Rahmstorf, S. & Coumou, D. Increase of extreme events in a warming world. Proc. Natl Acad. Sci. USA 108, 17905–17909 (2011).
Google Scholar
Somero, G. N. The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J. Exp. Biol. 213, 912–920 (2010).
Hoffmann, A. A. & Sgrò, C. M. Climate change and evolutionary adaptation. Nature 470, 479–485 (2011).
Google Scholar
Chevin, L.-M., Lande, R. & Mace, G. M. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol. 8, e1000357 (2010).
Google Scholar
Kawecki, T. J. & Ebert, D. Conceptual issues in local adaptation. Ecol. Lett. 7, 1225–1241 (2004).
Campbell-Staton, S. C. et al. Winter storms drive rapid phenotypic, regulatory, and genomic shifts in the green anole lizard. Science 357, 495–498 (2017).
Google Scholar
Barrett, R. D. H. et al. Linking a mutation to survival in wild mice. Science 363, 499–504 (2019).
Google Scholar
Therkildsen, N. O. et al. Contrasting genomic shifts underlie parallel phenotypic evolution in response to fishing. Science 365, 487–490 (2019).
Google Scholar
Brennan, R. S., Garrett, A. D., Huber, K. E., Hargarten, H. & Pespeni, M. H. Rare genetic variation and balanced polymorphisms are important for survival in global change conditions. Proc. R. Soc. B: Biol. Sci. 286, 20190943 (2019).
Google Scholar
Stearns, S. C. The evolutionary significance of phenotypic plasticity. Bioscience 39, 436–445 (1989).
Thompson, J. D. Phenotypic plasticity as a component of evolutionary change. Trends Ecol. Evol. 6, 246–249 (1991).
Google Scholar
Kelly, M. Adaptation to climate change through genetic accommodation and assimilation of plastic phenotypes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 374, 20180176 (2019).
Google Scholar
Chevin, L. M., Collins, S. & Lefèvre, F. Phenotypic plasticity and evolutionary demographic responses to climate change: taking theory out to the field. Funct. Ecol. https://doi.org/10.1111/j.1365-2435.2012.02043.x (2013).
Hendry, A. P. Key questions on the role of phenotypic plasticity in eco-evolutionary dynamics. J. Hered. 107, 25–41 (2016).
Google Scholar
Calosi, P., De Wit, P., Thor, P. & Dupont, S. Will life find a way? Evolution of marine species under global change. Evol. Appl. 9, 1035–1042 (2016).
Google Scholar
Fox, R. J., Donelson, J. M., Schunter, C., Ravasi, T. & Gaitán-Espitia, J. D. Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Philos. Trans. R. Soc. Lond. B Biol. Sci. 374, 20180174 (2019).
Google Scholar
Lande, R. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J. Evol. Biol. 22, 1435–1446 (2009).
Google Scholar
Murren, C. J. et al. Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity. Heredity 115, 293–301 (2015).
Google Scholar
Posavi, M., Gulisija, D., Munro, J. B., Silva, J. C. & Lee, C. E. Rapid evolution of genome-wide gene expression and plasticity during saline to freshwater invasions by the copepod Eurytemora affinis species complex. Mol. Ecol. 29, 4835–4856 (2020).
Google Scholar
Ghalambor, C. K. et al. Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature 525, 372–375 (2015).
Google Scholar
Kelly, M. W., Pankey, M. S., DeBiasse, M. B. & Plachetzki, D. C. Adaptation to heat stress reduces phenotypic and transcriptional plasticity in a marine copepod. Funct. Ecol. 31, 398–406 (2017).
Sikkink, K. L., Reynolds, R. M., Ituarte, C. M., Cresko, W. A. & Phillips, P. C. Rapid evolution of phenotypic plasticity and shifting thresholds of genetic assimilation in the nematode Caenorhabditis remanei. G3 4, 1103–1112 (2014).
Google Scholar
Brennan, R. S., Galvez, F. & Whitehead, A. Reciprocal osmotic challenges reveal mechanisms of divergence in phenotypic plasticity in the killifish Fundulus heteroclitus. J. Exp. Biol. 218, 1212–1222 (2015).
Google Scholar
Kelly, M. W., Pankey, M. S. & DeBiasse, M. B. Adaptation to heat stress reduces phenotypic and transcriptional plasticity in a marine copepod. Funct. Ecol. https://doi.org/10.1111/1365-2435.12725 (2017).
Waddington, C. H. Genetic assimilation of an acquired character. Evolution 7, 118–126 (1953).
