1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Entomology
  4. Volume 68, 2023
  5. Article

Annual Review of Entomology

Volume 68, 2023

Molecular Mechanisms of Winter Survival

Abstract

Winter provides many challenges for insects, including direct injury to tissues and energy drain due to low food availability. As a result, the geographic distribution of many species is tightly coupled to their ability to survive winter. In this review, we summarize molecular processes associated with winter survival, with a particular focus on coping with cold injury and energetic challenges. Anticipatory processes such as cold acclimation and diapause cause wholesale transcriptional reorganization that increases cold resistance and promotes cryoprotectant production and energy storage. Molecular responses to low temperature are also dynamic and include signaling events during and after a cold stressor to prevent and repair cold injury. In addition, we highlight mechanisms that are subject to selection as insects evolve to variable winter conditions. Based on current knowledge, despite common threads, molecular mechanisms of winter survival vary considerably across species, and taxonomic biases must be addressed to fully appreciate the mechanistic basis of winter survival across the insect phylogeny.

Keyword(s): acclimation, cold tolerance, diapause, energetics, stress, winter
Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-120120-095233
2023-01-23
2024-05-08
Loading full text...

Full text loading...

/deliver/fulltext/ento/68/1/annurev-ento-120120-095233.html?itemId=/content/journals/10.1146/annurev-ento-120120-095233&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Addo-Bediako A, Chown SL, Gaston KJ. 2000. Thermal tolerance, climatic variability and latitude. Proc. R. Soc. B 267:739–45
     [Google Scholar]
  2. 2.
    Ahmadi F, Mikani A, Moharramipour S. 2021. Induction of diapause by clock proteins period and timeless via changes in PTTH and ecdysteroid titer in the sugar beet moth, Scrobipalpa ocellatella (Lepidoptera: Gelechiidae). Arch. Insect Biochem. Physiol. 107:e21790
     [Google Scholar]
  3. 3.
    Andersen JL, Manenti T, Sorensen JG, MacMillan HA, Loeschcke V, Overgaard J. 2015. How to assess Drosophila cold tolerance: Chill coma temperature and lower lethal temperature are the best predictors of cold distribution limits. Funct. Ecol. 29:55–65
     [Google Scholar]
  4. 4.
    Ayrinhac A, Debat V, Gibert P, Kister AG, Legout H et al. 2004. Cold adaptation in geographical populations of Drosophila melanogaster: Phenotypic plasticity is more important than genetic variability. Funct. Ecol. 18:700–6
     [Google Scholar]
  5. 5.
    Bayley JS, Winther CB, Andersen MK, Gronkjaer C, Nielsen OB et al. 2018. Cold exposure causes cell death by depolarization-mediated Ca2+ overload in a chill-susceptible insect. PNAS 115:E9737–44
     [Google Scholar]
  6. 6.
    Benoit JB 2010. Water management by dormant insects: comparisons between dehydration resistance during summer aestivation and winter diapause. Aestivation: Molecular and Physiological Aspects CA Navas, JE Carvalho 209–29 Berlin: Springer
     [Google Scholar]
  7. 7.
    Bewick AJ, Vogel KJ, Moore AJ, Schmitz RJ. 2017. Evolution of DNA methylation across insects. Mol. Biol. Evol. 34:654–65
     [Google Scholar]
  8. 8.
    Bing X, Zhang J, Sinclair BJ. 2012. A comparison of Frost expression among species and life stages of Drosophila. Insect Mol. Biol. 21:31–39
     [Google Scholar]
  9. 9.
    Box ICH, Matthews BJ, Marshall KE. 2022. Molecular evidence of intertidal habitats selecting for repeated ice-binding protein evolution in invertebrates. J. Exp. Biol. 225:jeb243409
     [Google Scholar]
  10. 10.
    Butterson S, Roe AD, Marshall KE. 2021. Plasticity of cold hardiness in the eastern spruce budworm, Choristoneura fumiferana. Comp. Biochem. Physiol. A 259:110998
     [Google Scholar]
  11. 11.
    Chaverra-Rodriguez D, Macias VM, Hughes GL, Pujhari S, Suzuki Y et al. 2018. Targeted delivery of CRISPR-Cas9 ribonucleoprotein into arthropod ovaries for heritable germline gene editing. Nat. Commun. 9:3008
     [Google Scholar]
  12. 12.
    Chen YR, Jiang T, Zhu J, Xie YC, Tan ZC et al. 2017. Transcriptome sequencing reveals potential mechanisms of diapause preparation in bivoltine silkworm Bombyx mori (Lepidoptera: Bombycidae). Comp. Biochem. Physiol. D 24:68–78
     [Google Scholar]
  13. 13.
    Chen Z, Dong Y, Wang Y, Andongma AA, Rashid MA et al. 2016. Pupal diapause termination in Bactrocera minax: an insight on 20-hydroxyecdysone induced phenotypic and genotypic expressions. Sci. Rep. 6:27440
     [Google Scholar]
  14. 14.
