Record, N. R. et al. Copepod diapause and the biogeography of the marine lipidscape. J. Biogeogr. 45, 2238–2251 (2018).
Google Scholar
Conover, R. J. & Corner, E. D. S. Respiration and nitrogen excretion by some marine zooplankton in relation to their life cycles. J. Mar. Biol. Assoc. UK 48, 49–75 (1968).
Google Scholar
Kattner, G. et al. Perspectives on marine zooplankton lipids. Can. J. Fish. Aquat. Sci. 64, 1628–1639 (2007).
Google Scholar
Beaugrand, G., Brander, K. M., Lindley, J. A., Souissi, S. & Reid, P. C. Plankton effect on cod recruitment in the North Sea. Nature 426, 661–664 (2003).
Google Scholar
Coyle, K. et al. Climate change in the southeastern Bering Sea: impacts on pollock stocks and implications for the oscillating control hypothesis. Fish. Oceanogr. 20, 139–156 (2011).
Google Scholar
Liu, H., Bi, H. & Peterson, W. T. Large-scale forcing of environmental conditions on subarctic copepods in the northern California Current system. Prog. Oceanogr. 134, 404–412 (2015).
Google Scholar
Peterson, W. T. et al. The pelagic ecosystem in the Northern California Current off Oregon during the 2014–2016 warm anomalies within the context of the past 20 years. J. Geophys. Res. Oceans 122, 7267–7290 (2017).
Google Scholar
Bi, H., Peterson, W. T., Lamb, J. & Casillas, E. Copepods and salmon: characterizing the spatial distribution of juvenile salmon along the Washington and Oregon coast, USA. Fish. Oceanogr. 20, 125–138 (2011).
Google Scholar
Kirby, R. R. & Beaugrand, G. Trophic amplification of climate warming. Proc. R. Soc. B 276, 4095–4103 (2009).
Google Scholar
Hirche, H.-J. Temperature and plankton II. Effect on respiration and swimming activity in copepods from the Greenland Sea. Mar. Biol. 94, 347–356 (1987).
Google Scholar
Mahara, N., Pakhomov, E. A., Jackson, J. M. & Hunt, B. P. Seasonal zooplankton development in a temperate semi-enclosed basin: two years with different spring bloom timing. J. Plankton Res. 41, 309–328 (2019).
Google Scholar
Hooff, R. C. & Peterson, W. T. Copepod biodiversity as an indicator of changes in ocean and climate conditions of the northern California current ecosystem. Limnol. Oceanogr. 51, 2607–2620 (2006).
Google Scholar
Keister, J. E., Di Lorenzo, E., Morgan, C., Combes, V. & Peterson, W. Zooplankton species composition is linked to ocean transport in the Northern California Current. Glob. Change Biol. 17, 2498–2511 (2011).
Google Scholar
Johnson, C. L. et al. Characteristics of Calanus finmarchicus dormancy patterns in the Northwest Atlantic. ICES J. Mar. Sci. 65, 339–350 (2008).
Google Scholar
Ji, R. B., Edwards, M., Mackas, D. L., Runge, J. A. & Thomas, A. C. Marine plankton phenology and life history in a changing climate: current research and future directions. J. Plankton Res. 32, 1355–1368 (2010).
Google Scholar
Weydmann, A., Walczowski, W., Carstensen, J. & Kwaśniewski, S. Warming of Subarctic waters accelerates development of a key marine zooplankton Calanus finmarchicus. Glob. Change Biol. 24, 172–183 (2018).
Google Scholar
Niehoff, B., Madsen, S., Hansen, B. & Nielsen, T. Reproductive cycles of three dominant Calanus species in Disko Bay, West Greenland. Mar. Biol. 140, 567–576 (2002).
Google Scholar
Meise, C. J. & O’Reilly, J. E. Spatial and seasonal patterns in abundance and age-composition of Calanus finmarchicus in the Gulf of Maine and on Georges Bank: 1977–1987. Deep-Sea Res. II 43, 1473–1501 (1996).
Google Scholar
Fiksen, Ø. The adaptive timing of diapause–a search for evolutionarily robust strategies in Calanus finmarchicus. ICES J. Mar. Sci. 57, 1825–1833 (2000).
Google Scholar
Miller, C. B., Crain, J. A. & Morgan, C. A. Oil storage variability in Calanus finmarchicus. ICES J. Mar. Sci. 57, 1786–1799 (2000).