Schlötterer, C., Kofler, R., Versace, E., Tobler, R. & Franssen, S. U. Combining experimental evolution with next-generation sequencing: a powerful tool to study adaptation from standing genetic variation. Heredity 114, 431–440 (2015).
Google Scholar
Munday, P. L., Warner, R. R., Monro, K., Pandolfi, J. M. & Marshall, D. J. Predicting evolutionary responses to climate change in the sea. Ecol. Lett. 16, 1488–1500 (2013).
Google Scholar
Huang, Y. & Agrawal, A. F. Experimental evolution of gene expression and plasticity in alternative selective regimes. PLoS Genet. 12, e1006336 (2016).
Google Scholar
Mallard, F., Nolte, V. & Schlötterer, C. The evolution of phenotypic plasticity in response to temperature stress. Genome Biol. Evol. 12, 2429–2440 (2020).
Google Scholar
Schaum, C. E. & Collins, S. Plasticity predicts evolution in a marine alga. Proc. Biol. Sci. 281, 20141486 (2014).
Kelly, S. A., Czech, P. P., Wight, J. T., Blank, K. M. & Garland, T. Jr Experimental evolution and phenotypic plasticity of hindlimb bones in high-activity house mice. J. Morphol. 267, 360–374 (2006).
Google Scholar
Garland, T. Jr & Kelly, S. A. Phenotypic plasticity and experimental evolution. J. Exp. Biol. 209, 2344–2361 (2006).
Google Scholar
Gibbin, E. M., Massamba N’Siala, G., Chakravarti, L. J., Jarrold, M. D. & Calosi, P. The evolution of phenotypic plasticity under global change. Sci. Rep. 7, 17253 (2017).
Google Scholar
McCairns, R. J. S. & Bernatchez, L. Adaptive divergence between freshwater and marine sticklebacks: insights into the role of phenotypic plasticity from an integrated analysis of candidate gene expression. Evolution 64, 1029–1047 (2010).
Google Scholar
Whitehead, A. The evolutionary radiation of diverse osmotolerant physiologies in killifish (Fundulus sp.). Evolution 64, 2070–2085 (2010).
Google Scholar
Lind, M. I. & Johansson, F. The degree of adaptive phenotypic plasticity is correlated with the spatial environmental heterogeneity experienced by island populations of Rana temporaria. J. Evol. Biol. 20, 1288–1297 (2007).
Google Scholar
Lázaro-Nogal, A. et al. Environmental heterogeneity leads to higher plasticity in dry-edge populations of a semi-arid Chilean shrub: insights into climate change responses. J. Ecol. 103, 338–350 (2015).
Gianoli, E. Plasticity of traits and correlations in two populations of Convolvulus arvensis (Convolvulaceae) differing in environmental heterogeneity. Int. J. Plant Sci. 165, 825–832 (2004).
Fischer, E. K., Song, Y., Hughes, K. A., Zhou, W. & Hoke, K. L. Nonparallel transcriptional divergence during parallel adaptation. Mol. Ecol. 30, 1516–1530 (2021).
Google Scholar
Gunter, H. M., Schneider, R. F., Karner, I., Sturmbauer, C. & Meyer, A. Molecular investigation of genetic assimilation during the rapid adaptive radiations of East African cichlid fishes. Mol. Ecol. 26, 6634–6653 (2017).
Google Scholar
Bitter, M. C. et al. Fluctuating selection and global change: a synthesis and review on disentangling the roles of climate amplitude, predictability and novelty. Proc. Biol. Sci. 288, 20210727 (2021).
Google Scholar
Skliris, N. et al. Salinity changes in the World Ocean since 1950 in relation to changing surface freshwater fluxes. Clim. Dyn. 43, 709–736 (2014).
Collins, M. et al. Long-term climate change: projections, commitments and irreversibility. in Climate Change 2013-The Physical Science Basis: Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. 1029–1136 (Cambridge University Press, 2013).
Sunday, J. M. et al. Evolution in an acidifying ocean. Trends Ecol. Evol. 29, 117–125 (2014).
Google Scholar
Reusch, T. B. H. & Boyd, P. W. Experimental evolution meets marine phytoplankton. Evolution 67, 1849–1859 (2013).
Google Scholar
Palumbi, S. R., Evans, T. G., Pespeni, M. H. & Somero, G. N. Present and future adaptation of marine species assemblages. Oceanography https://doi.org/10.5670/oceanog.2019.314 (2019).
Helmuth, B. et al. Long-term, high frequency in situ measurements of intertidal mussel bed temperatures using biomimetic sensors. Sci. Data 3, 160087 (2016).