    Chowański S, Walkowiak-Nowicka K, Winkiel M, Marciniak P, Urbański A, Pacholska-Bogalska J. 2021. Insulin-like peptides and cross-talk with other factors in the regulation of insect metabolism. Front. Physiol. 12:701203
     [Google Scholar]
  15. 15.
    Chown SL, Gaston KJ. 2008. Macrophysiology for a changing world. Proc. R. Soc. B 275:1469–78
     [Google Scholar]
  16. 16.
    Clark MS, Worland MR. 2008. How insects survive the cold: molecular mechanisms—a review. J. Comp. Physiol. B 178:917–33
     [Google Scholar]
  17. 17.
    Colinet H, Hoffmann AA. 2012. Comparing phenotypic effects and molecular correlates of developmental, gradual and rapid cold acclimation responses in Drosophila melanogaster. Funct. Ecol. 26:84–93
     [Google Scholar]
  18. 18.
    Colinet H, Lee SF, Hoffmann A. 2010. Knocking down expression of Hsp22 and Hsp23 by RNA interference affects recovery from chill coma in Drosophila melanogaster. J. Exp. Biol. 213:4146–50
     [Google Scholar]
  19. 19.
    Colinet H, Rinehart JP, Yocum GD, Greenlee KJ. 2018. Mechanisms underpinning the beneficial effects of fluctuating thermal regimes in insect cold tolerance. J. Exp. Biol. 221:jeb164806
     [Google Scholar]
  20. 20.
    Cui WZ, Qiu JF, Dai TM, Chen Z, Li JL et al. 2021. Circadian clock gene period contributes to diapause via GABAeric-diapause hormone pathway in Bombyx mori. Biology 10:842
     [Google Scholar]
  21. 21.
    Dalla Benetta E, Beukeboom LW, van de Zande L 2019. Adaptive differences in circadian clock gene expression patterns and photoperiodic diapause induction in Nasonia vitripennis. Am. Nat. 193:881–96
     [Google Scholar]
  22. 22.
    Davis JR, Kirkland RL. 1982. Physiological and environmental factors related to the dispersal flight of the convergent lady beetle, Hippodamia convergens (Guerin-Meneville). J. Kans. Entomol. Soc. 55:187–96
     [Google Scholar]
  23. 23.
    Denlinger DL. 2022. Insect Diapause Cambridge, UK: Cambridge Univ. Press
  24. 24.
    Denlinger DL, Armbruster PA. 2014. Mosquito diapause. Annu. Rev. Entomol. 59:73–93
     [Google Scholar]
  25. 25.
    Denlinger DL, Yocum GD, Rinehart JP 2012. Hormonal control of diapause. Insect Endocrinology LI Gilbert 430–63 San Diego: Academic
     [Google Scholar]
  26. 26.
    Des Marteaux LE, Hůla P, Koštál V. 2019. Transcriptional analysis of insect extreme freeze tolerance. Proc. R. Soc. B 286:20192019
     [Google Scholar]
  27. 27.
    Des Marteaux LE, Khazraeenia S, Yerushalmi GY, Donini A, Li NG, Sinclair BJ. 2018. The effect of cold acclimation on active ion transport in cricket ionoregulatory tissues. Comp. Biochem. Physiol. A 216:28–33
     [Google Scholar]
  28. 28.
    Des Marteaux LE, McKinnon AH, Udaka H, Toxopeus J, Sinclair BJ 2017. Effects of cold-acclimation on gene expression in Fall field cricket (Gryllus pennsylvanicus) ionoregulatory tissues. BMC Genom. 18:357
     [Google Scholar]
  29. 29.
    Di Cara F, King-Jones K. 2016. The circadian clock is a key driver of steroid hormone production in Drosophila. Curr. Biol. 26:2469–77
     [Google Scholar]
  30. 30.
    Doucet D, Tyshenko MG, Davies PL, Walker VK. 2002. A family of expressed antifreeze protein genes from the moth, Choristoneura fumiferana. Eur. J. Biochem. 269:38–46
     [Google Scholar]
  31. 31.
    Dowle EJ, Powell THQ, Doellman MM, Meyers PJ, Calvert MB et al. 2020. Genome-wide variation and transcriptional changes in diverse developmental processes underlie the rapid evolution of seasonal adaptation. PNAS 117:23960–69
     [Google Scholar]
  32. 32.
    Duman JG, Walters KR, Sformo T, Carrasco MA, Nickell P, Barnes BM 2010. Antifreeze and ice nucleator proteins. Low Temperature Biology of Insects DL Denlinger, RE Lee 59–90 Cambridge, UK: Cambridge Univ. Press
     [Google Scholar]
  33. 33.
    Dunning LT, Dennis AB, Sinclair BJ, Newcomb RD, Buckley TR. 2014. Divergent transcriptional responses to low temperature among populations of alpine and lowland species of New Zealand stick insects (Micrarchus). Mol. Ecol. 23:2712–26
     [Google Scholar]
  34. 34.
