Am. Nat. 170:331–42
    [Google Scholar]
  55. Giraud T, Koskella B, Laine A-L 2017. Introduction: microbial local adaptation: insights from natural populations, genomics and experimental evolution. Mol. Ecol. 26:1703–10
    [Google Scholar]
  56. Goldsby HJ, Knoester DB, Ofria C, Kerr B 2014. The evolutionary origin of somatic cells under the dirty work hypothesis. PLOS Biol 12:e1001858
    [Google Scholar]
  57. Gomez-Mestre I, Jovani R. 2013. A heuristic model on the role of plasticity in adaptive evolution: Plasticity increases adaptation, population viability and genetic variation. Proc. R. Soc. B 280:20131869
    [Google Scholar]
  58. Gorter FA, Aarts MMG, Zwaan BJ, de Visser JAGM 2016. Dynamics of adaptation in experimental yeast populations exposed to gradual and abrupt change in heavy metal concentration. Am. Nat. 187:110–19
    [Google Scholar]
  59. Gorter FA, Derks MFL, van den Heuvel J, Aarts MGM, Zwaan BJ et al. 2017. Genomics of adaptation depends on the rate of environmental change in experimental yeast populations. Mol. Biol. Evol. 34:2613–26
    [Google Scholar]
  60. Gunderson AR, Armstrong EJ, Stillman JH 2015. Multiple stressors in a changing world: the need for an improved perspective on physiological responses to the dynamic marine environment. Annu. Rev. Mar. Sci. 8:357–78
    [Google Scholar]
  61. Heckwolf MJ, Meyer BS, Döring T, Eizaguirre C, Reusch TBH 2018. Transgenerational plasticity and selection shape the adaptive potential of sticklebacks to salinity change. Evol. Appl. 11:1873–85
    [Google Scholar]
  62. Hendry AP. 2015. Key questions on the role of phenotypic plasticity in eco-evolutionary dynamics. J. Hered. 107:25–41
    [Google Scholar]
  63. Hermisson J, Pennings PS. 2017. Soft sweeps and beyond: understanding the patterns and probabilities of selection footprints under rapid adaptation. Methods Ecol. Evol. 8:700–16
    [Google Scholar]
  64. Hoppe CJM, Flintrop CM, Rost B 2018. The Arctic picoeukaryote Micromonas pusilla benefits synergistically from warming and ocean acidification. Biogeosciences 15:4353–65
    [Google Scholar]
  65. Hosaka A, Kakutani T. 2018. Transposable elements, genome evolution and transgenerational epigenetic variation. Curr. Opin. Genet. Dev. 49:43–48
    [Google Scholar]
  66. Houle D, Bolstad GH, van der Linde K, Hansen TF 2017. Mutation predicts 40 million years of fly wing evolution. Nature 548:447–50
    [Google Scholar]
  67. Hutchins DA, Fu F-X, Webb EA, Walworth N, Tagliabue A 2013. Taxon-specific response of marine nitrogen fixers to elevated carbon dioxide concentrations. Nat. Geosci. 6:790–95
    [Google Scholar]
  68. Hutchins DA, Mulholland MR, Fu F 2009. Nutrient cycles and marine microbes in a CO2-enriched ocean. Oceanography 22:4128–45
    [Google Scholar]
  69. Hutchins DA, Walworth NG, Webb EA, Saito MA, Moran D et al. 2015. Irreversibly increased nitrogen fixation in Trichodesmium experimentally adapted to elevated carbon dioxide. Nat. Commun. 6:8155
    [Google Scholar]
  70. Jablonka E. 2017. The evolutionary implications of epigenetic inheritance. Interface Focus 7:20160135
    [Google Scholar]
  71. Keller KM, Joos F, Raible C 2014. Time of emergence of trends in ocean biogeochemistry. Biogeosciences 11:3647–59
    [Google Scholar]
  72. Ketola T, Mikonranta L, Zhang J, Saarinen K, Ormala A-M et al. 2013. Fluctuating temperature leads to evolution of thermal generalism and preadaptation to novel environments. Evol. Biol. 67:2936–44
    [Google Scholar]