Google Scholar
Feely, R. A., Sabine, C. L., Hernandez-Ayon, J. M., Ianson, D. & Hales, B. Evidence for upwelling of corrosive ‘acidified’ water onto the continental shelf. Science 320, 1490–1492 (2008).
Google Scholar
Cowen, R. K. & Sponaugle, S. Larval dispersal and marine population connectivity. Ann. Rev. Mar. Sci. 1, 443–466 (2009).
Google Scholar
Huys, R. & Boxshall, G. A. Copepod Evolution. (marinespecies.org, 1991).
Langer, J. A. F. et al. Acclimation and adaptation of the coastal calanoid copepod Acartia tonsa to ocean acidification: a long-term laboratory investigation. Mar. Ecol. Prog. Ser. 619, 35–51 (2019).
Google Scholar
Dam, H. G. Evolutionary adaptation of marine zooplankton to global change. Ann. Rev. Mar. Sci. 5, 349–370 (2013).
Google Scholar
De Wit, P., Dupont, S. & Thor, P. Selection on oxidative phosphorylation and ribosomal structure as a multigenerational response to ocean acidification in the common copepod Pseudocalanus acuspes. Evol. Appl. 9, 1112–1123 (2016).
Google Scholar
Thor, P. & Dupont, S. Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod. Glob. Chang. Biol. 21, 2261–2271 (2015).
Google Scholar
Donelson, J. M. et al. Understanding interactions between plasticity, adaptation and range shifts in response to marine environmental change. Philos. Trans. R. Soc. Lond. B Biol. Sci. 374, 20180186 (2019).
Google Scholar
Gibbin, E. M. et al. 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, 551–563 (2017).
Google Scholar
Mauchline, J. The Biology of Calanoid Copepods (Academic Press, 1998).
Steinberg, D. K. & Landry, M. R. Zooplankton and the ocean carbon cycle. Ann. Rev. Mar. Sci. 9, 413–444 (2017).
Google Scholar
Gobler, C. J. & Baumann, H. Hypoxia and acidification in ocean ecosystems: coupled dynamics and effects on marine life. Biol. Lett. 12, 20150976 (2016).
Rice, E., Dam, H. G. & Stewart, G. Impact of climate change on estuarine zooplankton: surface water warming in Long Island Sound is associated with changes in copepod size and community structure. Estuaries Coasts 38, 13–23 (2015).
IPCC. Climate Change 2014: Mitigation of Climate Change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Vol. 1454 (IPCC, 2014).
Caldeira, K. & Wickett, M. E. Oceanography: anthropogenic carbon and ocean pH. Nature 425, 365 (2003).
Google Scholar
Dam, H. G. et al. Rapid, but limited, zooplankton adaptation to simultaneous warming and acidification. Nat. Clim. Chang. 11, 780–786 (2021).
Google Scholar
Behrenfeld, M. J. et al. Climate-driven trends in contemporary ocean productivity. Nature 444, 752–755 (2006).
Google Scholar
Barghi, N., Hermisson, J. & Schlötterer, C. Polygenic adaptation: a unifying framework to understand positive selection. Nat. Rev. Genet. 21, 769–781 (2020).
Google Scholar
Láruson, Á. J., Yeaman, S. & Lotterhos, K. E. The importance of genetic redundancy in evolution. Trends Ecol. Evol. 35, 809–822 (2020).
Google Scholar
Tobler, R. et al. Massive habitat-specific genomic response in D. melanogaster populations during experimental evolution in hot and cold environments. Mol. Biol. Evol. 31, 364–375 (2014).
Google Scholar
Belhadj Slimen, I. et al. Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. A review. Int. J. Hyperth. 30, 513–523 (2014).
Google Scholar
Downs, C. A. & Heckathorn, S. A. The mitochondrial small heat-shock protein protects NADH:ubiquinone oxidoreductase of the electron transport chain during heat stress in plants. FEBS Lett. 430, 246–250 (1998).
Google Scholar
Harada, A. E., Healy, T. M. & Burton, R. S. Variation in thermal tolerance and its relationship to mitochondrial function across populations of Tigriopus californicus. Front. Physiol. 10, 213 (2019).
Google Scholar
Chung, D. J. & Schulte, P. M. Mitochondria and the thermal limits of ectotherms. J. Exp. Biol. 223 (2020).
Mathew, A. N. U. & Morimoto, R. I. Role of the heat-shock response in the life and death of proteins. Ann. N. Y. Acad. Sci. 851, 99–111 (1998).