    Durmaz E, Rajpurohit S, Betancourt N, Fabian DK, Kapun M et al. 2019. A clinal polymorphism in the insulin signaling transcription factor foxo contributes to life-history adaptation in Drosophila. Evolution 73:1774–92
     [Google Scholar]
  35. 35.
    Emerson KJ, Bradshaw WE, Holzapfel CM. 2009. Complications of complexity: integrating environmental, genetic and hormonal control of insect diapause. Trends Genet 25:217–25
     [Google Scholar]
  36. 36.
    Enriquez T, Colinet H. 2019. Cold acclimation triggers major transcriptional changes in Drosophila suzukii. BMC Genom 20:413
     [Google Scholar]
  37. 37.
    Erickson PA, Weller CA, Song DY, Bangerter AS, Schmidt P, Bergland AO. 2020. Unique genetic signatures of local adaptation over space and time for diapause, an ecologically relevant complex trait, in Drosophila melanogaster. PLOS Genet 16:e1009110
     [Google Scholar]
  38. 38.
    Feder JL, Filchak KE. 1999. It's about time: the evidence for host plant-mediated selection in the apple maggot fly, Rhagoletis pomonella, and its implications for fitness trade-offs in phytophagous insects. Entomol. Exp. Appl. 91:211–25
     [Google Scholar]
  39. 39.
    Feder ME, Hofmann GE. 1999. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61:243–82
     [Google Scholar]
  40. 40.
    Fujiwara Y, Denlinger DL. 2007. p38 MAPK is a likely component of the signal transduction pathway triggering rapid cold hardening in the flesh fly Sarcophaga crassipalpis. J. Exp. Biol. 210:3295–300
     [Google Scholar]
  41. 41.
    Garcia MJ, Littler AS, Sriram A, Teets NM. 2020. Distinct cold tolerance traits independently vary across genotypes in Drosophila melanogaster. Evolution 74:1437–50
     [Google Scholar]
  42. 42.
    Gerber L, Kresse J-C, Šimek P, Berková P, Overgaard J. 2021. Cold acclimation preserves hindgut reabsorption capacity at low temperature in a chill-susceptible insect, Locusta migratoria. Comp. Biochem. Physiol. A 252:110850
     [Google Scholar]
  43. 43.
    Gerken AR, Eller OC, Hahn DA, Morgan TJ. 2015. Constraints, independence, and evolution of thermal plasticity: probing genetic architecture of long- and short-term thermal acclimation. PNAS 112:4399–404
     [Google Scholar]
  44. 44.
    Hahn DA, Denlinger DL. 2011. Energetics of insect diapause. Annu. Rev. Entomol. 56:103–21
     [Google Scholar]
  45. 45.
    Hamanaka Y, Yasuyama K, Numata H, Shiga S. 2005. Synaptic connections between pigment-dispersing factor-immunoreactive neurons and neurons in the pars lateralis of the blow fly Protophormia terraenovae. J. Comp. Neurol. 491:390–99
     [Google Scholar]
  46. 46.
    Hand SC, Menze MA, Borcar A, Patil Y, Covi JA et al. 2011. Metabolic restructuring during energy-limited states: insights from Artemia franciscana embryos and other animals. J. Insect Physiol. 57:584–94
     [Google Scholar]
  47. 47.
    Hao K, Jarwar AR, Ullah H, Tu X, Nong X, Zhang Z. 2019. Transcriptome sequencing reveals potential mechanisms of the maternal effect on egg diapause induction of Locusta migratoria. Int. J. Mol. Sci. 20:1974
     [Google Scholar]
  48. 48.
    Hayward SAL, Manso B, Cossins AR. 2014. Molecular basis of chill resistance adaptations in poikilothermic animals. J. Exp. Biol. 217:6–15
     [Google Scholar]
  49. 49.
    Hazel JR. 1995. Thermal adaptation in biological membranes: Is homeoviscous adaptation the explanation?. Annu. Rev. Physiol. 57:19–42
     [Google Scholar]
  50. 50.
    Hoffmann AA. 2010. Physiological climatic limits in Drosophila: patterns and implications. J. Exp. Biol. 213:870–80
     [Google Scholar]
  51. 51.
    i5K Consort. 2013. The i5K Initiative: advancing arthropod genomics for knowledge, human health, agriculture, and the environment. J. Hered. 104:595–600
     [Google Scholar]
  52. 52.
    Iga M, Nakaoka T, Suzuki Y, Kataoka H. 2014. Pigment dispersing factor regulates ecdysone biosynthesis via bombyx neuropeptide G protein coupled receptor-B2 in the prothoracic glands of Bombyx mori. PLOS ONE 9:e103239
     [Google Scholar]
  53. 53.
    Ikeno T, Numata H, Goto SG. 2011. Circadian clock genes period and cycle regulate photoperiodic diapause in the bean bug Riptortus pedestris males. J. Insect Physiol. 57:935–38
     [Google Scholar]
  54. 54.
