Molecular physiology of copepods - from biomarkers to transcriptomes and back again

Ann M. Tarrant1, Birgitte Nilsson2, Benni Winding Hansen2
1Biology Department, Woods Hole Oceanographic Institution, 45 Water Street, Woods Hole, MA 02544, USA
2Department of Science and Environment, Roskilde University, Universitetsvej 1, Roskilde, Denmark

Tài liệu tham khảo

Aaen, 2015, Drug resistance in sea lice: a threat to salmonid aquaculture, Trends Parasitol., 31, 72, 10.1016/j.pt.2014.12.006 Aguilera, 2016, Adaptive variability to low-pH river discharges in Acartia tonsa and stress responses to high pCO2 conditions, Mar. Ecol., 37, 215, 10.1111/maec.12282 Almada, A.A., Tarrant, A.M., 2016. Vibrio colonists elicit targeted transcriptional responses from copepod hosts. FEMS Microbiol. Ecol. 92, fiw072. Amato, A., and Carotenuto, Y., 2018. Planktonic calanoids embark into the 'omics' era. In: Trends in Copepod Studies - Distribution, Biology and Ecology, edited by M. Uttieri. New York: Nova Science Publishers, Inc. pp 287-314. ISBN: 978-1 53612-593-1. Anders, 2010, Differential expression analysis for sequence count data, Genome Biol., 11, R106, 10.1186/gb-2010-11-10-r106 Andersen, 2004, Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets, Cancer Res., 64, 5245, 10.1158/0008-5472.CAN-04-0496 Aruda, 2011, Heat shock protein expression during stress and diapause in the marine copepod Calanus finmarchicus, J. Insect Physiol., 57, 665, 10.1016/j.jinsphys.2011.03.007 Asai, 2015, High-quality RNA extraction from copepods for Next Generation Sequencing: a comparative study, Mar. Genom., 24, 115, 10.1016/j.margen.2014.12.004 Avery, 2005, Induction of embryonic dormancy in the calanoid copepod Acartia hudsonica: heritability and phenotypic plasticity in two geographically separated populations, J. Exp. Mar. Biol. Ecol., 314, 215, 10.1016/j.jembe.2004.09.005 Bailey, 2017, Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO2-acidified sea water, Ecol. Evol., 7, 7145, 10.1002/ece3.3063 Barreto, 2014, Hybrid dysfunction and physiological compensation in gene expression, Mol. Biol. Evol., 32, 613, 10.1093/molbev/msu321 Barreto, 2015, Reverse genetics in the tide pool: knock-down of target gene expression via RNA interference in the copepod Tigriopus californicus, Mol. Ecol. Res., 15, 868, 10.1111/1755-0998.12359 Barreto, 2018, Genomic signatures of mitonuclear coevolution across populations of Tigriopus californicus, Nature Ecol. Evol., 2, 1250, 10.1038/s41559-018-0588-1 Barrett, 2013, NCBI GEO: archive for functional genomics data sets—update, Nucl. Acids Research., 41, D991, 10.1093/nar/gks1193 Bersanelli, 2016, Methods for the integration of multi-omics data: mathematical aspects, BMC Bioinformatics, 17, S15, 10.1186/s12859-015-0857-9 Borchel, 2018, Systematic identification and characterization of stress-inducible heat shock proteins (HSPs) in the salmon louse (Lepeophtheirus salmonis), Cell Stress Chaperones, 23, 127, 10.1007/s12192-017-0830-9 Boxshall, 2008, Global diversity of copepods (Crustacea: Copepoda) in freshwater, Hydrobiologia, 595, 195, 10.1007/s10750-007-9014-4 Bray, 2016, Near-optimal probabilistic RNA-seq quantification, Nat. Biotechnol., 34, 525, 10.1038/nbt.3519 Brazma, 2001, Minimum information about a microarray experiment (MIAME)—toward standards for microarray data, Nat. Genet., 29, 365, 10.1038/ng1201-365 Bron, 2011, Observing copepods through a genomic lens, Front. Zool., 8, 22, 10.1186/1742-9994-8-22 Carnielli, 2015, Functional annotation and biological interpretation of proteomics data, Biochimica et Biophysica Acta -Proteins Proteomics, 1854, 46, 10.1016/j.bbapap.2014.10.019 Carotenuto, 2014, Insights into the transcriptome of the marine copepod Calanus helgolandicus feeding on the oxylipin-producing diatom Skeletonema marinoi, Harmful Algae, 31, 153, 10.1016/j.hal.2013.11.002 Chan, 2014, Identifying the gene (s) that allow Tigriopus californicus to survive under thermal stress, Can. Young Sci. J., 2014, 18 Chen, 2011, Cryptic diversity and comparative phylogeography of the estuarine copepod Acartia tonsa on the US Atlantic coast, Mol. Ecol., 20, 2425, 10.1111/j.1365-294X.2011.05079.x Chervoneva, 2010, Selection of optimal reference genes for normalization in quantitative RT-PCR, BMC Bioinformatics, 11, 253, 10.1186/1471-2105-11-253 Ching, 2014, Power analysis and sample size estimation for RNA-Seq differential expression, RNA, 20, 1, 10.1261/rna.046011.114 Choquet, 2017, Genetics redraws pelagic biogeography of Calanus, Biol. Lett., 13, 20170588, 10.1098/rsbl.2017.0588 Choquet, 2018, Can morphology reliably distinguish between the copepods Calanus finmarchicus and C. glacialis, or is DNA the only way? Limnol. Oceanogr, Methods, 16, 237 Christie, 2013, Peptidergic signaling