Fluctuating thermal regimes prevent chill injury but do not change patterns of oxidative stress in the alfalfa leafcutting bee, Megachile rotundata

Aurori, 2014, What is the main driver of ageing in long-lived winter honeybees: antioxidant enzymes, innate immunity, or vitellogenin?, J. Gerontol. Ser. A, Biol. Sci. Med. Sci., 69, 633, 10.1093/gerona/glt134 Bayley, 2018, Cold exposure causes cell death by depolarization-mediated Ca2+ overload in a chill-susceptible insect, Proceedings of the National Academy of Sciences, USA, 115, E9737, 10.1073/pnas.1813532115 Bennett, 2015, Exposure to suboptimal temperatures during metamorphosis reveals a critical developmental window in the solitary bee, Megachile rotundata, Physiol. Biochem. Zool., 88, 508, 10.1086/682024 Chen, 2016, Molecular identification and expression patterns of apolipoprotein d from Bombyx mori (Lepidoptera: Bombycidae) in response to oxidative stress and bacterial challenge, Ann. Entomol. Soc. Am., 109, 759, 10.1093/aesa/saw035 Colinet, 2006, The impact of fluctuating thermal regimes on the survival of a cold-exposed parasitic wasp, Aphidius colemani, Physiol. Entomol., 31, 234, 10.1111/j.1365-3032.2006.00511.x Colinet, 2015, Insects in fluctuating thermal environments, Annu. Rev. Entomol., 60, 123, 10.1146/annurev-ento-010814-021017 Corona, 2007, Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity, Proceedings of the National Academy of Sciences, USA, 104, 7128, 10.1073/pnas.0701909104 2008, Proc. R. Soc. B, 275, 781, 10.1098/rspb.2007.1515 Gironella, 2009, P8/nupr1 regulates DNA-repair activity after double-strand gamma irradiation-induced DNA damage, J. Cell. Physiol., 221, 594, 10.1002/jcp.21889 Goruppi, 2010, Stress-inducible protein p8 is involved in several physiological and pathological processes, J. Biol. Chem., 285, 1577, 10.1074/jbc.R109.080887 Grumiaux, 2019, Fluctuating thermal regime preserves physiological homeostasis and reproductive capacity in drosophila suzukii, J. Insect Physiol., 113, 33, 10.1016/j.jinsphys.2019.01.001 Haddadi, 2014, Brain aging, memory impairment and oxidative stress: a study in Drosophila melanogaster, Behav. Brain Res., 259, 60, 10.1016/j.bbr.2013.10.036 Havukainen, 2013, Vitellogenin recognizes cell damage through membrane binding and shields living cells from reactive oxygen species, J. Biol. Chem., 288, 28369, 10.1074/jbc.M113.465021 Hayward, 2014, Molecular basis of chill resistance adaptations in poikilothermic animals, J. Exp. Biol., 217, 6, 10.1242/jeb.096537 Hochachka, 1998, Integrating metabolic pathway fluxes with gene-to-enzyme expression rates, Comparative Biochem. Physiol. B-Biochem. Mol. Biol., 120, 17, 10.1016/S0305-0491(98)00019-4 Hori, 2000, A novel hemocyte-specific membrane protein of Sarcophaga (flesh fly), Eur. J. Biochem., 267, 5397, 10.1046/j.1432-1327.2000.01578.x Ihle, 2015, Genotype effect on lifespan following vitellogenin knockdown, Exp. Gerontol., 61, 113, 10.1016/j.exger.2014.12.007 Imlay, 2003, Pathways of oxidative damage, Annu. Rev. Microbiol., 57, 395, 10.1146/annurev.micro.57.030502.090938 Jin, 2009, Nuclear protein 1 induced by ATF4 in response to various stressors acts as a positive regulator on the transcriptional activation of ATF4, International Union of Biochemistry and Molecular Biology, 61, 1153, 10.1002/iub.271 Joanisse, 1996, Oxidative stress and antioxidants in overwintering larvae of cold-hardy goldenrod gall insects, J. Exp. Biol., 199, 1483, 10.1242/jeb.199.7.1483 Joanisse, 1998, Oxidative stress and antioxidants in stress and recovery of cold-hardy insects, Insect Biochem. Mol. Biol., 28, 23, 10.1016/S0965-1748(97)00070-2 Kocks, 2005, Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila, Cell, 123, 335, 10.1016/j.cell.2005.08.034 Koštál, 2007, Insect cold tolerance and repair of chill-injury at fluctuating thermal regimes: Role of ion homeostasis, Comp. Biochem. Physiol. A: Mol. Integr. Physiol., 147, 231, 10.1016/j.cbpa.2006.12.033 Koštál, 