    Isabel G, Gourdoux L, Moreau R. 2001. Changes of biogenic amine levels in haemolymph during diapausing and non-diapausing status in Pieris brassicae L. Comp. Biochem. Physiol. A 128:117–27
     [Google Scholar]
  55. 55.
    Jakobs R, Gariepy TD, Sinclair BJ. 2015. Adult plasticity of cold tolerance in a continental-temperate population of Drosophila suzukii. J. Insect Physiol. 79:1–9
     [Google Scholar]
  56. 56.
    Jumper J, Evans R, Pritzel A, Green T, Figurnov M et al. 2021. Highly accurate protein structure prediction with AlphaFold. Nature 596:583–89
     [Google Scholar]
  57. 57.
    Kellermann V, Loeschcke V, Hoffmann AA, Kristensen TN, Flojgaard C et al. 2012. Phylogenetic contstraints in key functional traits behind species' climate niches: patterns of desiccation and cold resistance across 95 Drosophila species. Evolution 66:3377–89
     [Google Scholar]
  58. 58.
    Kenny MC, Giarra MN, Granata E, Socha JJ. 2018. How temperature influences the viscosity of hornworm hemolymph. J. Exp. Biol. 221:jeb186338
     [Google Scholar]
  59. 59.
    Kim M, Robich RM, Rinehart JP, Denlinger DL. 2006. Upregulation of two actin genes and redistribution of actin during diapause and cold stress in the northern house mosquito, Culex pipiens. J. Insect Physiol. 52:1226–33
     [Google Scholar]
  60. 60.
    King AM, MacRae TH. 2015. Insect heat shock proteins during stress and diapause. Annu. Rev. Entomol. 60:59–75
     [Google Scholar]
  61. 61.
    Knight CA, Duman JG. 1986. Inhibition of recrystallization of ice by insect thermal hysteresis proteins: a possible cryoprotective role. Cryobiology 23:256–62
     [Google Scholar]
  62. 62.
    Königer A, Arif S, Grath S. 2019. Three quantitative trait loci explain more than 60% of variation for chill coma recovery time in a natural population of Drosophila ananassae. G3 9:3715–25
     [Google Scholar]
  63. 63.
    Koštál V. 2006. Eco-physiological phases of insect diapause. J. Insect Physiol. 52:113–27
     [Google Scholar]
  64. 64.
    Koštál V. 2011. Insect photoperiodic calendar and circadian clock: independence, cooperation, or unity?. J. Insect Physiol. 57:538–56
     [Google Scholar]
  65. 65.
    Koštál V, Štětina T, Poupardin R, Korbelová J, Bruce AW. 2017. Conceptual framework of the eco-physiological phases of insect diapause development justified by transcriptomic profiling. PNAS 114:8532–37
     [Google Scholar]
  66. 66.
    Koubová J, Jehlík T, Kodrík D, Sábová M, Šima P et al. 2019. Telomerase activity is upregulated in the fat bodies of pre-diapause bumblebee queens (Bombus terrestris). Insect Biochem. Mol. Biol. 115:103241
     [Google Scholar]
  67. 67.
    Kozak GM, Wadsworth CB, Kahne SC, Bogdanowicz SM, Harrison RG et al. 2019. Genomic basis of circannual rhythm in the European corn borer moth. Curr. Biol. 29:3501–9.e5
     [Google Scholar]
  68. 68.
    Leal L, Talla V, Källman T, Friberg M, Wiklund C et al. 2018. Gene expression profiling across ontogenetic stages in the wood white (Leptidea sinapis) reveals pathways linked to butterfly diapause regulation. Mol. Ecol. 27:935–48
     [Google Scholar]
  69. 69.
    Lecheta MC, Awde DN, O'Leary TS, Unfried LN, Jacobs NA et al. 2020. Integrating GWAS and transcriptomics to identify the molecular underpinnings of thermal stress responses in Drosophila melanogaster. Front. Genet. 11:658
     [Google Scholar]
  70. 70.
    Lee RE, Denlinger DL. 1985. Cold tolerance in diapausing and non-diapausing stages of the flesh fly, Sarcophaga crassipalpis. Physiol. Entomol. 10:309–15
     [Google Scholar]
  71. 71.
    Lewin HA, Robinson GE, Kress WJ, Baker WJ, Coddington J et al. 2018. Earth BioGenome Project: sequencing life for the future of life. PNAS 115:4325–33
     [Google Scholar]
  72. 72.
    Li YN, Ren XB, Liu ZC, Ye B, Zhao ZJ et al. 2021. Insulin-like peptide and FoxO mediate the trehalose catabolism enhancement during the diapause termination period in the Chinese oak silkworm (Antheraea pernyi). Insects 12:784
     [Google Scholar]
  73. 73.
    Lubawy J, Urbański A, Colinet H, Pflüger H-J, Marciniak P. 2020. Role of the insect neuroendocrine system in the response to cold stress. Front. Physiol. 11:376
     [Google Scholar]
  74. 74.