in Calanus finmarchicus (Crustacea, Copepoda): in silico identification of putative peptide hormones and their receptors using a de novo assembled transcriptome, Gen. Comp. Endocrinol., 187, 117, 10.1016/j.ygcen.2013.03.018 Christie, 2016, Diversity of insulin-like peptide signaling system proteins in Calanus finmarchicus (Crustacea; Copepoda)–possible contributors to seasonal pre-adult diapause, Gen. Comp. Endocrinol., 236, 157, 10.1016/j.ygcen.2016.07.016 Conesa, 2016, A survey of best practices for RNA-seq data analysis, Genome Biol., 17, 13, 10.1186/s13059-016-0881-8 Cournoyer, B.L., 2013. Can Acartia spp. adapt to global warming? Heritable Within-Population Genetic Variation in Life History Traits. M.S. Thesis, University of Connecticut, 48 pp. Dalvin, 2011, Characterisation of two vitellogenins in the salmon louse Lepeophtheirus salmonis: molecular, functional and evolutional analysis, Dis. Aquat. Org., 94, 211, 10.3354/dao02331 Das, 2016, Analysis of annotation and differential expression methods used in RNA-Seq studies in crustacean systems, Integr. Comp. Biol., 56, 1067, 10.1093/icb/icw117 De Wit, 2016, Selection on oxidative phosphorylation and ribosomal structure as a multigenerational response to ocean acidification in the common copepod Pseudocalanus acuspes, Evol. App., 9, 1112, 10.1111/eva.12335 DeBiasse, 2018, Phenotypic and transcriptomic responses to salinity stress across genetically and geographically divergent Tigriopus californicus populations, Mol. Ecol., 27, 1621, 10.1111/mec.14547 Dheda, 2005, The implications of using an inappropriate reference gene for real-time reverse transcription PCR data normalization, Anal. Biochem., 344, 141, 10.1016/j.ab.2005.05.022 Dohle, 2001, Are the insects terrestrial crustaceans? A discussion of some new facts and arguments and the proposal of the proper name 'Tetraconata' for the monophyletic unit Crustacea+ Hexapoda, J Ann. Soc. Entomol. Fr., 37, 85 Drillet, 2011, Status and recommendations on marine copepod cultivation for use as live feed, Aquaculture, 315, 155, 10.1016/j.aquaculture.2011.02.027 Eichner, 2008, Salmon louse (Lepeophtheirus salmonis) transcriptomes during post molting maturation and egg production, revealed using EST-sequencing and microarray analysis, BMC Genomics, 9, 126, 10.1186/1471-2164-9-126 Eichner, 2015, Characterization of a novel RXR receptor in the salmon louse (Lepeophtheirus salmonis, Copepoda) regulating growth and female reproduction, BMC Genomics, 16, 81, 10.1186/s12864-015-1277-y Eyun, 2017, Evolutionary history of chemosensory-related gene families across the Arthropoda, Mol. Biol. Evol., 34, 1838, 10.1093/molbev/msx147 Foley, 2019, Sex-specific stress tolerance, proteolysis, and lifespan in the invertebrate Tigriopus californicus, Exp. Gerontol., 119, 146, 10.1016/j.exger.2019.02.006 Francis, 2013, A comparison across non-model animals suggests an optimal sequencing depth for de novo transcriptome assembly, BMC Genomics, 14, 1, 10.1186/1471-2164-14-167 Fuess, 2018, Transcriptional analyses provide new insight into the late-stage immune response of a diseased Caribbean coral, R. Soc. Open Sci., 5, 172062, 10.1098/rsos.172062 Golestan Hashemi, 2018, Intelligent mining of large-scale bio-data: bioinformatics applications, Biotechnol. Biotechnol. Equip., 32, 10, 10.1080/13102818.2017.1364977 Grishanin, 2014, Chromatin diminution in Copepoda (Crustacea): pattern, biological role and evolutionary aspects, Comp. Cytogenetics, 8, 1, 10.3897/compcytogen.v8i1.5913 Haas, 2013, De novo transcript sequence reconstruction from RNA-seq using the trinity platform for reference generation and analysis, Nat. Protoc., 8, 1494, 10.1038/nprot.2013.084 Hairston, 1996, Zooplankton egg banks as biotic reservoirs in changing environments, Limnol. Oceanogr., 41, 1087, 10.4319/lo.1996.41.5.1087 Han, 2015, Identification of the full 46 cytochrome P450 (CYP) complement and modulation of CYP expression in response to water-accommodated fractions of crude oil in the cyclopoid copepod Paracyclopina nana, Environ. Sci. Technol., 49, 6982, 10.1021/acs.est.5b01244 Han, 2015, Developmental retardation, reduced fecundity, and modulated expression of the defensome in the intertidal copepod Tigriopus japonicus exposed to BDE-47 and PFOS, Aquat. Toxicol., 165, 136, 10.1016/j.aquatox.2015.05.022 Hansen, 2007, Suppression subtractive hybridization library prepared from the copepod Calanus finmarchicus exposed to a sublethal mixture of environmental stressors, Comp. Biochem. Physiol. D: Genom. Proteom., 2, 250 Hansen, 2008, Effects of naphthalene on gene transcription in Calanus finmarchicus (Crustacea: Copepoda), Aquat. Toxicol., 86, 157, 10.1016/j.aquatox.2007.10.009 Hansen, 2009, Gene expression of GST and CYP330A1 in lipid-rich