  73. Ketola T, Saarinen K. 2015. Experimental evolution in fluctuating environments: tolerance measurements at constant temperatures incorrectly predict the ability to tolerate fluctuating temperatures. J. Evol. Biol. 28:800–6
    [Google Scholar]
  74. Kirkup BC, Riley MA. 2004. Antibiotic-mediated antagonism leads to a bacterial game of rock–paper–scissors in vivo. Nature 428:412–14
    [Google Scholar]
  75. Klironomos FD, Berg J, Collins S 2013. How epigenetic mutations can affect genetic evolution: model and mechanism. BioEssays 35:571–78
    [Google Scholar]
  76. Knies JL, Izem R, Supler KL, Kingsolver JG, Burch CL 2006. The genetic basis of thermal reaction norm evolution in lab and natural phage populations. PLOS Biol 4:e201
    [Google Scholar]
  77. Kronholm I. 2017. Adaptive evolution and epigenetics. Handbook of Epigenetics: The New Molecular and Medical Genetics TO Tollefsbol 427–38 Cambridge, MA: Academic
    [Google Scholar]
  78. 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]
  79. Kronholm I, Collins S. 2015. Epigenetic mutations can both help and hinder adaptive evolution. Mol. Ecol. 25:1856–68
    [Google Scholar]
  80. Kronholm I, Johannesson H, Ketola T 2016. Epigenetic control of phenotypic plasticity in the filamentous fungus Neurospora crassa. . G3 6:4009–22
    [Google Scholar]
  81. Lachapelle J, Bell G. 2012. Evolutionary rescue of sexual and asexual populations in a deteriorating environment. Evol. Biol. 66:3508–18
    [Google Scholar]
  82. Lachapelle J, Colegrave N, Bell G 2017. The effect of selection history on extinction risk during severe environmental change. J. Evol. Biol. 30:1872–83
    [Google Scholar]
  83. Lande R. 2009. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J. Evol. Biol. 22:1435–46
    [Google Scholar]
  84. Lande R. 2014. Evolution of phenotypic plasticity and environmental tolerance of a labile quantitative character in a fluctuating environment. J. Evol. Biol. 27:866–75
    [Google Scholar]
  85. Landry CR, Lemos B, Rifkin SA, Dickenson WJ, Hartl DL 2007. Genetic properties influencing the evolvability of gene expression. Science 317:118–21
    [Google Scholar]
  86. Lässig M, Mustonen V, Walczak AM 2017. Predicting evolution. Nat. Ecol. Evol. 1:77
    [Google Scholar]
  87. Lawson CR, Vindenes Y, Bailey L, van de Pol M 2015. Environmental variation and population responses to global change. Ecol. Lett. 18:724–36
    [Google Scholar]
  88. Lenski RE. 2017a. Experimental evolution and the dynamics of adaptation and genome evolution in microbial populations. ISME J 11:2181–94
    [Google Scholar]
  89. Lenski RE. 2017b. What is adaptation by natural selection? Perspectives of an experimental microbiologist. PLOS Genet 13:e1006668
    [Google Scholar]
  90. Li F, Beardall J, Collins S, Gao K 2017. Decreased photosynthesis and growth with reduced respiration in the model diatom Phaeodactylum tricornutum grown under elevated CO2 over 1800 generations. Glob. Change Biol. 23:127–37
    [Google Scholar]
  91. Li W, Ding J, Li F, Wang T, Yang Y, Li Y, Campbell DA, Gao K 2019. Functional responses of smaller and larger diatoms to gradual CO2 rise. Sci. Total Environ. 680:79–90
    [Google Scholar]
  92. Lind MI, Spagopoulou F. 2018. Evolutionary consequences of epigenetic inheritance. Heredity 121:205–9
    [Google Scholar]
  93. Listmann L, LeRoch M, Schlüter L, Thomas MK, Reusch TBH 2016. Swift thermal reaction norm evolution in a key marine phytoplankton species. Evol. Appl. 9:1156–64
    [Google Scholar]
  94. Litchman E, Edwards KF, Klausmeier CA 2015. Microbial resource utilization traits and trade-offs: implications for community structure, functioning, and biogeochemical impacts at present and in the future. Front. Microbiol. 6:254