    Lumley LM, Pouliot E, Laroche J, Boyle B, Brunet BMT et al. 2020. Continent-wide population genomic structure and phylogeography of North America's most destructive conifer defoliator, the spruce budworm (Choristoneura fumiferana). Ecol. Evol. 10:914–27
     [Google Scholar]
  75. 75.
    MacMillan HA, Knee JM, Dennis AB, Udaka H, Marshall KE et al. 2016. Cold acclimation wholly reorganizes the Drosophila melanogaster transcriptome and metabolome. Sci. Rep. 6:28999
     [Google Scholar]
  76. 76.
    Maino JL, Kong JD, Hoffmann AA, Barton MG, Kearney MR. 2016. Mechanistic models for predicting insect responses to climate change. Curr. Opin. Insect Sci. 17:81–86
     [Google Scholar]
  77. 77.
    Marshall KE, Gotthard K, Williams CM. 2020. Evolutionary impacts of winter climate change on insects. Curr. Opin. Insect Sci. 41:54–62
     [Google Scholar]
  78. 78.
    Marshall KE, Sinclair BJ. 2012. Threshold temperatures mediate the impact of reduced snow cover on overwintering freeze-tolerant caterpillars. Naturwissenschaften 99:33–41
     [Google Scholar]
  79. 79.
    Marshall KE, Sinclair BJ. 2015. The relative importance of number, duration and intensity of cold stress events in determining survival and energetics of an overwintering insect. Funct. Ecol. 29:357–66
     [Google Scholar]
  80. 80.
    Marshall KE, Thomas RH, Roxin Á, Chen EKY, Brown JCL et al. 2014. Seasonal accumulation of acetylated triacylglycerols by a freeze-tolerant insect. J. Exp. Biol. 217:1580–87
     [Google Scholar]
  81. 81.
    Matthews BJ, Vosshall LB. 2020. How to turn an organism into a model organism in 10 “easy” steps. J. Exp. Biol. 223:jeb218198
     [Google Scholar]
  82. 82.
    Meuti ME, Denlinger DL. 2013. Evolutionary links between circadian clocks and photoperiodic diapause in insects. Integr. Comp. Biol. 53:131–43
     [Google Scholar]
  83. 83.
    Meuti ME, Stone M, Ikeno T, Denlinger DL. 2015. Functional circadian clock genes are essential for the overwintering diapause of the Northern house mosquito, Culex pipiens. J. Exp. Biol. 218:412–22
     [Google Scholar]
  84. 84.
    Michaud MR, Denlinger DL. 2004. Molecular modalities of insect cold survival: current understanding and future trends. Int. Congr. Ser. 1275:32–46
     [Google Scholar]
  85. 85.
    Mohamed AA, Wang Q, Bembenek J, Ichihara N, Hiragaki S et al. 2014. N-acetyltransferase (nat) is a critical conjunct of photoperiodism between the circadian system and endocrine axis in Antheraea pernyi. PLOS ONE 9:e92680
     [Google Scholar]
  86. 86.
    Morimoto RI. 1998. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12:3788–96
     [Google Scholar]
  87. 87.
    Nagy D, Cusumano P, Andreatta G, Anduaga AM, Hermann-Luibl C et al. 2019. Peptidergic signaling from clock neurons regulates reproductive dormancy in Drosophila melanogaster. PLOS Genet 15:e1008158
     [Google Scholar]
  88. 88.
    Nässel DR, Kubrak OI, Liu Y, Luo J, Lushchak OV. 2013. Factors that regulate insulin producing cells and their output in Drosophila. Front. Physiol. 4:252
     [Google Scholar]
  89. 89.
    Newman CE, Toxopeus J, Udaka H, Ahn S, Martynowicz DM et al. 2017. CRISPR-induced null alleles show that Frost protects Drosophila melanogaster reproduction after cold exposure. J. Exp. Biol. 220:3344–54
     [Google Scholar]
  90. 90.
    Olademehin OP, Liu C, Rimal B, Adegboyega NF, Chen F et al. 2020. Dsi-RNA knockdown of genes regulated by Foxo reduces glycogen and lipid accumulations in diapausing Culex pipiens. Sci. Rep. 10:17201
     [Google Scholar]
  91. 91.
    Overgaard J, MacMillan HA. 2017. The integrative physiology of insect chill tolerance. Annu. Rev. Physiol. 79:187–208
     [Google Scholar]
  92. 92.
    Park Y, Kim Y. 2013. RNA interference of glycerol biosynthesis suppresses rapid cold hardening of the beet armyworm, Spodoptera exigua. J. Exp. Biol. 216:4196–203
     [Google Scholar]
  93. 93.
    Pegoraro M, Gesto JS, Kyriacou CP, Tauber E. 2014. Role for circadian clock genes in seasonal timing: testing the Bünning hypothesis. PLOS Genet. 10:e1004603
     [Google Scholar]
  94. 94.
    Pimsler ML, Oyen KJ, Herndon JD, Jackson JM, Strange JP et al. 2020. Biogeographic parallels in thermal tolerance and gene expression variation under temperature stress in a widespread bumble bee. Sci. Rep. 10:17063
     [Google Scholar]
  95. 95.