and lipid-poor female Calanus finmarchicus (Copepoda: Crustacea) exposed to dispersed oil. J. Toxicol. Environ, Health Part A, 72, 131 Hansen, 2010, Molecular effects of diethanolamine exposure on Calanus finmarchicus (Crustacea: Copepoda), Aquat. Toxicol., 99, 212, 10.1016/j.aquatox.2010.04.018 Hansen, 2011, Comparative study on acute effects of water accommodated fractions of an artificially weathered crude oil on Calanus finmarchicus and Calanus glacialis (Crustacea: Copepoda), Sci. Total Environ., 409, 704, 10.1016/j.scitotenv.2010.10.035 Hansen, 2016, Acute toxicity of dispersed crude oil on the cold-water copepod Calanus finmarchicus: elusive implications of lipid content. J. Toxicol. Environ, Health Part A, 79, 549 Hassett, 2010, Gene expression and biochemical studies of the marine copepod Calanus finmarchicus, MDI Biol. Lab. Bull., 49, 115 Holm, 2017, Resting eggs in free living marine and estuarine copepods, J. Plankton Res., 40, 2, 10.1093/plankt/fbx062 Hook, 2014, The role of biomarkers in the assessment of aquatic ecosystem health, Integr. Environ. Assess. Manage., 10, 327, 10.1002/ieam.1530 Huggett, 2005, Real-time RT-PCR normalisation; strategies and considerations, Genes Immun., 6, 279, 10.1038/sj.gene.6364190 Hwang, 2009, Cloning and expression of vitellogenin 2 gene from the intertidal copepod Tigriopus japonicus, Annals New York Acad. Sci., 1163, 417, 10.1111/j.1749-6632.2008.03631.x Hwang, 2010, Modulation of p53 gene expression in the intertidal copepod Tigriopus japonicus exposed to alkylphenols, Mar. Environ. Res., 69, S77, 10.1016/j.marenvres.2009.12.002 Hwang, 2010, Molecular characterization and expression of vitellogenin (Vg) genes from the cyclopoid copepod, Paracyclopina nana exposed to heavy metals, Comp. Biochem. Physiol. C: Pharmacol. Toxicol. Endocrinol., 151, 360 Hwang, 2016, BDE-47 causes developmental retardation with down-regulated expression profiles of ecdysteroid signaling pathway-involved nuclear receptor (NR) genes in the copepod Tigriopus japonicus, Aquat. Toxicol., 177, 285, 10.1016/j.aquatox.2016.06.004 Iqbal, 2012, De novo assembly and genotyping of variants using colored de Bruijn graphs, Nat. Genet., 44, 226, 10.1038/ng.1028 Jager, 2016, Stage-dependent and sex-dependent sensitivity to water-soluble fractions of fresh and weathered oil in the marine copepod Calanus finmarchicus, Environ. Toxicol. Chem., 35, 728, 10.1002/etc.3237 Jensen, 2016, Individual and molecular level effects of produced water contaminants on nauplii and adult females of Calanus finmarchicus. J. Toxicol. Environ, Health Part A, 79, 585 Jeong, 2014, Functional characterization of P-glycoprotein in the intertidal copepod Tigriopus japonicus and its potential role in remediating metal pollution, Aquat. Toxicol., 156, 135, 10.1016/j.aquatox.2014.08.005 Jeong, 2015, Identification and molecular characterization of dorsal and dorsal-like genes in the cyclopoid copepod Paracyclopina nana, Mar. Genom., 24, 319, 10.1016/j.margen.2015.08.002 Jeong, 2016, Identification and molecular characterization of nitric oxide synthase (NOS) gene in the intertidal copepod Tigriopus japonicus, Gene, 577, 47, 10.1016/j.gene.2015.11.019 Jiang, 2013, Differential gene expression profile of the calanoid copepod, Pseudodiaptomus annandalei, in response to nickel exposure, Comp. Biochem. Physiol. C: Toxicol. Physiol., 157, 203 Johnson, 2011, Taxonomically restricted genes are associated with the evolution of sociality in the honey bee, BMC Genomics, 12, 164, 10.1186/1471-2164-12-164 Johnson, 2019, Seasonal transcriptomes of the Antarctic pteropod, Limacina helicina antarctica, Mar. Environ. Res., 143, 49, 10.1016/j.marenvres.2018.10.006 Jónasdóttir, 2015, Seasonal copepod lipid pump promotes carbon sequestration in the deep North Atlantic, Proc Nat Acad Sci, 112, 12122, 10.1073/pnas.1512110112 Jørgensen, 2019, G3 Jørgensen, 2019, The genome and transcriptome of the cosmopolitan calanoid copepod Acartia tonsa Dana expand the understanding of copepod genome size evolution. Manuscript in revision, submitted to Genome Biol, Evol. Kang, S., Ahn, D.H., Lee, J.H., Lee, S.G., Shin, S.C., Lee, J., Min, G.S., Lee, H., Kim, H.W., Kim, S., Park, H., 2017. The genome of the Antarctic-endemic copepod, Tigriopus kingsejongensis. Gigascience, 6, giw010. Kelly, 2017, Adaptation to heat stress reduces phenotypic and transcriptional plasticity in a marine copepod, Funct. Ecol., 31, 398, 10.1111/1365-2435.12725 Ki, 2009, Gene expression profiling of copper-induced responses in the intertidal copepod Tigriopus japonicus using a 6K oligochip microarray, Aquat. Toxicol., 93, 177, 10.1016/j.aquatox.2009.04.004 Kim, 2011, Cu/Zn-and Mn-superoxide dismutase (SOD) from the copepod Tigriopus japonicus: molecular cloning and