    [Google Scholar]
  95. Lohbeck KT, Riebesell U, Reusch TBH 2012. Adaptive evolution of a key phytoplankton species to ocean acidification. Nat. Geosci. 5:346–51
    [Google Scholar]
  96. Low-Décarie E, Jewell MD, Fussmann GF, Bell G 2013. Long-term culture at elevated atmospheric CO2 fails to evoke specific adaptation in seven freshwater phytoplankton species. Proc. R. Soc. B 280:20122598
    [Google Scholar]
  97. Malerba ME, Palacios MM, Palacios Delgado YM, Beardall J, Marshall DJ 2018. Cell size, photosynthesis and the package effect: an artificial selection approach. New Phytol 219:449–61
    [Google Scholar]
  98. Martin G, Elena SF, Lenormand T 2007. Distributions of epistasis in microbes fit predictions from a fitness landscape model. Nat. Genet. 39:555–60
    [Google Scholar]
  99. Matuszewski S, Hermisson J, Kopp M 2014. Fisher's geometric model with a moving optimum. Evol. Biol. 68:2571–88
    [Google Scholar]
  100. Matuszewski S, Hermisson J, Kopp M 2015. Catch me if you can: adaptation from standing genetic variation to a moving phenotypic optimum. Genetics 200:1255–74
    [Google Scholar]
  101. 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:e1007220
    [Google Scholar]
  102. Merilä J, Hendry AP. 2014. Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol. Appl. 7:1–14
    [Google Scholar]
  103. Miller CR, Van Leuven JT, Wichman HA, Joyce P 2018. Selecting among three basic fitness landscape models: additive, multiplicative and stickbreaking. Theor. Popul. Biol. 122:97–109
    [Google Scholar]
  104. Mora C, Fazier AG, Longman RJ, Dacks RS, Walton MM, Tong EJ et al. 2013. The projected timing of climate departure from recent variability. Nature 502:183–87
    [Google Scholar]
  105. Morley VJ, Turner PE. 2017. Dynamics of molecular evolution in RNA virus populations depend on sudden versus gradual environmental change. Evol. Biol. 71:872–83
    [Google Scholar]
  106. Müller MN, Schulz KG, Riebesell U 2010. Effects of long-term high CO2 exposure on two species of coccolithophores. Biogeosciences 7:1109–16
    [Google Scholar]
  107. Munday PL, Warner RR, Monro K, Pandolfi JM, Marshall DJ 2013. Predicting evolutionary responses to climate change in the sea. Ecol. Lett. 16:1488–500
    [Google Scholar]
  108. Murren CJ, Auld JR, Callahan H, Ghalambor CK, Handelsman CA et al. 2015. Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity. Heredity 115:293–301
    [Google Scholar]
  109. Noble DWA, Radersma R, Uller T 2019. Plastic responses to novel environments are biased towards phenotypic dimensions with high additive genetic variation. PNAS 116:13452–61
    [Google Scholar]
  110. O'Donnell DR, Hamman CR, Johnson EC, Kremer CT, Klausmeier CA, Litchman E 2018. Rapid thermal adaptation in a marine diatom reveals constraints and trade-offs. Glob. Change Biol. 24:4554–65
    [Google Scholar]
  111. Olson-Manning CF, Wagner MR, Mitchell-Olds T 2012. Adaptive evolution: evaluating empirical support for theoretical predictions. Nat. Rev. Genet. 13:867–77
    [Google Scholar]
  112. Osmond MM, Klausmeier CA. 2017. An evolutionary tipping point in a changing environment. Evol. Biol. 71:2930–41
    [Google Scholar]
  113. Pawlowski J, Audic S, Adl S, Bass D, Belbahri L et al. 2012. CBOL Protist Working Group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. PLOS Biol 10:e1001419
    [Google Scholar]
  114. Pillai P, Gouhier TC, Vollmer SV 2016. Ecological rescue of host-microbial systems under environmental change. Theor Ecol 10:51–63