Google Scholar
Evans, T. G., Pespeni, M. H., Hofmann, G. E., Palumbi, S. R. & Sanford, E. Transcriptomic responses to seawater acidification among sea urchin populations inhabiting a natural pH mosaic. Mol. Ecol. 26, 2257–2275 (2017).
Google Scholar
Bailey, A. et al. Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO2-acidified sea water. Ecol. Evol. 7, 7145–7160 (2017).
Google Scholar
Tenaillon, O. et al. The molecular diversity of adaptive convergence. Science 335, 457–461 (2012).
Google Scholar
Anjum, R. & Blenis, J. The RSK family of kinases: emerging roles in cellular signalling. Nat. Rev. Mol. Cell Biol. 9, 747–758 (2008).
Google Scholar
Marshall, D. J. Transgenerational plasticity in the sea: context-dependent maternal effects across the life history. Ecology 89, 418–427 (2008).
Google Scholar
Vehmaa, A., Brutemark, A. & Engström-Öst, J. Maternal effects may act as an adaptation mechanism for copepods facing pH and temperature changes. PLoS ONE 7, e48538 (2012).
Google Scholar
Skinner, M. K. What is an epigenetic transgenerational phenotype? F3 or F2. Reprod. Toxicol. 25, 2–6 (2008).
Google Scholar
Sasaki, M. C. & Dam, H. G. Integrating patterns of thermal tolerance and phenotypic plasticity with population genetics to improve understanding of vulnerability to warming in a widespread copepod. Glob. Chang. Biol. 25, 4147–4164 (2019).
Google Scholar
Sasaki, M. C. & Dam, H. G. Genetic differentiation underlies seasonal variation in thermal tolerance, body size, and plasticity in a short‐lived copepod. Ecol. Evol. 90, 193 (2020).
Ho, W.-C., Li, D., Zhu, Q. & Zhang, J. Phenotypic plasticity as a long-term memory easing readaptations to ancestral environments. Sci. Adv. 6, eaba3388 (2020).
Google Scholar
Caswell, H. Matrix population models. Encyclopedia of Environmetrics 3, https://doi.org/10.1002/9781118445112.stat07481 (2006).
Huey, R. B., Wakefield, T., Crill, W. D. & Gilchrist, G. W. Within- and between-generation effects of temperature on early fecundity of Drosophila melanogaster. Heredity 74, 216–223 (1995). Pt 2.
Google Scholar
Zwaan, B., Bijlsma, R. & Hoekstra, R. F. Direct selection on life span in Drosophila melanogaster. Evolution 49, 649–659 (1995).
Google Scholar
Reznick, D. A., Bryga, H. & Endler, J. A. Experimentally induced life-history evolution in a natural population. Nature 346, 357–359 (1990).
Google Scholar
Jerison, E. R., Nguyen Ba, A. N., Desai, M. M. & Kryazhimskiy, S. Chance and necessity in the pleiotropic consequences of adaptation for budding yeast. Nat. Ecol. Evol. 4, 601–611 (2020).
Google Scholar
Zhong, S., Khodursky, A., Dykhuizen, D. E. & Dean, A. M. Evolutionary genomics of ecological specialization. Proc. Natl Acad. Sci. USA 101, 11719–11724 (2004).
Google Scholar
MacLean, R. C., Bell, G. & Rainey, P. B. The evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens. Proc. Natl Acad. Sci. USA 101, 8072–8077 (2004).
Google Scholar
Bettencourt, B. R., Feder, M. E. & Cavicchi, S. Experimental evolution of HSP70 expression and thermotolerance in Drosophila melanogaster. Evolution 53, 484–492 (1999).
Google Scholar
Schaum, C.-E., Buckling, A., Smirnoff, N., Studholme, D. J. & Yvon-Durocher, G. Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom. Nat. Commun. 9, 1719 (2018).
Google Scholar
Orr, H. A. Adaptation and the cost of complexity. Evolution 54, 13–20 (2000).
Google Scholar
Chen, P. & Zhang, J. Antagonistic pleiotropy conceals molecular adaptations in changing environments. Nat. Ecol. Evol. 4, 461–469 (2020).
Google Scholar
Cox, P. M., Betts, R. A., Jones, C. D., Spall, S. A. & Totterdell, I. J. Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408, 184–187 (2000).
Google Scholar
Mayor, D. J., Sommer, U., Cook, K. B. & Viant, M. R. The metabolic response of marine copepods to environmental warming and ocean acidification in the absence of food. Sci. Rep. 5, 13690 (2015).
Google Scholar
Pedersen, S. A. et al. Multigenerational exposure to ocean acidification during food limitation reveals consequences for copepod scope for growth and vital rates. Environ. Sci. Technol. 48, 12275–12284 (2014).