expression in response to environmental pollutants, Chemosphere, 84, 1467, 10.1016/j.chemosphere.2011.04.043 Kim, 2013, Expression profile analysis of antioxidative stress and developmental pathway genes in the manganese-exposed intertidal copepod Tigriopus japonicus with 6K oligochip, Chemosphere, 92, 1214, 10.1016/j.chemosphere.2013.04.047 Kim, 2013, Role of crustacean hyperglycemic hormone (CHH) in the environmental stressor-exposed intertidal copepod Tigriopus japonicus, Comp. Biochem. Physiol. C: Toxicol. Physiol., 158, 131 Kim, 2014, Heavy metals induce oxidative stress and trigger oxidative stress-mediated heat shock protein (hsp) modulation in the intertidal copepod Tigriopus japonicus, Comp. Biochem. Physiol. C: Toxicol. Physiol., 166, 65 Kim, 2015, Identification of the retinoblastoma (Rb) gene and expression in response to environmental stressors in the intertidal copepod Tigriopus japonicus, Mar. Genom., 24, 387, 10.1016/j.margen.2015.09.008 Kim, 2015, Identification of xenobiotic biodegradation and metabolism-related genes in the copepod Tigriopus japonicus whole transcriptome analysis, Mar. Genom., 24, 207, 10.1016/j.margen.2015.05.011 Kim, 2016, De novo assembly and annotation of the Antarctic copepod (Tigriopus kingsejongensis) transcriptome, Mar. Genom., 28, 37, 10.1016/j.margen.2016.04.009 Knapen, 2009, Best practices for hybridization design in two-colour microarray analysis, Trends Biotechnol., 27, 406, 10.1016/j.tibtech.2009.03.007 Kozera, 2013, Reference genes in real-time PCR, J. Appl. Genet., 54, 391, 10.1007/s13353-013-0173-x Kregel, 2002, Invited review: heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance, J. Appl. Physiol., 92, 2177, 10.1152/japplphysiol.01267.2001 Kurihara, 2008, Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates, Mar. Ecol. Prog. Ser., 373, 275, 10.3354/meps07802 Lanneau, 2010, Heat shock proteins: cell protection through protein triage, Sci. World J., 10, 1543, 10.1100/tsw.2010.152 Lauritano, 2011, First molecular evidence of diatom effects in the copepod Calanus helgolandicus, J. Exp. Mar. Biol. Ecol., 404, 79, 10.1016/j.jembe.2011.05.009 Lauritano, 2011, Molecular evidence of the toxic effects of diatom diets on gene expression patterns in copepods, PLoS One, 6, 10.1371/journal.pone.0026850 Lauritano, 2012, Gene expression patterns and stress response in marine copepods, Mar. Environ. Res., 76, 22, 10.1016/j.marenvres.2011.09.015 Lauritano, 2013, Changes in expression of stress genes in copepods feeding upon a non-brevetoxin-producing strain of the dinoflagellate Karenia brevis, Harmful Algae, 28, 23, 10.1016/j.hal.2013.05.004 Lauritano, 2015, Effects of the oxylipin-producing diatom Skeletonema marinoi on gene expression levels of the calanoid copepod Calanus sinicus, Mar. Genom., 24, 89, 10.1016/j.margen.2015.01.007 Lauritano, 2016, New oxylipins produced at the end of a diatom bloom and their effects on copepod reproductive success and gene expression levels, Harmful Algae, 55, 221, 10.1016/j.hal.2016.03.015 Lee, 2006, Cloning and characterization of glutathione S-transferase gene in the intertidal copepod Tigriopus japonicus and its expression after exposure to endocrine-disrupting chemicals, Mar. Environ. Res., 62, S219, 10.1016/j.marenvres.2006.04.050 Lee, 2007, Sequence, biochemical characteristics and expression of a novel Sigma-class of glutathione S-transferase from the intertidal copepod, Tigriopus japonicus with a possible role in antioxidant defense, Chemosphere, 69, 893, 10.1016/j.chemosphere.2007.05.087 Lee, 2008, Molecular cloning, phylogenetic analysis and developmental expression of a vitellogenin (vg) gene from the intertidal copepod Tigriopus japonicus, Comp. Biochem. Physiol. B: Biochem. Mol. Biol., 150, 395, 10.1016/j.cbpb.2008.04.009 Lee, 2008, Expression of glutathione S-transferase (GST) genes in the marine copepod Tigriopus japonicus exposed to trace metals, Aquat. Toxicol., 89, 158, 10.1016/j.aquatox.2008.06.011 Lee, 2008, A corticotropin-releasing hormone binding protein (CRH-BP) gene from the intertidal copepod, Tigriopus japonicus, Gen. Comp. Endocrinol., 158, 54, 10.1016/j.ygcen.2008.05.002 Lee, 2010, The copepod Tigriopus japonicus genomic DNA information (574 Mb) and molecular anatomy, Mar. Environ. Res., 69, S21, 10.1016/j.marenvres.2009.12.003 Lee, 2011, Pumping ions: rapid parallel evolution of ionic regulation following habitat invasions, Evolution, 65, 2229, 10.1111/j.1558-5646.2011.01308.x Lee, 2012, Effect of culture density and antioxidants on naupliar production and gene expression of the cyclopoid copepod, Paracyclopina nana, Comp. Biochem. Physiol. A Mol. Integr. Physiol., 161, 145, 10.1016/j.cbpa.2011.10.019 Lee, 2015, RNA-seq based whole transcriptome analysis of the cyclopoid