García-Roger, E. M., Carmona, M. J. & Serra, M. Facing adversity: Dormant embryos in rotifers. Biol. Bull. 237, 119–144 (2019).
Denlinger, D. L. Regulation of diapause. Annu. Rev. Entomol. 47, 93–122 (2002).
Reynolds, J. A. & Hand, S. C. Embryonic diapause highlighted by differential expression of mRNAs for ecdysteroidogenesis, transcription and lipid sparing in the cricket Allonemobius socius. J. Exp. Biol. 212, 2075–2084 (2009).
Ricci, C. Dormancy patterns in rotifers. Hydrobiologia 446(447), 1–11 (2001).
Poelchau, M. F., Reynolds, J. A., Elsik, C. G., Denlinger, D. L. & Armbruster, P. A. Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus. Proc. R. Soc. B. 280, 20130143 (2013).
Alekseev, V. R., De Stasio, B. T., Gilbert, J. J. & Ravera, O. Preface. In Diapause in Aquatic Invertebrates, Theory and Human Use (eds Alekseev, V. R. et al.) xiii–xvi (Springer, New York, 2007).
Hand, S. C. & Podrabsky, J. E. Bioenergetics of diapause and quiescence in aquatic animals. Thermochim. Acta 349, 31–42 (2000).
Ślusarczyk, M., Chlebicki, W., Pijanowska, J. & Radzikowski, J. The role of the refractory period in diapause length determination in a freshwater crustacean. Sci. Rep. 9, 11905 (2019).
Tauber, M. J., Tauber, C. A. & Masaki, S. Seasonal Adaptations of Insects (Oxford University Press, Oxford, 1986).
Alekseev, V. R., De Stasio, B. T. & Gilbert, J. J. Diapause in Aquatic Invertebrates, Theory and Human Use (Springer, New York, 2012).
García-Roger, E. M., Carmona, M. J. & Serra, M. Modes, mechanisms and evidence of bet hedging in rotifer diapause traits. Hydrobiologia 796, 223–233 (2017).
Cohen, D. Optimizing reproduction in a randomly varying environment. J. Theor. Biol. 12, 119–129 (1966).
Seger, J. & Brockmann, H. J. What is bet-hedging? In Oxford Surveys in Evolutionary Biology Vol. 4 (eds Harvey, P. H. & Partridge, L.) 182–211 (Oxford University Press, Oxford, 1987).
Philippi, T. & Seger, J. Hedging one’s evolutionary bets, revisited. Trends Ecol. Evol. 4, 41–44 (1989).
Simons, A. M. Modes of response to environmental change and the elusive empirical evidence for bet hedging. Proc. R. Soc. B Biol. Sci. 278, 1601–1609 (2011).
Menu, F. & Desouhant, E. Bet-hedging for variability in life cycle duration: bigger and later-emerging chestnut weevils have increased probability of a prolonged diapause. Oecologia 132, 167–174 (2002).
Franch-Gras, L., García-Roger, E. M., Serra, M. & Carmona, M. J. Adaptation in response to environmental unpredictability. Proc. R. Soc. B Biol. Sci. 284, 20170427 (2017).
Tarazona, E., García-Roger, E. M. & Carmona, M. J. Experimental evolution of bet hedging in rotifer diapause traits as a response to environmental unpredictability. Oikos 126, 1162–1172 (2017).
Koštál, V. Eco-physiological phases of insect diapause. J. Insect Physiol. 52, 113–127 (2006).
Tammariello, S. P. & Denlinger, D. L. G0/G1 cell cycle arrest in the brain of Sarcophaga crassipalpis during pupal diapause and the expression pattern of the cell cycle regulator, proliferating cell nuclear antigen. Insect. Biochem. Mol. Biol. 28, 83–89 (1998).
Denekamp, N. Y., Reinhardt, R., Kube, M. & Lubzens, E. Late embryogenesis abundant (LEA) proteins in nondesiccated, encysted, and diapausing embryos of rotifers. Biol. Repr. 82, 714–724 (2010).
Qiu, Z. & MacRae, T. H. A molecular overview of diapause in embryos of the crustacean, Artemia franciscana. In Dormancy and Resistance in Harsh Environments (eds Lubzens, E. et al.) 165–188 (Springer, New York, 2010).
Ziv, T. et al. Dormancy in embryos: Insight from hydrated encysted embryos of an aquatic invertebrate. Mol. Cell. Proteomics 16, 1746–1769 (2017).