    Poelchau MF, Reynolds JA, Elsik CG, Denlinger DL, Armbruster PA. 2013. Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus. Proc. R. Soc. B 280:20130143
     [Google Scholar]
  96. 96.
    Pool JE, Braun DT, Lack JB. 2016. Parallel evolution of cold tolerance within Drosophila melanogaster. Mol. Biol. Evol. 34:349–60
     [Google Scholar]
  97. 97.
    Ragland GJ, Armbruster PA, Meuti ME. 2019. Evolutionary and functional genetics of insect diapause: a call for greater integration. Curr. Opin. Insect Sci. 36:74–81
     [Google Scholar]
  98. 98.
    Ragland GJ, Denlinger DL, Hahn DA. 2010. Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly. PNAS 107:14909–14
     [Google Scholar]
  99. 99.
    Ragland GJ, Egan SP, Feder JL, Berlocher SH, Hahn DA. 2011. Developmental trajectories of gene expression reveal candidates for diapause termination: a key life-history transition in the apple maggot fly Rhagoletis pomonella. J. Exp. Biol. 214:3948–59
     [Google Scholar]
  100. 100.
    Ragland GJ, Keep E. 2017. Comparative transcriptomics support evolutionary convergence of diapause responses across Insecta. Physiol. Entomol. 42:246–56
     [Google Scholar]
  101. 101.
    Rank NE, Bruce DA, McMillan DM, Barclay C, Dahlhoff EP. 2007. Phosphoglucose isomerase genotype affects running speed and heat shock protein expression after exposure to extreme temperatures in a montane willow beetle. J. Exp. Biol. 210:750–64
     [Google Scholar]
  102. 102.
    Ren S, Hao Y-J, Chen B, Yin Y-P. 2018. Global transcriptome sequencing reveals molecular profiles of summer diapause induction stage of onion maggot, Delia antiqua (Diptera: Anthomyiidae). G3 8:207–17
     [Google Scholar]
  103. 103.
    Reynolds JA. 2017. Epigenetic influences on diapause. Adv. Insect Physiol. 53:115–44
     [Google Scholar]
  104. 104.
    Reynolds JA. 2019. Noncoding RNA regulation of dormant states in evolutionarily diverse animals. Biol. Bull. 237:192–209
     [Google Scholar]
  105. 105.
    Reynolds JA, Bautista-Jimenez R, Denlinger DL. 2016. Changes in histone acetylation as potential mediators of pupal diapause in the flesh fly, Sarcophaga bullata. Insect Biochem. Mol. Biol. 76:29–37
     [Google Scholar]
  106. 106.
    Reynolds JA, Nachman RJ, Denlinger DL. 2019. Distinct microRNA and mRNA responses elicited by ecdysone, diapause hormone and a diapause hormone analog at diapause termination in pupae of the corn earworm, Helicoverpa zea. Gen. Comp. Endocrinol. 278:68–78
     [Google Scholar]
  107. 107.
    Rinehart JP, Li A, Yocum GD, Robich RM, Hayward SAL, Denlinger DL. 2007. Up-regulation of heat shock proteins is essential for cold survival during insect diapause. PNAS 104:11130–37
     [Google Scholar]
  108. 108.
    Roberts KT, Rank NE, Dahlhoff EP, Stillman JH, Williams CM. 2021. Snow modulates winter energy use and cold exposure across an elevation gradient in a montane ectotherm. Glob. Change Biol. 27:6103–16
     [Google Scholar]
  109. 109.
    Rozsypal J. 2022. Cold and freezing injury in insects: an overview of molecular mechanisms. Eur. J. Entomol. 119:43–57
     [Google Scholar]
  110. 110.
    Rozsypal J, Kostal V, Berkova P, Zahradnickova H, Simek P. 2014. Seasonal changes in the composition of storage and membrane lipids in overwintering larvae of the codling moth, Cydia pomonella. J. Therm. Biol. 45:124–33
     [Google Scholar]
  111. 111.
    Saastamoinen M, Hanski I. 2008. Genotypic and environmental effects on flight activity and oviposition in the Glanville fritillary butterfly. Am. Nat. 171:701–12
     [Google Scholar]
  112. 112.
    Schmidt PS, Zhu C-T, Das J, Batavia M, Yang L, Eanes WF 2008. An amino acid polymorphism in the couch potato gene forms the basis for climatic adaptation in Drosophila melanogaster. PNAS 105:16207–11
     [Google Scholar]
  113. 113.
    Sehnal D, Bittrich S, Deshpande M, Svobodová R, Berka K et al. 2021. Mol* Viewer: modern web app for 3D visualization and analysis of large biomolecular structures. Nucleic Acids Res. 49:W431–37
     [Google Scholar]
  114. 114.
    Shafer OT, Yao Z. 2014. Pigment-dispersing factor signaling and circadian rhythms in insect locomotor activity. Curr. Opin. Insect Sci. 1:73–80
     [Google Scholar]
  115. 115.