copepod Paracyclopina nana focusing on xenobiotics metabolism, Comp. Biochem. Physiol. D: Genom. Proteom., 15, 12 Lee, 2016, BDE-47 induces oxidative stress, activates MAPK signaling pathway, and elevates de novo lipogenesis in the copepod Paracyclopina nana, Aquat. Toxicol., 181, 104, 10.1016/j.aquatox.2016.10.025 Lee, 2017, Adverse effects of methylmercury (MeHg) on life parameters, antioxidant systems, and MAPK signaling pathways in the copepod Tigriopus japonicus, Aquat. Toxicol., 184, 133, 10.1016/j.aquatox.2017.01.010 Legrand, 2016, Transcriptome analysis of the copepod Eurytemora affinis upon exposure to endocrine disruptor pesticides: focus on reproduction and development, Aquat. Toxicol., 176, 64, 10.1016/j.aquatox.2016.04.010 Lenz, 2012, Functional genomics resources for the North Atlantic copepod, Calanus finmarchicus: EST database and physiological microarray, Comp. Biochem. Physiol. D: Genom. Proteom., 7, 110 Lenz, 2014, De novo assembly of a transcriptome for Calanus finmarchicus (Crustacea, Copepoda) - the dominant zooplanker of the North Atlantic Ocean, PLoS One, 9, 10.1371/journal.pone.0088589 Lespinet, 2002, The role of lineage-specific gene family expansion in the evolution of eukaryotes, Genome Res., 12, 1048, 10.1101/gr.174302 Li, 2014, Evaluation of de novo transcriptome assemblies from RNA-Seq data, Genome Biol., 15, 553, 10.1186/s13059-014-0553-5 Lima, 2017, Locally adapted populations of a copepod can evolve different gene expression patterns under the same environmental pressures, Ecol. Evol., 7, 4312, 10.1002/ece3.3016 Liu, 2013, RNA-seq differential expression studies: more sequence or more replication?, Bioinformatics, 30, 301, 10.1093/bioinformatics/btt688 Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2(-DDC(T)) method, Methods, 25, 402, 10.1006/meth.2001.1262 Lotufo, 1997, Effects of sediment-associated phenanthrene on survival, development and reproduction of two species of meiobenthic copepods, Mar. Ecol. Prog. Ser., 151, 91, 10.3354/meps151091 Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biol., 15, 550, 10.1186/s13059-014-0550-8 Maas, 2018, Variations in copepod proteome and respiration rate in association with diel vertical migration and circadian cycle, Biol. Bull., 235, 30, 10.1086/699219 MacManes, 2016, Establishing evidenced-based best practice for the de novo assembly and evaluation of transcriptomes from non-model organisms. bioRxiv Madoui, 2017, New insights into global biogeography, population structure and natural selection from the genome of the epipelagic copepod Oithona, Mol. Ecol., 26, 4467, 10.1111/mec.14214 Marcus, 1994, Age, viability, and vertical distribution of zooplankton resting eggs from an anoxic basin: evidence of an egg bank, Limnol. Oceanogr., 39, 154, 10.4319/lo.1994.39.1.0154 McCarthy, 2015, ‘Degraded’ RNA profiles in Arthropoda and beyond, PeerJ, 3, 10.7717/peerj.1436 Milligan, 2011, Phylogeography of the copepod Acartia hudsonica in estuaries of the northeastern United States, Hydrobiologia, 666, 155, 10.1007/s10750-010-0097-y Moreton, 2016, Assembly, assessment, and availability of de novo generated eukaryotic transcriptomes, Front. Genet., 6, 361, 10.3389/fgene.2015.00361 Moya, 2012, Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO2-driven acidification during the initiation of calcification, Mol. Ecol., 21, 2440, 10.1111/j.1365-294X.2012.05554.x Mykles, 2016, Resources and recommendations for using transcriptomics to address grand challenges in comparative biology, Integr. Comp. Biol., 56, 1183, 10.1093/icb/icw083 Nguyen, 2018, Guidelines for RNA-seq projects: applications and opportunities in non-model decapod crustacean species, Hydrobiologia, 1 Nielsen, 2017, The importance of live-feed traps–farming marine fish species, Aquac. Res., 48, 2623, 10.1111/are.13281 Nilsson, B., 2018. Molecular Stress Physiology in the Calanoid Copepod Acartia tonsa. PhD Dissertation, Roskilde University, 148 pp. Nilsson, 2018, Timing of embryonic quiescence determines viability of embryos from the calanoid copepod, Acartia tonsa (Dana), PLoS One, 13, 10.1371/journal.pone.0193727 Nilsson, 2014, Expression of hsp70 and ferritin in embryos of the copepod Acartia tonsa (Dana) during transition between subitaneous and quiescent state, J. Plankton Res., 36, 513, 10.1093/plankt/fbt099 Nilsson, 2017, Copepod swimming behavior, respiration, and expression of stress-related genes in response to high stocking densities, Aquacult. Rep., 6, 35, 10.1016/j.aqrep.2017.03.001 Nilsson, 2018, Environmental stress responses and experimental handling artifacts of a model organism, the copepod Acartia tonsa (Dana), Front. Mar. Sci., 5, 156, 10.3389/fmars.2018.00156 Núñez-Acuña, 2016, In-feed additives modulate ionotropic receptor genes