Roncalli, V. et al. Physiological characterization of the emergence from diapause: A transcriptomics approach. Sci. Rep. 8, 12577 (2018).
Rozema, E. et al. Metabolomics reveals novel insight on dormancy of aquatic invertebrate encysted embryos. Sci. Rep. 9, 8878 (2019).
Vanvlasselaer, E. & De Meester, L. An exploratory review on the molecular mechanisms of diapause termination in the waterflea. In Daphnia in Dormancy and Resistance in Harsh Environments (eds Lubzens, E. et al.) 189–202 (Springer, New York, 2010).
Declerck, S. A. J. & Papakostas, S. Monogonont rotifers as model systems for the study of micro-evolutionary adaptation and its eco-evolutionary implications. Hydrobiologia 796, 131–144 (2017).
Serra, M., García-Roger, E. M., Ortells, R. & Carmona, M. J. Cyclically parthenogenetic rotifers and the theories of population and evolutionary ecology. Limnetica 38, 67–93 (2019).
García-Roger, E. M., Serra, M. & Carmona, M. J. Bet-hedging in diapausing egg hatching of temporary rotifer populations—A review of models and new insights. Int. Rev. Hydrobiol. 99, 96–106 (2014).
Ricci, C. & Pagani, M. Desiccation of Panagrolaimus rigidus (Nematoda): Survival, reproduction and the influence on the internal clock. Hydrobiologia 347, 1–13 (1997).
Gordon, G. & Headrick, D. H. A Dictionary of Entomology (Oxford CABI Publ Series, Oxford, 2001).
Fan, L., Lin, J., Zhong, Y. & Liu, J. Shotgun proteomic analysis on the diapause and nondiapause eggs of domesticated silkworm Bombyx mori. PLoS ONE 8, e60386 (2013).
Schröder, T. Diapause in monogonont rotifers. Hydrobiologia 546, 291–306 (2005).
Denekamp, N. Y. et al. Discovering genes associated with dormancy in the monogonont rotifer Brachionus plicatilis. BMC Genomics 10, 108 (2009).
Denekamp, N. Y. et al. The expression pattern of dormancy-associated genes in multiple life-history stages in the rotifer Brachionus plicatilis. Hydrobiologia 662, 51–63 (2011).
Clark, M. S. et al. Long-term survival of hydrated resting eggs from Brachionus plicatilis. PLoS ONE 7, e29365 (2012).
Waterworth, W. M., Bray, C. M. & West, C. E. The importance of safeguarding genome integrity in germination and seed longevity. J. Exp. Bot. 66, 3549–3558 (2015).
Sim, C. & Denlinger, D. L. Catalase and superoxide dismutase-2 enhance survival and protect ovaries during overwintering diapause in the mosquito Culex pipiens. J. Insect Physiol. 57, 628–634 (2011).
Ragland, G. J., Denlinger, D. L. & Hahn, D. A. Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly. Proc. Natl. Acad. Sci. USA 107, 14909–14914 (2010).
Duceppe, M. O. et al. Analysis of survival and hatching transcriptomes from potato cyst nematodes, Globodera rostochiensis and G. pallida. Sci. Rep. 7, 3882 (2017).
Wise, M. J. & Tunnacliffe, A. POPP the question: What do LEA proteins do?. Trends Plant. Sci. 9, 13–17 (2004).
García-Roger, E. M. & Ortells, R. Trade-offs in rotifer diapausing egg traits: Survival, hatching, and lipid content. Hydrobiologia 805, 339–350 (2018).
Hand, S. C., Menze, M. A., Toner, M., Boswell, L. & Moore, D. LEA proteins during water stress: Not just for plants anymore. Annu. Rev. Physiol. 73, 115–134 (2011).
Crowe, J. H. et al. The trehalose myth revisited: Introduction to a symposium on stabilization of cells in the dry state. Cryobiology 43, 89–105 (2001).
Moore, D. S. & Hand, S. C. Cryopreservation of lipid bilayers by LEA proteins from Artemia franciscana and trehalose. Cryobiology 73, 240–247 (2016).
Clegg, J. S. Origin of trehalose and its significance during formation of encysted dormant embryos of Artemia Salina. Comp. Biochem. Physiol. 14, 135–143 (1965).
Caprioli, M. et al. Trehalose in desiccated rotifers: A comparison between a bdelloid and a monogonont species. Comp. Biochem. Physiol. 139, 527–532 (2004).