    Sheldon KS, Padash M, Carter AW, Marshall KE. 2020. Different amplitudes of temperature fluctuation induce distinct transcriptomic and metabolomic responses in the dung beetle Phanaeus vindex. J. Exp. Biol. 223:jeb233239
     [Google Scholar]
  116. 116.
    Sim C, Denlinger DL. 2011. Catalase and superoxide dismutase-2 enhance survival and protect ovaries during overwintering diapause in the mosquito Culex pipiens. J. Insect Physiol. 57:628–34
     [Google Scholar]
  117. 117.
    Sim C, Denlinger DL. 2013. Insulin signaling and the regulation of insect diapause. Front. Physiol. 4:189
     [Google Scholar]
  118. 118.
    Sim C, Kang DS, Kim S, Bai X, Denlinger DL. 2015. Identification of FOXO targets that generate diverse features of the diapause phenotype in the mosquito Culex pipiens. PNAS 112:3811–16
     [Google Scholar]
  119. 119.
    Sinclair BJ, Alvarado LEC, Ferguson LV. 2015. An invitation to measure insect cold tolerance: methods, approaches, and workflow. J. Therm. Biol. 53:180–97
     [Google Scholar]
  120. 120.
    Sinclair BJ, Ferguson LV, Salehipour-shirazi G, MacMillan HA. 2013. Cross-tolerance and cross-talk in the cold: relating low temperatures to desiccation and immune stress in insects. Integr. Comp. Biol. 53:545–56
     [Google Scholar]
  121. 121.
    Sinclair BJ, Gibbs AG, Roberts SP. 2007. Gene transcription during exposure to, and recovery from, cold and desiccation stress in Drosophila melanogaster. Insect Mol. Biol. 16:435–43
     [Google Scholar]
  122. 122.
    Sinclair BJ, Renault D 2010. Intracellular ice formation in insects: unresolved after 50 years?. Comp. Biochem. Physiol. A 155:14–18
     [Google Scholar]
  123. 123.
    Sobek-Swant S, Crosthwaite JC, Lyons DB, Sinclair BJ. 2012. Could phenotypic plasticity limit an invasive species? Incomplete reversibility of mid-winter deacclimation in emerald ash borer. Biol. Invasions 14:115–25
     [Google Scholar]
  124. 124.
    Somero GN, Lockwood BL, Tomanek L. 2017. Biochemical Adaptation: Response to Environmental Challenges, from Life's Origins to the Anthropocene Sunderland, MA: Sinauer Assoc.
  125. 125.
    Stehlík J, Závodská R, Shimada K, Sauman I, Koštál V. 2008. Photoperiodic induction of diapause requires regulated transcription of timeless in the larval brain of Chymomyza costata. J. Biol. Rhythms 23:129–39
     [Google Scholar]
  126. 126.
    Štětina T, Kostal V, Korbelova J. 2015. The role of inducible Hsp70, and other heat shock proteins, in adaptive complex of cold tolerance of the fruit fly (Drosophila melanogaster). PLOS ONE 10:e0128976
     [Google Scholar]
  127. 127.
    Štětina T, Poupardin R, Moos M, Šimek P, Šmilauer P, Koštál V. 2019. Larvae of Drosophila melanogaster exhibit transcriptional activation of immune response pathways and antimicrobial peptides during recovery from supercooling stress. Insect Biochem. Mol. Biol. 105:60–68
     [Google Scholar]
  128. 128.
    Storey KB, Storey JM. 2012. Insect cold hardiness: metabolic, gene, and protein adaptation. Can. J. Zool. 90:456–75
     [Google Scholar]
  129. 129.
    Studd EK, Bates AE, Bramburger AJ, Fernandes T, Hayden B et al. 2021. Nine maxims for the ecology of cold-climate winters. BioScience 71:820–30
     [Google Scholar]
  130. 130.
    Sunday JM, Bates AE, Dulvy NK. 2011. Global analysis of thermal tolerance and latitude in ectotherms. Proc. R. Soc. B 278:1823–30
     [Google Scholar]
  131. 131.
    Tamura K, Stecher G, Kumar S. 2021. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol. Biol. Evol. 38:3022–27
     [Google Scholar]
  132. 132.
    Teets NM, Denlinger DL. 2013. Physiological mechanisms of seasonal and rapid cold-hardening in insects. Physiol. Entomol. 38:105–16
     [Google Scholar]
  133. 133.
    Teets NM, Denlinger DL. 2016. Quantitative phosphoproteomics reveals signaling mechanisms associated with rapid cold hardening in a chill-tolerant fly. J. Proteome Res. 15:2855–62
     [Google Scholar]
  134. 134.
    Teets NM, Gantz JD, Kawarasaki Y. 2020. Rapid cold hardening: ecological relevance, physiological mechanisms and new perspectives. J. Exp. Biol. 223:jeb203448
     [Google Scholar]
  135. 135.