Google Scholar
Miller, C. B., Cowles, T. J., Wiebe, P. H., Copley, N. J. & Grigg, H. Phenology in Calanus finmarchicus – Hypotheses about control mechanisms. Mar. Ecol. Prog. Ser. 72, 79–91 (1991).
Google Scholar
Speirs, D. C. et al. Ocean-scale modelling of the distribution, abundance, and seasonal dynamics of the copepod Calanus finmarchicus. Mar. Ecol. Prog. Ser. 313, 173–192 (2006).
Google Scholar
Tarrant, A. M. et al. Transcriptional profiling of metabolic transitions during development and diapause preparation in the copepod Calanus finmarchicus. Integr. Comp. Biol. 56, 1157–1169 (2016).
Google Scholar
Baumgartner, M. F. & Tarrant, A. M. The physiology and ecology of diapause in marine copepods. Annu. Rev. Mar. Sci. 9, 387–411 (2017).
Google Scholar
Wilson, R. J., Banas, N. S., Heath, M. R. & Speirs, D. C. Projected impacts of 21st century climate change on diapause in Calanus finmarchicus. Glob. Change Biol. 22, 3332–3340 (2016).
Google Scholar
Jónasdóttir, S. H., Visser, A. W., Richardson, K. & Heath, M. R. Seasonal copepod lipid pump promotes carbon sequestration in the deep North Atlantic. Proc. Natl Acad. Sci. USA. 112, 12122–12126 (2015).
Google Scholar
Jónasdóttir, S. H., Wilson, R. J., Gislason, A. & Heath, M. R. Lipid content in overwintering Calanus finmarchicus across the Subpolar Eastern North Atlantic Ocean. Limnol. Oceanogr. 64, 2029–2043 (2019).
Google Scholar
Varpe, Ø. Fitness and phenology: annual routines and zooplankton adaptations to seasonal cycles. J. Plankton Res. 34, 267–276 (2012).
Google Scholar
Denlinger, D. L., Yocum, G. D. & Rinehart, J. P. in Insect Endocrinology (ed Gilbert, L. I.) 430–463 (Academic Press, 2012).
Hirche, H. J. Diapause in the marine copepod, Calanus finmarchicus – a review. Ophelia 44, 129–143 (1996).
Google Scholar
Häfker, N. S. et al. Calanus finmarchicus seasonal cycle and diapause in relation to gene expression, physiology, and endogenous clocks. Limnol. Oceanogr. 63, 2815–2838 (2018).
Google Scholar
Roncalli, V. et al. Physiological characterization of the emergence from diapause: a transcriptomics approach. Sci. Rep. 8, 12577 (2018).
Google Scholar
Roncalli, V., Cieslak, M. C., Hopcroft, R. R. & Lenz, P. H. Capital breeding in a diapausing copepod: a transcriptomics analysis. Front. Mar. Sci. 7, 56 (2020).
Google Scholar
MacRae, T. H. Gene expression, metabolic regulation and stress tolerance during diapause. Cell. Mol. Life Sci. 67, 2405–2424 (2010).
Google Scholar
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 (2013).
Ragland, G. J. & Keep, E. Comparative transcriptomics support evolutionary convergence of diapause responses across Insecta. Physiol. Entomol. 42, 246–256 (2017).
Google Scholar
Koštál, V. Eco-physiological phases of insect diapause. J. Insect Physiol. 52, 113–127 (2006).
Google Scholar
Tarrant, A. M. et al. Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus. Front. Zool. 11, 1 (2014).
Google Scholar
Jensen, L. K. et al. A multi-generation Calanus finmarchicus culturing system for use in long-term oil exposure experiments. J. Exp. Mar. Biol. Ecol. 333, 71–78 (2006).
Google Scholar
Cieslak, M. C., Castelfranco, A. M., Roncalli, V., Lenz, P. H. & Hartline, D. K. t-Distributed Stochastic Neighbor Embedding (t-SNE): a tool for eco-physiological transcriptomic analysis. Mar. Genomics 51, 100723 (2020).
Google Scholar
van der Maaten, L. & Hinton, G. Visualizing data using t-SNE. J. Mach. Learn. Res. 9, 2579–2605 (2008).
Roncalli, V., Cieslak, M. C., Germano, M., Hopcroft, R. R. & Lenz, P. H. Regional heterogeneity impacts gene expression in the sub-arctic zooplankter Neocalanus flemingeri in the northern Gulf of Alaska. Commun. Biol. 2, 1–13 (2019).