from the sea louse Caligus rogercresseyi: a comparative analysis in two host salmonid species, Aquaculture, 451, 99, 10.1016/j.aquaculture.2015.09.001 Oakley, 2012, Phylotranscriptomics to bring the understudied into the fold: monophyletic Ostracoda, fossil placement, and pancrustacean phylogeny, Mol. Biol. Evol., 30, 215, 10.1093/molbev/mss216 Oliver, 2000, Proteomics: guilt-by-association goes global, Nature, 403, 601, 10.1038/35001165 Orsini, 2018, Early transcriptional response pathways in Daphnia magna are coordinated in networks of crustacean-specific genes, Mol. Ecol., 27, 886, 10.1111/mec.14261 Papatheodorou, 2017, Expression Atlas: gene and protein expression across multiple studies and organisms, Nucleic Acids Res., 46, D246, 10.1093/nar/gkx1158 Park, 2017, Effects of triclosan (TCS) on fecundity, the antioxidant system, and oxidative stress-mediated gene expression in the copepod Tigriopus japonicus, Aquat. Toxicol., 189, 16, 10.1016/j.aquatox.2017.05.012 Parrish, 1978, Fecundity studies on Acartia tonsa (Copepoda: Calanoida) in standardized culture, Mar. Biol., 46, 65, 10.1007/BF00393822 Paszkiewicz, 2010, De novo assembly of short sequence reads, Brief. Bioinform., 11, 457, 10.1093/bib/bbq020 Pereira, 2014, Ecological novelty by hybridization: experimental evidence for increased thermal tolerance by transgressive segregation in Tigriopus californicus, Evolution, 68, 204, 10.1111/evo.12254 Pereira, 2017, Adaptation to a latitudinal thermal gradient within a widespread copepod species: the contributions of genetic divergence and phenotypic plasticity. Proc. Royal Soc. London B: Biol. Sci., 284, 20170236 Perkins, 2012, ReadqPCR and NormqPCR: R packages for the reading, quality checking and normalisation of RT-qPCR quantification cycle (Cq) data, BMC Genomics, 13, 296, 10.1186/1471-2164-13-296 Petkeviciute, 2015, Genetic responses of the marine copepod Acartia tonsa (Dana) to heat shock and epibiont infestation, Aquacult. Rep., 2, 10, 10.1016/j.aqrep.2015.04.001 Pfaffl, 2001, A new mathematical model for relative quantification in real-time RT-PCR, Nucleic Acids Res., 29, 10.1093/nar/29.9.e45 Pfaffl, 2004, Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper–Excel-based tool using pair-wise correlations, Biotechnol. Lett., 26, 509, 10.1023/B:BILE.0000019559.84305.47 Pimentel, 2016, The Lair: a resource for exploratory analysis of published RNA-Seq data, BMC Bioinformatics, 17, 490, 10.1186/s12859-016-1357-2 Poley, 2015, Towards a consensus: multiple experiments provide evidence for constitutive expression differences among sexes and populations of sea lice (Lepeophtheirus salmonis) related to emamectin benzoate resistance, Aquaculture, 448, 445, 10.1016/j.aquaculture.2015.06.026 Porter, 2017, Molecular characterization of copepod photoreception, Biol. Bull., 233, 96, 10.1086/694564 Puthumana, 2017, Ecdysone receptor (EcR) and ultraspiracle (USP) genes from the cyclopoid copepod Paracyclopina nana: identification and expression in response to water accommodated fractions (WAFs), Comp. Biochem. Physiol. C: Toxicol. Physiol., 192, 7 Rahlff, 2017, Short-term molecular and physiological responses to heat stress in neritic copepods Acartia tonsa and Eurytemora affinis, Comp. Biochem. Physiol. A Mol. Integr. Physiol., 203, 348, 10.1016/j.cbpa.2016.11.001 Ramos, 2015, A transcriptome resource for the copepod Calanus glacialis across a range of culture temperatures, Mar. Genomics, 23, 27, 10.1016/j.margen.2015.03.014 Regier, 2005, Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic, Proc. Royal Soc. London B: Biol. Sci., 272, 395 Regier, 2010, Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences, Nature, 463, 1079, 10.1038/nature08742 Rhee, 2009, Heat shock protein (Hsp) gene responses of the intertidal copepod Tigriopus japonicus to environmental toxicants, Comp. Biochem. Physiol. C: Toxicol. Pharmacol., 149, 104 Rhee, 2012, Expression pattern analysis of DNA repair-related and DNA damage response genes revealed by 55 K oligomicroarray upon UV-B irradiation in the intertidal copepod, Tigriopus japonicus, Comp. Biochem. Physiol. C: Toxicol. Pharmacol., 155, 359 Rhee, 2013, Copper induces apoptotic cell death through reactive oxygen species-triggered oxidative stress in the intertidal copepod Tigriopus japonicus, Aquat. Toxicol., 132, 182, 10.1016/j.aquatox.2013.02.013 Rhee, 2015, β-Naphthoflavone induces oxidative stress in the intertidal copepod, Tigriopus japonicus, Environ. Toxicol., 30, 332, 10.1002/tox.21911 Riemer, 2012, Identification and validation of reference genes for expression studies in human keratinocyte cell lines treated with and without interferon-γ–a method for qRT-PCR reference gene determination, Exp. Dermatology, 21, 625, 10.1111/j.1600-0625.2012.01537.x