    [Google Scholar]
  115. Putnam HM, Barott KL, Ainsworth TD, Gates RD 2017. The vulnerability and resilience of reef-building corals. Curr. Biol. 27:R528–40
    [Google Scholar]
  116. Rengefors K, Kremp A, Reusch TBH, Wood AM 2017. Genetic diversity and evolution in eukaryotic phytoplankton: revelations from population genetic studies. J. Plankton Res. 39:165–79
    [Google Scholar]
  117. Reusch TBH. 2014. Climate change in the oceans: evolutionary versus phenotypically plastic responses of marine animals and plants. Evol. Appl. 7:104–22
    [Google Scholar]
  118. Richardson AJ, Schoeman DS. 2004. Climate impact on plankton ecosystems in the Northeast Atlantic. Science 305:1609–12
    [Google Scholar]
  119. Riebesell U, Gattuso J-P. 2014. Lessons learned from ocean acidification research. Nat. Clim. Change 5:12–14
    [Google Scholar]
  120. Rynearson TA, Armbrust EV. 2005. Maintenance of clonal diversity during a spring bloom of the centric diatom Ditylum brightwellii. Mol. Ecol 14:1631–40
    [Google Scholar]
  121. Saarinen K, Laakso J, Lindstrom L, Ketola T 2018. Adaptation to fluctuations in temperature by nine species of bacteria. Ecol. Evol. 8:2901–10
    [Google Scholar]
  122. Sandrini G, Ji X, Verspagen JMH, Tann RP, Slot PC et al. 2016. Rapid adaptation of harmful cyanobacteria to rising CO2. PNAS 113:9315–20
    [Google Scholar]
  123. Schaum CE, Buckling A, Smirnoff N, Studholme DJ, Yvon-Durocher G 2018. Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom. Nat. Commun. 9:1719
    [Google Scholar]
  124. Schaum CE, Collins S. 2014. Plasticity predicts evolution in a marine alga. Proc. R. Soc. B 281:20141486
    [Google Scholar]
  125. Schaum CE, Rost B, Collins S 2015. Environmental stability affects phenotypic evolution in a globally distributed marine picoplankton. ISME J 10:75–84
    [Google Scholar]
  126. Schaum CE, Rost B, Millar AJ, Collins S 2013. Variation in plastic responses of a globally distributed picoplankton species to ocean acidification. Nat. Clim. Change 3:298–302
    [Google Scholar]
  127. Scheinin M, Riebesell U, Rynearson TA, Lohbeck KT, Collins S 2015. Experimental evolution gone wild. J. R. Soc. Interface 12:20150056
    [Google Scholar]
  128. Schlichting CD, Wund MA. 2014. Phenotypic plasticity and epigenetic marking: an assessment of evidence for genetic accommodation. Evol. Biol. 68:656–72
    [Google Scholar]
  129. Schlüter L, Lohbeck KT, Gutowska MA, Gröger JP, Riebesell U, Reusch TBH 2014. Adaptation of a globally important coccolithophore to ocean warming and acidification. Nat. Clim. Change 4:1024–30
    [Google Scholar]
  130. Schulz KG, Bach LT, Bellerby RGJ, Bermúdez R, Büdenbender J et al. 2017. Phytoplankton blooms at increasing levels of atmospheric carbon dioxide: experimental evidence for negative effects on prymnesiophytes and positive on small picoeukaryotes. Front. Mar. Sci. 4:7193
    [Google Scholar]
  131. Silverstein RN, Cunning R, Baker AC 2017. Tenacious D: Symbiodinium in clade D remain in reef corals at both high and low temperature extremes despite impairment. J. Exp. Biol. 220:1192–96
    [Google Scholar]
  132. Snell-Rood EC, Van Dyken JD, Cruickshank T, Wade MJ, Moczek AP 2010. Toward a population genetic framework of developmental evolution: the costs, limits, and consequences of phenotypic plasticity. BioEssays 32:71–81
    [Google Scholar]
  133. Sunday JM, Calosi P, Dupont S, Munday PL, Stillman JH, Reusch TBH 2014. Evolution in an acidifying ocean. Trends Ecol. Evol. 29:117–25
    [Google Scholar]