    Teets NM, Hahn DA. 2018. Genetic variation in the shape of cold-survival curves in a single fly population suggests potential for selection from climate variability. J. Evol. Biol. 31:543–55
     [Google Scholar]
  136. 136.
    Teets NM, Peyton JT, Ragland GJ, Colinet H, Renault D et al. 2012. Combined transcriptomic and metabolomic approach uncovers molecular mechanisms of cold tolerance in a temperate flesh fly. Physiol. Genom. 44:764–77
     [Google Scholar]
  137. 137.
    Teets NM, Yi SX, Lee RE, Denlinger DL. 2013. Calcium signaling mediates cold sensing in insect tissues. PNAS 110:9154–59
     [Google Scholar]
  138. 138.
    Telonis-Scott M, Hallas R, McKechnie SW, Wee CW, Hoffmann AA. 2009. Selection for cold resistance alters gene transcript levels in Drosophila melanogaster. J. Insect Physiol. 55:549–55
     [Google Scholar]
  139. 139.
    Terhzaz S, Teets NM, Cabrero P, Henderson L, Ritchie MG et al. 2015. Insect capa neuropeptides impact desiccation and cold tolerance. PNAS 112:2882–87
     [Google Scholar]
  140. 140.
    Thorne MAS, Seybold A, Marshall C, Wharton D. 2017. Molecular snapshot of an intracellular freezing event in an Antarctic nematode. Cryobiology 75:117–24
     [Google Scholar]
  141. 141.
    Todgham AE, Hoaglund EA, Hofmann GE. 2007. Is cold the new hot? Elevated ubiquitin-conjugated protein levels in tissues of Antarctic fish as evidence for cold-denaturation of proteins in vivo. J. Comp. Physiol. B 177:857–66
     [Google Scholar]
  142. 142.
    Toxopeus J, Marteaux LED, Sinclair BJ. 2019. How crickets become freeze tolerant: the transcriptomic underpinnings of acclimation in Gryllus veletis. Comp. Biochem. Physiol. D 29:55–66
     [Google Scholar]
  143. 143.
    Toxopeus J, Sinclair BJ. 2018. Mechanisms underlying insect freeze tolerance. Biol. Rev. 93:1891–914
     [Google Scholar]
  144. 144.
    Vesala L, Hoikkala A. 2011. Effects of photoperiodically induced reproductive diapause and cold hardening on the cold tolerance of Drosophila montana. J. Insect Physiol. 57:46–51
     [Google Scholar]
  145. 145.
    Vigoder FM, Parker DJ, Cook N, Tournière O, Sneddon T, Ritchie MG. 2016. Inducing cold-sensitivity in the frigophilic fly Drosophila montana by RNAi. PLOS ONE 11:e0165724
     [Google Scholar]
  146. 146.
    Whelan S, Goldman N. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18:691–99
     [Google Scholar]
  147. 147.
    Williams CM, Henry HAL, Sinclair BJ. 2015. Cold truths: how winter drives responses of terrestrial organisms to climate change. Biol. Rev. 90:214–35
     [Google Scholar]
  148. 148.
    Xu K, Niu Q, Zhao H, Du Y, Jiang Y. 2017. Transcriptomic analysis to uncover genes affecting cold resistance in the Chinese honey bee (Apis cerana cerana). PLOS ONE 12:e0179922
     [Google Scholar]
  149. 149.
    Yin ZJ, Dong XL, Kang K, Chen H, Dai XY et al. 2018. FoxO transcription factor regulate hormone mediated signaling on nymphal diapause. Front. Physiol. 9:1654
     [Google Scholar]
  150. 150.
    Zachariassen KE, Kristiansen E. 2000. Ice nucleation and antinucleation in nature. Cryobiology 41:257–79
     [Google Scholar]
  151. 151.
    Zhang J, Marshall KE, Westwood JT, Clark MS, Sinclair BJ. 2011. Divergent transcriptomic responses to repeated and single cold exposures in Drosophila melanogaster. J. Exp. Biol. 214:4021–29
     [Google Scholar]
  152. 152.
    Zhang Q, Nachman RJ, Kaczmarek K, Zabrocki J, Denlinger DL. 2011. Disruption of insect diapause using agonists and an antagonist of diapause hormone. PNAS 108:16922–26
     [Google Scholar]
  153. 153.
    Zhu L, Tian Z, Guo S, Liu W, Zhu F, Wang XP. 2019. Circadian clock genes link photoperiodic signals to lipid accumulation during diapause preparation in the diapause-destined female cabbage beetles Colaphellus bowringi. Insect Biochem. Mol. Biol. 104:1–10
     [Google Scholar]
/content/journals/10.1146/annurev-ento-120120-095233
Loading
Molecular Mechanisms of Winter Survival
Annual Review of Entomology 68, 319 (2023); https://doi.org/10.1146/annurev-ento-120120-095233
/content/journals/10.1146/annurev-ento-120120-095233
/content/journals/10.1146/annurev-ento-120120-095233
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error