Google Scholar
Johnson, K. M., Wong, J. M., Hoshijima, U., Sugano, C. S. & Hofmann, G. E. Seasonal transcriptomes of the Antarctic pteropod Limacina helicina antarctica. Mar. Env. Res. 143, 49–59 (2019).
Google Scholar
Denlinger, D. L. Regulation of diapause. Annu. Rev. Entomol. 47, 93–122 (2002).
Google Scholar
Denlinger, D. L. & Armbruster, P. A. Mosquito diapause. Annu. Rev. Entomol. 59, 73–93 (2014).
Google Scholar
Hahn, D. A. & Denlinger, D. L. Energetics of insect diapause. Annu. Rev. Entomol. 56, 103–121 (2011).
Google Scholar
Sim, C. & Denlinger, D. L. Transcription profiling and regulation of fat metabolism genes in diapausing adults of the mosquito Culex pipiens. Physiol. Genomics 39, 202–209 (2009).
Google Scholar
Sim, C. & Denlinger, D. L. Insulin signaling and the regulation of insect diapause. Front. Physiol. 4, 189 (2013).
Andrews, T. S. & Hemberg, M. Identifying cell populations with scRNASeq. Mol. Asp. Med. 59, 114–122 (2018).
Google Scholar
Habib, N. et al. Div-Seq: single-nucleus RNA-Seq reveals dynamics of rare adult newborn neurons. Science 353, 925–928 (2016).
Google Scholar
Arrese, E. L. & Soulages, J. L. Insect fat body: energy, metabolism, and regulation. Annu. Rev. Entomol. 55, 207–225 (2010).
Google Scholar
Hahn, D. A. & Denlinger, D. L. Meeting the energetic demands of insect diapause: nutrient storage and utilization. J. Insect Physiol. 53, 760–773 (2007).
Google Scholar
Lee, R. F., Hagen, W. & Kattner, G. Lipid storage in marine zooplankton. Mar. Ecol. Prog. Ser. 307, 273–306 (2006).
Google Scholar
Kattner, G. & Hagen, W. Polar herbivorous copepods–different pathways in lipid biosynthesis. ICES J. Mar. Sci. 52, 329–335 (1995).
Google Scholar
Miller, C. B., Morgan, C. A., Prahl, F. G. & Sparrow, M. A. Storage lipids of the copepod Calanus finmarchicus from Georges Bank and the Gulf of Maine. Limnol. Oceanogr. 43, 488–497 (1998).
Google Scholar
Hirche, H. J. & Niehoff, B. Reproduction of the Arctic copepod Calanus hyperboreus in the Greenland Sea-field and laboratory observations. Pol. Biol. 16, 209–219 (1996).
Google Scholar
Niehoff, B. & Hirche, H.-J. Oogenesis and gonad maturation in the copepod Calanus finmarchicus and the prediction of egg production from preserved samples. Pol. Biol. 16, 601–612 (1996).
Google Scholar
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).
Google Scholar
Aruda, A. M., Baumgartner, M. F., Reitzel, A. M. & Tarrant, A. M. Heat shock protein expression during stress and diapause in the marine copepod Calanus finmarchicus. J. Insect Physiol. 57, 665–675 (2011).
Google Scholar
Unal, E., Bucklin, A., Lenz, P. H. & Towle, D. W. Gene expression of the marine copepod Calanus finmarchicus: responses to small-scale environmental variation in the Gulf of Maine (NW Atlantic Ocean). J. Exp. Mar. Biol. Ecol. 446, 76–85 (2013).
Google Scholar
Ning, J., Wang, M. X., Li, C. L. & Sun, S. Transcriptome sequencing and de novo analysis of the copepod Calanus sinicus using 454 GS FLX. PLoS ONE 8, e63741 (2013).
Google Scholar
Zhang, Q., Lu, Y.-X. & Xu, W.-H. Proteomic and metabolomic profiles of larval hemolymph associated with diapause in the cotton bollworm, Helicoverpa armigera. BMC Genomics 14, 751 (2013).
Google Scholar
Hansen, M. et al. A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. PLoS Genet. 4, e24 (2008).
Qiu, Z. & MacRae, T. H. ArHsp21, a developmentally regulated small heat-shock protein synthesized in diapausing embryos of Artemia franciscana. Biochem. J. 411, 605–611 (2008).
Google Scholar
Lu, M.-X. et al. Diapause, signal and molecular characteristics of overwintering Chilo suppressalis (Insecta: Lepidoptera: Pyralidae). Sci. Rep. 3, 1–9 (2013).