  134. Tatters AO, Roleda MY, Schnetzer A, Fu F, Hurd CL et al. 2013a. Short- and long-term conditioning of a temperate marine diatom community to acidification and warming. Philos. Trans. R. Soc. B 368:20120437
    [Google Scholar]
  135. Tatters AO, Schnetzer A, Fu F, Lie AYA, Caron DA, Hutchins DA 2013b. Short- versus long-term responses to changing CO2 in a coastal dinoflagellate bloom: implications for interspecific competitive interactions and community structure. Evol. Biol. 67:1879–91
    [Google Scholar]
  136. Thomas MK, Aranguren-Gassis M, Kremer CT, Gould MR, Anderson K et al. 2017. Temperature-nutrient interactions exacerbate sensitivity to warming in phytoplankton. Glob. Change Biol. 23:3269–80
    [Google Scholar]
  137. Thomas MK, Kremer CT, Klausmeier CA, Litchman E 2012. A global pattern of thermal adaptation in marine phytoplankton. Science 338:1085–88
    [Google Scholar]
  138. Torda G, Donelson JM, Aranda M, Barshis DJ, Bay L, Berumen ML et al. 2017. Rapid adaptive responses to climate change in corals. Nat. Clim. Change 7:627–36
    [Google Scholar]
  139. Travisano M, Mongold JA, Bennett AF 1995. Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267:87–90
    [Google Scholar]
  140. Van den Bergh B, Swings T, Fauvart M, Michiels J 2018. Experimental design, population dynamics, and diversity in microbial experimental evolution. Microbiol. Mol. Biol. Rev. 82:e00008–18
    [Google Scholar]
  141. van Oppen MJH, Gates RD, Blackall LL, Cantin N, Chakravarti LJ et al. 2017. Shifting paradigms in restoration of the world's coral reefs. Glob. Change Biol. 23:3437–48
    [Google Scholar]
  142. Verhoeven KJF, vonHoldt BM, Sork VL 2016. Epigenetics in ecology and evolution: what we know and what we need to know. Mol. Ecol. 25:1631–38
    [Google Scholar]
  143. Walworth NG, Fu F-X, Webb EA, Saito MA, Moran D et al. 2016. Mechanisms of increased Trichodesmium fitness under iron and phosphorus co-limitation in the present and future ocean. Nat. Commun. 7:12081
    [Google Scholar]
  144. Walworth NG, Hutchins DA, Dolzhenko E, Lee MD, Fu F et al. 2017. Biogeographic conservation of the cytosine epigenome in the globally important marine, nitrogen-fixing cyanobacterium Trichodesmium. Environ. Microbiol 19:4700–13
    [Google Scholar]
  145. Walworth NG, Zakem EJ, Dunne JP, Collins S, Levine NM 2019. Hitting a moving target: microbial evolutionary strategies in a dynamic ocean. bioRxiv 637272. https://doi.org/10.1101/637272
    [Crossref] [Google Scholar]
  146. Weinreich DM, Watson RA, Chao L 2005. Perspective: sign epistasis and genetic constraint on evolutionary trajectories. Evol. Biol. 59:1165–74
    [Google Scholar]
  147. Wiser MJ, Ribeck N, Lenski RE 2013. Long-term dynamics of adaptation in asexual populations. Science 342:1364–67
    [Google Scholar]
  148. Wolf KKE, Romanelli E, Rost B, John U, Collins S, Weigand H, Hoppe CJM 2019. Company matters: The presence of other genotypes alters traits and intraspecific selection in an Arctic diatom under climate change. Glob. Change Biol. 25:2689–84
    [Google Scholar]
  149. Zhang Y, Bach LT, Schulz KG, Riebesell U 2015. The modulating effect of light intensity on the response of the coccolithophore Gephyrocapsa oceanica to ocean acidification. Limnol. Oceanogr. 60:2145–57
    [Google Scholar]
  150. Zhang Y-Y, Latzel V, Fischer M, Bossdorf O 2018. Understanding the evolutionary potential of epigenetic variation: a comparison of heritable phenotypic variation in epiRILs, RILs, and natural ecotypes of Arabidopsis thaliana. . Heredity 121:257–65
    [Google Scholar]
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