Ritchie, 2015, limma powers differential expression analyses for RNA-sequencing and microarray studies, Nucleic Acids Res., 43, e47, 10.1093/nar/gkv007 Robinson, 2010, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616 Roncalli, 2016, Transcriptomic responses of the calanoid copepod Calanus finmarchicus to the saxitoxin producing dinoflagellate Alexandrium fundyense, Sci. Rep., 6, 25708, 10.1038/srep25708 Roncalli, 2016, Glutathione S-transferase regulation in Calanus finmarchicus feeding on the toxic dinoflagellate Alexandrium fundyense, PLoS One, 11, 10.1371/journal.pone.0159563 Roncalli, 2017, A deep transcriptomic resource for the copepod crustacean Labidocera madurae: a potential indicator species for assessing near shore ecosystem health, PLoS One, 12, 10.1371/journal.pone.0186794 Roncalli, 2017, Complementary mechanisms for neurotoxin resistance in a copepod, Sci. Rep., 7, 14201, 10.1038/s41598-017-14545-z Roncalli, 2018, De novo transcriptome assembly of the calanoid copepod Neocalanus flemingeri: a new resource for emergence from diapause, Mar. Genom., 37, 114, 10.1016/j.margen.2017.09.002 Roncalli, 2018, Physiological characterization of the emergence from diapause: a transcriptomics approach, Sci. Rep., 8, 12577, 10.1038/s41598-018-30873-0 Rota-Stabelli, 2012, Serine codon-usage bias in deep phylogenomics: pancrustacean relationships as a case study, Syst. Biol., 62, 121, 10.1093/sysbio/sys077 Ruijter, 2009, Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data, Nucleic Acids Res., 37, e45, 10.1093/nar/gkp045 Saiz, 2009, Lethal and sublethal effects of naphthalene and 1, 2-dimethylnaphthalene on naupliar and adult stages of the marine cyclopoid copepod Oithona davisae, Environ. Pollut., 157, 1219, 10.1016/j.envpol.2008.12.011 Schiffer, 2014, Temperature tolerance of different larval stages of the spider crab Hyas araneus exposed to elevated seawater pCO2, Front. Zool., 11, 87, 10.1186/s12983-014-0087-4 Schlötterer, 2015, Genes from scratch–the evolutionary fate of de novo genes, Trends Genet., 31, 215, 10.1016/j.tig.2015.02.007 Schoville, 2012, Investigating the molecular basis of local adaptation to thermal stress: population differences in gene expression across the transcriptome of the copepod Tigriopus californicus, BMC Evol. Biol., 12, 170, 10.1186/1471-2148-12-170 Semmouria, 2019, The transcriptome of the marine calanoid copepod Temora longicornis under heat stress and recovery, Mar. Environ. Res., 143, 10, 10.1016/j.marenvres.2018.10.017 Seo, 2006, Small heat shock protein 20 gene (Hsp20) of the intertidal copepod Tigriopus japonicus as a possible biomarker for exposure to endocrine disruptors, Bull. Environ. Contam. Toxicol., 76, 10.1007/s00128-006-0957-3 Seo, 2006, Environmental stressors (salinity, heavy metals, H2O2) modulate expression of glutathione reductase (GR) gene from the intertidal copepod Tigriopus japonicus, Aquat. Toxicol., 80, 281, 10.1016/j.aquatox.2006.09.005 Seo, 2006, The intertidal copepod Tigriopus japonicus small heat shock protein 20 gene (Hsp20) enhances thermotolerance of transformed Escherichia coli, Biochem. Biophys. Res. Comm., 340, 901, 10.1016/j.bbrc.2005.12.086 Sherr, 2016, 3 Shi, 2008, Reproducible and reliable microarray results through quality control: good laboratory proficiency and appropriate data analysis practices are essential, Curr. Opin. Biotechnol., 19, 10, 10.1016/j.copbio.2007.11.003 Simão, 2015, BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs, Bioinformatics, 31, 3210, 10.1093/bioinformatics/btv351 Smit, 2009, Relating biomarkers to whole-organism effects using species sensitivity distributions: a pilot study for marine species exposed to oil, Environ. Toxicol. Chem., 28, 1104, 10.1897/08-464.1 Smith-Unna, 2016, TransRate: reference-free quality assessment of de novo transcriptome assemblies, Genome Res., 26, 1134, 10.1101/gr.196469.115 Smolina, 2015, Contrasting transcriptome response to thermal stress in two key zooplankton species Calanus finmarchicus and C. glacialis, Mar. Ecol. Prog. Ser., 534, 79, 10.3354/meps11398 Steinberg, 2017, Zooplankton and the ocean carbon cycle, Annu. Rev. Mar. Sci., 9, 413, 10.1146/annurev-marine-010814-015924 Storch, 2011, Thermal tolerance of larval stages of the Chilean kelp crab Taliepus dentatus, Mar. Ecol. Prog. Ser., 429, 157, 10.3354/meps09059 Sutherland, 2012, Transcriptomics of coping strategies in free-swimming Lepeophtheirus salmonis (Copepoda) larvae responding to abiotic stress, Mol. Ecol., 21, 6000, 10.1111/mec.12072 Svingen, 2015, Selection of reference genes for quantitative RT-PCR (RT-qPCR) analysis of rat tissues under physiological and toxicological conditions, PeerJ, 3, 10.7717/peerj.855 Tangwancharoen, 2014, Early life stages are not always the most