2006, Chilling-injury and disturbance of ion homeostasis in the coxal muscle of the tropical cockroach (Nauphoeta cinerea), Comp. Biochem. Physiol. B: Biochem. Mol. Biol., 143, 171, 10.1016/j.cbpb.2005.11.005 Lalouette, 2011, Metabolic rate and oxidative stress in insects exposed to low temperature thermal fluctuations, Comp. Biochem. Physiol. A: Mol. Integr. Physiol., 158, 229, 10.1016/j.cbpa.2010.11.007 Lee, 2010, A primer on insect cold tolerance, 3 Li-Byarlay, 2016, Honey bee (Apis mellifera) drones survive oxidative stress due to increased tolerance instead of avoidance or repair of oxidative damage, Exp. Gerontol., 83, 15, 10.1016/j.exger.2016.07.003 López-Martínez, 2008, High resistance to oxidative damage in the antarctic midge Belgica antarctica, and developmentally linked expression of genes encoding superoxide dismutase, catalase and heat shock proteins, Insect Biochem. Mol. Biol., 38, 796, 10.1016/j.ibmb.2008.05.006 López-Martínez, 2012, Short-term anoxic conditioning hormesis boosts antioxidant defenses, lowers oxidative damage following irradiation and enhances male sexual performance in the Caribbean fruit fly, Anastrepha suspensa, J. Exp. Biol., 215, 2150, 10.1242/jeb.065631 Maier, 2009, Correlation of mRNA and protein in complex biological samples, FEBS Lett., 583, 3966, 10.1016/j.febslet.2009.10.036 Melicher, 2019, Immediate transcriptional response to a temperature pulse under a fluctuating thermal regime, Integr. Comp. Biol., 1 Monaghan, 2009, Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation, Ecol. Lett., 12, 75, 10.1111/j.1461-0248.2008.01258.x Overgaard, 2017, The integrative physiology of insect chill tolerance, Annu. Rev. Physiol., 79, 187, 10.1146/annurev-physiol-022516-034142 Renault, 2004, The importance of fluctuating thermal regimes for repairing chill injuries in the tropical beetle Alphitobius diaperinus (Coleoptera : Tenebrionidae) during exposure to low temperature, Physiol. Entomol., 29, 139, 10.1111/j.0307-6962.2004.00377.x Reynolds, 2013, Natural variation for lifespan and stress response in the nematode Caenorhabditis remanei, PLoS ONE, 8, 10.1371/journal.pone.0058212 Rinehart, 2013, A fluctuating thermal regime improves long-term survival of quiescent prepupal Megachile rotundata (Hymenoptera: Megachilidae), J. Econ. Entomol., 106, 1081, 10.1603/EC12486 Rojas, 1996, Chilling injury in the housefly: Evidence for the role of oxidative stress between pupariation and emergence, Cryobiology, 33, 447, 10.1006/cryo.1996.0045 Salmela, 2016, Ancient duplications have led to functional divergence of vitellogenin-like genes potentially involved in inflammation and oxidative stress in honey bees, Genome Biol. Evol., 8, 495, 10.1093/gbe/evw014 Sanchez, 2006, Loss of Glial Lazarillo, a homolog of Apolipoprotein D, reduces lifespan and stress resistance in Drosophila, Curr. Biol., 16, 680, 10.1016/j.cub.2006.03.024 Sun, 2015, Immune-relevant and antioxidant activities of vitellogenin and yolk proteins in fish, Nutrients, 7, 8818, 10.3390/nu7105432 Torson, 2015, Transcriptional responses to fluctuating thermal regimes underpinning differences in survival in the solitary bee Megachile rotundata, J. Exp. Biol., 218, 1060, 10.1242/jeb.113829 Torson, 2017, Physiological responses to fluctuating temperatures are characterized by distinct transcriptional profiles in a solitary bee, J. Exp. Biol., 220, 3372, 10.1242/jeb.156695 Vandesompele, 2002, Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes, Genome Biol., 3, 10.1186/gb-2002-3-7-research0034 Walker, 2006, Overexpression of a Drosophila homolog of Apolipoprotein D leads to increased stress resistance and extended lifespan, Curr. Biol., 16, 674, 10.1016/j.cub.2006.01.057 Winston, 1960, Saturated solutions for the control of humidity in biological research, Ecology, 41, 232, 10.2307/1931961 Zhou, 2001, Ced-1 is a transmembrane receptor that mediates cell corpse engulfment in C. Elegans, Cell, 104, 43, 10.1016/S0092-8674(01)00190-8