Google Scholar
Forreryd, A., Johansson, H., Albrekt, A.-S. & Lindstedt, M. Evaluation of high throughput gene expression platforms using a genomic biomarker signature for prediction of skin sensitization. BMC Genomics 15, 379 (2014).
Google Scholar
Lenz, P. H. et al. De novo assembly of a transcriptome for Calanus finmarchicus (Crustacea, Copepoda)–the dominant zooplankter of the North Atlantic Ocean. PLoS ONE 9, e88589 (2014).
Google Scholar
Roncalli, V., Cieslak, M. C. & Lenz, P. H. Transcriptomic responses of the calanoid copepod Calanus finmarchicus to the saxitoxin producing dinoflagellate Alexandrium fundyense. Sci. Rep. 6, 25708 (2016).
Google Scholar
Roncalli, V., Cieslak, M. C. & Lenz, P. H. Data from: Transcriptomic responses of the calanoid copepod Calanus finmarchicus to the saxitoxin producing dinoflagellate Alexandrium fundyense. Dryad, Dataset (2016).
Choquet, M. et al. Genetics redraws pelagic biogeography of Calanus. Biol. Lett. 13, 20170588 (2017).
Google Scholar
Choquet, M. et al. Can morphology reliably distinguish between the copepods Calanus finmarchicus and C. glacialis, or is DNA the only way? Limnol. Oceanogr.: Methods 16, 237–252 (2018).
Google Scholar
Skottene, E. et al. A crude awakening: effects of crude oil on lipid metabolism in calanoid copepods terminating diapause. Biol. Bull. 237, 90–110 (2019).
Google Scholar
Melle, W. & Skjoldal, H. R. Reproduction and development of Calanus finmarchicus, C. glacialis and C. hyperboreus in the Barents Sea. Mar. Ecol. Prog. Ser. 169, 211–228 (1998).
Google Scholar
Weydmann, A. et al. Mitochondrial genomes of the key zooplankton copepods Arctic Calanus glacialis and North Atlantic Calanus finmarchicus with the longest crustacean non-coding regions. Sci. Rep. 7, 1–11 (2017).
Google Scholar
Lenz, P. H., Lieberman, B., Cieslak, M. C., Roncalli, V. & Hartline, D. K. Transcriptomics and metatranscriptomics in zooplankton: wave of the future? J. Plankton Res. 43, 3–9 (2021).
Google Scholar
Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. https://doi.org/10.1186/Gb-2009-10-3-R25 (2009).
Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621 (2008).
Google Scholar
van der Maaten, L. Accelerating t-SNE using tree-based algorithms. J. Mach. Learn. Res. 15, 3221–3245 (2014).
Krijthe, J. H. Rtsne: t-Distributed Stochastic Neighbor Embedding using a Barnes-Hut implementation, version 0.13. (2015).
Ester, M., Kriegel, H.-P., Sander, J. & Xu, X. A density-based algorithm for discovering clusters in large spatial databases with noise. Proc. Second International Conference on Knowledge Discovery and Data Mining (KDD-96) 96, 226–231 (1996).
Dunn, J. C. Well-separated clusters and optimal fuzzy partitions. J. Cybern. 4, 95–104 (1974).
Google Scholar
Hahsler, M. & Piekenbrock, M. Dbscan: density based clustering of applications with noise (DBSCAN) and related algorithms. R. package version 1, 1–3 (2018).
Desgraupes, B. ClusterCrit: Clustering Indices. R package version 1.2.8. (2018).
Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).
Google Scholar
Langfelder, P. & Horvath, S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinforma. 9, 559 (2008).
Google Scholar
Zhang, B. & Horvath, S. A general framework for weighted gene co-expression network analysis. Stat. Appl. Genet. Mol. 4, 17 (2005).
Supek, F., Bošnjak, M., Škunca, N. & Šmuc, T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6, e21800 (2011).
Google Scholar
Alexa, A. & Rahnenfuhrer, J. topGO: enrichment analysis for gene ontology. R. package version 2, 2010 (2010).
Galili, T., O’Callaghan, A., Sidi, J. & Sievert, C. heatmaply: an R package for creating interactive cluster heatmaps for online publishing. Bioinformatics 34, 1600–1602 (2018).
Google Scholar
Lenz, P. H. et al. Diapause vs. reproductive programs: transcriptional phenotypes in Calanus finmarchicus. Dryad, Dataset, https://doi.org/10.5061/dryad.12jm63xw7 (2021).
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