Li, T., Liu, L., Zhang, L. & Liu, N. Role of G-protein-coupled receptor-related genes in insecticide resistance of the mosquito, Culex quinquefasciatus. Sci. Rep. 4, 6474 (2015).
Hommaa, T. et al. G protein-coupled receptor for diapause hormone, an inducer of Bombyx embryonic diapause. Biochem. Biophys. Res. Comm. 344, 386–393 (2006).
Jones, S. J. et al. Changes in gene expression associated with developmental arrest and longevity in Caenorhabditis elegans. Genome Res. 11, 1346–1352 (2001).
Fielenbach, N. & Antebi, A. C. elegans dauer formation and the molecular basis of plasticity. Genes Dev. 15, 2149–2165 (2008).
Hand, S. C., Denlinger, D. L., Podrabsky, J. E. & Roy, R. Mechanisms of animal diapause: recent developments from nematodes, crustaceans, insects, and fish. Am. J. Physiol. Regul. Integr. Comp. Physiol. 310, R1193–R1211 (2016).
Woll, S. C. & Podrabsky, J. E. Insulin-like growth factor signaling regulates developmental trajectory associated with diapause in embryos of the annual killifish Austrofundulus limnaeus. J. Exp. Biol. 220, 2777–2786 (2017).
Yu, C. T. & Hirsh, D. The stimulatory effect of ammonium or potassium ions on the activity of leucyl-tRNA synthetase from Escherichia coli. Biochim. Biophys. Acta 142, 149–154 (1967).
Beck, S. D., Shane, J. L. & Garland, J. A. Ammonium-induced termination of diapause in the European corn borer, Ostrinia nubilalis. J. Insect. Physiol. 15, 945–951 (1969).
Birnbaumer, L. Expansion of signal transduction by G proteins. The second 15 years or so: From 3 to 16 alpha subunits plus betagamma dimers. Biochim. Biophys. Acta 1768, 772–793 (2007).
Dumont, H., Casier, P., Munuswamy, N. & De Wasche, C. Cyst hatching in Anostraca accelerated by retinoic acid, amplified by calcium ionosphore A23187, and inhibited by calcium-channel blockers. Hydrobiologia 230, 1–7 (1992).
Kim, H. J. et al. Light-dependent transcriptional events during resting egg hatching of the rotifer Brachionus manjavacas. Mar. Genomics 20, 25–31 (2015).
Boschetti, C., Ricci, C., Sotgia, C. & Fascio, U. The development of a bdelloid egg: A contribution after 100 years. Hydrobiologia 546, 323–331 (2005).
Bonneau, B., Popgeorgiev, N., Prudent, J. & Gillet, G. Cytoskeleton dynamics in early zebrafish development. A matter of phosphorylation?. Bioarchitecture 1, 216–220 (2011).
Eno, C., Solanki, B. & Pelegri, F. Aura (mid1ip1l) regulates the cytoskeleton at the zebrafish egg-to-embryo transition. Development 143, 1585–1599 (2016).
Cáceres, C. E. & Schwalbach, M. S. How well do laboratory experiments explain field patterns of zooplankton emergence?. Freshw. Biol. 46, 1179–1189 (2001).
De Stasio, B. T. Diapause in calanoid copepods: Within-clutch hatching patterns. J. Limnol. 63, 26–31 (2004).
García-Roger, E. M., Carmona, M. J. & Serra, M. Patterns in rotifer diapausing egg banks: Density and viability. J. Exp. Mar. Biol. Ecol. 336, 198–210 (2006).
Helland, S., Nejstgaard, C., Fyhn, J. J., Egge, J. K. & Båmstedt, U. Effects of starvation, season, and diet on the free amino acid and protein content of Calanus finmarchicus females. Mar. Biol. 143, 297–306 (2003).
Skottene, E. et al. The β-oxidation pathway is downregulated during diapause termination in Calanus copepods. Sci. Rep. 9, 16686 (2019).
Tan, Q., Liu, W., Zhu, F., Lei, C. & Wang, X. Fatty acid synthase 2 contributes to diapause preparation in a beetle by regulating lipid accumulation and stress tolerance genes expression. Sci. Rep. 7, 40509 (2016).
Gilbert, J. J. & Schröder, T. Rotifers from diapausing, fertilized eggs: Unique features and emergence. Limnol. Oceanogr. 49, 1341–1354 (2004).
Alekseev, V. R., Hwang, J.-S. & Tseng, M.-H. Diapause in aquatic invertebrates: What’s known and what’s next in research and medical application?. J. Mar. Sci. Tech. 14, 269–286 (2006).