sensitive: heat stress responses in the copepod Tigriopus californicus, Mar. Ecol. Prog. Ser., 517, 75, 10.3354/meps11013 Tangwancharoen, 2018, Multiple modes of adaptation: regulatory and structural evolution in a small heat shock protein gene, Mol. Biol. Evol., 35, 2110, 10.1093/molbev/msy138 Tarrant, 2008, Differential gene expression in diapausing and active Calanus finmarchicus (Copepoda), Mar. Ecol. Prog. Ser., 355, 193, 10.3354/meps07207 Tarrant, 2014, Transcriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus, Front. Zool., 11, 91, 10.1186/s12983-014-0091-8 Todd, 2016, The power and promise of RNA-seq in ecology and evolution, Mol. Ecol., 25, 1224, 10.1111/mec.13526 Toxværd, 2018, Impact of pyrene exposure during overwintering of the Arctic copepod Calanus glacialis, Environ. Sci. Technol., 52, 10328, 10.1021/acs.est.8b03327 Tribble, 2007, Evidence for changes in the transcription levels of two putative P-glycoprotein genes in sea lice (Lepeophtheirus salmonis) in response to emamectin benzoate exposure, Mol. Biochem. Parasitol., 153, 10.1016/j.molbiopara.2007.02.002 Tröße, 2014, RNA interference mediated knockdown of the KDEL receptor and COPB2 inhibits digestion and reproduction in the parasitic copepod Lepeophtheirus salmonis, Comp. Biochem. Physiol. B: Biochem. Mol. Biol., 170, 1, 10.1016/j.cbpb.2013.12.006 Turner, 2004, The importance of small planktonic copepods and their roles in pelagic marine food webs, Zool. Stud., 43, 255 Unal, 2013, 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, 10.1016/j.jembe.2013.04.020 VanderLugt, 2009, Cultivation of the paracalanid copepod, Bestiolina similis (Calanoida: Crustacea), J. World Aquacult. Soc., 40, 616, 10.1111/j.1749-7345.2009.00282.x Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., Speleman, F., 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, RESEARCH0034. Voznesensky, 2004, Genomic approaches to detecting thermal stress in Calanus finmarchicus (Copepoda: Calanoida), J. Exp. Mar. Biol. Ecol., 311, 37, 10.1016/j.jembe.2004.04.017 Vu, 2017, The constraints of high density production of the calanoid copepod Acartia tonsa Dana, J. Plankton Res., 39, 1028, 10.1093/plankt/fbx056 Walsh, 2007, Identification of cDNAs induced by the organophosphate trichlorphon in the parasitic copepod Lepeophtheirus salmonis (Copepoda; Caligidae), Pestic. Biochem. Physiol., 88, 26, 10.1016/j.pestbp.2006.08.008 Walter, T.C., Boxshall, G., 2019. World of copepods database. Accessed at http://www.marinespecies.org/copepoda on 2019-01-31. Weaver, 2016, Copper exposure reduces production of red carotenoids in a marine copepod, Ecol. Indic., 70, 393, 10.1016/j.ecolind.2016.06.040 Willett, 2002, Proline biosynthesis genes and their regulation under salinity stress in the euryhaline copepod Tigriopus californicus. Comp. Biochem.Physiol.B: Biochem, Mol. Biol., 132, 739 Willett, 2003, Characterization of the glutamate dehydrogenase gene and its regulation in a euryhaline copepod, Comp. Biochem. Physiol. B: Biochem. Mol. Biol., 135, 639, 10.1016/S1096-4959(03)00145-3 Xuereb, 2012, Molecular characterization and mRNA expression of grp78 and hsp90A in the estuarine copepod Eurytemora affinis, Cell Stress Chaperones, 17, 457, 10.1007/s12192-012-0323-9 Yi, 2014, Ecotoxicity of triphenyltin on the marine copepod Tigriopus japonicus at various biological organisations: from molecular to population-level effects, Ecotoxicology, 23, 1314, 10.1007/s10646-014-1274-y Zhang, 2013, An improved method for achieving high-quality RNA for copepod transcriptomic studies, J. Exp. Mar. Biol. Ecol., 446, 57, 10.1016/j.jembe.2013.04.021 Zhang, 2014, A circadian gene expression atlas in mammals: implications for biology and medicine, Proc. Nat. Acad. Sci., 111, 16219, 10.1073/pnas.1408886111 Zhou, 2015, Genome-wide identification of lineage-specific genes within Caenorhabditis elegans, Genomics, 106, 242, 10.1016/j.ygeno.2015.07.002 Zhou, 2016, Effects of elevated temperature and food supply on the termination of over-summering and subsequent development of the calanoid copepod Calanus sinicus: morphology, physiology and gene expression, PLoS One, 11 Zhou, 2018, De novo transcriptome assembly and differential gene expression analysis of the calanoid copepod Acartia tonsa exposed to nickel nanoparticles, Chemosphere, 209, 163, 10.1016/j.chemosphere.2018.06.096 Zhuang, 2017, Spliced leader-based analyses reveal the effects of polycyclic aromatic hydrocarbons on gene expression in the copepod Pseudodiaptomus poplesia, Aquat. Toxicol., 183, 114, 10.1016/j.aquatox.2016.12.014 Zöllner, 2009, Effect of zooplankton-mediated trophic cascades on marine microbial food web components (bacteria, nanoflagellates, ciliates), Limnol. Oceanogr., 54, 262, 10.4319/lo.2009.54.1.0262