Google Scholar
Bono, L. M., Smith, L. B. Jr, Pfennig, D. W. & Burch, C. L. The emergence of performance trade-offs during local adaptation: insights from experimental evolution. Mol. Ecol. 26, 1720–1733 (2017).
Google Scholar
Masel, J., King, O. D. & Maughan, H. The loss of adaptive plasticity during long periods of environmental stasis. Am. Nat. 169, 38–46 (2007).
Google Scholar
Bay, R. A. et al. Genomic signals of selection predict climate-driven population declines in a migratory bird. Science 359, 83–86 (2018).
Google Scholar
Bay, R. A. et al. Predicting responses to contemporary environmental change using evolutionary response architectures. Am. Nat. 189, 463–473 (2017).
Google Scholar
Bush, A. et al. Incorporating evolutionary adaptation in species distribution modelling reduces projected vulnerability to climate change. Ecol. Lett. 19, 1468–1478 (2016).
Google Scholar
Valladares, F. et al. The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecol. Lett. 17, 1351–1364 (2014).
Google Scholar
Feinberg, L. R. & Dam, H. G. Effects of diet on dimensions, density and sinking rates of fecal pellets of the copepod Acartia tonsa. Mar. Ecol. Prog. Ser. 175, 87–96 (1998).
Google Scholar
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
Google Scholar
Jørgensen, T. S. et al. The genome and mRNA transcriptome of the cosmopolitan calanoid copepod Acartia tonsa Dana improve the understanding of copepod genome size evolution. Genome Biol. Evol. https://doi.org/10.1093/gbe/evz067 (2019).
Haas, B. J. et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494–1512 (2013).
Google Scholar
Davidson, N. M., Hawkins, A. D. K. & Oshlack, A. SuperTranscripts: a data driven reference for analysis and visualisation of transcriptomes. Genome Biol. 18, 148 (2017).
Google Scholar
Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://arxiv.org/abs/1303.3997 (2013).
Faust, G. G. & Hall, I. M. SAMBLASTER: fast duplicate marking and structural variant read extraction. Bioinformatics 30, 2503–2505 (2014).
Google Scholar
Koboldt, D. C. et al. VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res. 22, 568–576 (2012).
Google Scholar
Soneson, C., Love, M. I. & Robinson, M. D. Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences. F1000Res. 4, 1521 (2016).
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017).
Google Scholar
R Core Team. R: A Language and Environment for Statistical Computing (R Core Team, 2019).
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
Google Scholar
Kenkel, C. D. & Matz, M. V. Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nat. Ecol. Evol. 1, 14 (2016).
Google Scholar
Campbell-Staton, S. C., Velotta, J. P. & Winchell, K. M. Selection on adaptive and maladaptive gene expression plasticity during thermal adaptation to urban heat islands. Nat. Commun. 12, 6195 (2021).
Google Scholar
Jombart, T. & Ahmed, I. adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics https://doi.org/10.1093/bioinformatics/btr521 (2011).
Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R Package. J. Stat. Softw. 33, 1–22 (2010).
Orozco-terWengel, P. et al. Adaptation of Drosophila to a novel laboratory environment reveals temporally heterogeneous trajectories of selected alleles. Mol. Ecol. 21, 4931–4941 (2012).
Google Scholar
Kofler, R. et al. PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS ONE 6, e15925 (2011).
Google Scholar
Wright, R. M., Aglyamova, G. V., Meyer, E. & Matz, M. V. Gene expression associated with white syndromes in a reef building coral, Acropora hyacinthus. BMC Genomics 16, 371 (2015).
Google Scholar
Therneau, T. M. & Grambsch, P. M. Modeling Survival Data: Extending the Cox Model (Springer, 2013).
Therneau, T. A Package for Survival Analysis in S. version 2.38. (Mayo Foundation, 2015).
Kassambara, A., Kosinski, M., Biecek, P. & Fabian, S. Package ‘survminer’. Drawing Survival Curves using ‘ggplot2’. (R package version 0. 3. 1.) (2017).
Houde, S. E. L. & Roman, M. R. Effects of food quality on the functional ingestion response of the copepod Acartia tonsa. Mar. Ecol. Prog. Ser. 40, 69–77 (1987).
Google Scholar
Brennan, R. S. et al. Code repository for ‘Loss of transcriptional plasticity but sustained adaptive capacity after adaptation to global change conditions in a marine copepod’. Zenodo https://doi.org/10.5281/zenodo.5840148 (2022).
Source: Ecology - nature.com