Gilbert, J. J. Timing of diapause in monogonont rotifers. In Mechanisms and Strategies in Diapause in Aquatic Invertebrates. Theory and Human Use (eds Alekseev, V. R. et al.) 11–27 (Springer, New York, 2012).
Koštál, V., Štětina, T., Poupardin, R., Korbelová, J. & Bruce, A. W. Conceptual framework of the eco-physiological phases of insect diapause development justified by transcriptomic profiling. Proc. Natl. Acad. Sci. USA 114, 8532–8537 (2017).
Podrabsky, J. E. & Hand, S. C. Physiological strategies during animal diapause: Lessons from brine shrimp and annual killifish. J. Exp. Biol. 218, 1897–1906 (2015).
Zahradka, K. et al. Reassembly of shattered chromosomes in Deinococcus radiodurans. Nature 443, 569–573 (2006).
Gladyshev, E. & Meselson, M. Extreme resistance of bdelloid rotifers to ionizing radiation. Proc. Natl. Acad. Sci. USA 105, 5139–5144 (2008).
Kim, R. O. et al. Ultraviolet B retards growth, induces oxidative stress, and modulates DNA repair-related gene and heat shock protein gene expression in the monogonont rotifer, Brachionus sp. Aquat. Toxicol. 101, 529–539 (2011).
Han, J. et al. Sublethal gamma irradiation affects reproductive impairment and elevates antioxidant enzyme and DNA repair activities in the monogonont rotifer Brachionus koreanus. Aquat Toxicol. 155, 101–109 (2014).
Hagiwara, A., Hoshi, N., Kawahara, F., Tominaga, K. & Hirayama, K. Resting eggs of the marine rotifer Brachionus plicatilis Müller: Development and effect of irradiation on hatching. Hydrobiologia 313(314), 223–229 (1995).
IPCC. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (Cambridge University Press, Cambridge, 2013).
Pourriot, R. & Snell, T. W. Resting eggs of rotifers. Hydrobiologia 104, 213–224 (1983).
Altman, N. & Krzywinski, M. Split plot design. Nat. Meth. 12, 165–166 (2015).
Nelder, J. A. & Wedderburn, R. W. M. Generalized linear models. J. Roy. Stat. Soc. Ser. A 135, 370–384 (1972).
Cox, D. R. Regression models and life-tables (with discussion). J. R. Statist. Soc. B 34, 187–220 (1972).
R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/ (2017).
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
Therneau, T. M. & Grambsch, P. M. Modeling Survival Data: Extending the Cox Model (Springer, New York, 2020).
Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578 (2012).
Franch-Gras, L. et al. Genomic signatures of local adaptation to the degree of environmental unpredictability in rotifers. Sci. Rep. 8, 16051 (2018).
Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotech. 28, 511–515 (2010).
Li, B. & Dewey, C. N. RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323 (2011).
Hoffman, G. E. & Schadt, E. E. VariancePartition: Interpreting drivers of variation in complex gene expression studies. BMC Bioinformatics 17, 483 (2016).
Ritchie, M. E. et al. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015).
Benjamini, Y. & Hochberg, Y. On the adaptive control of the false discovery rate in multiple testing with independent statistics. J. Educ. Behav. Stat. 25, 60–83 (2000).
Gianetto, G. Q. et al. Calibration plot for proteomics: A graphical tool to visually check the assumptions underlying FDR control in quantitative experiments. Proteomics 16, 29–32 (2016).
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).
McCarthy, D. J., Chen, Y. & Smyth, G. K. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nuc. Acids Res. 10, 4288–4297 (2012).
Witten, D. Classification and clustering of sequencing data using a Poisson model. Ann. Appl. Stat. 5, 2493–2518 (2011).
Anderson, M. J. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62, 245–253 (2006).
Sims, D. et al. CGAT: Computational genomics analysis toolkit. Bioinformatics 30, 1290–1291 (2014).
Jones, P. et al. InterProScan 5: Genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014).
Alexa, A. & Rahnenführer, J. TopGO: Enrichment analysis for gene ontology. R package version 2.40.0. Bioconductor https://doi.org/10.18129/B9.bioc.topGO (2020).
Hanson, S. J., Stelzer, C.-P., Welch, D. B. & Logsdon, J. Comparative transcriptome analysis of obligately asexual and cyclically sexual rotifers reveals genes with putative functions in sexual reproduction, dormancy, and asexual egg production. BMC Genomics 14, 412 (2013).
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