Journal of Comparative Physiology B

, Volume 178, Issue 8, pp 917–933 | Cite as

How insects survive the cold: molecular mechanisms—a review

  • Melody S. Clark
  • M. Roger Worland


Insects vary considerably in their ability to survive low temperatures. The tractability of these organisms to experimentation has lead to considerable physiology-based work investigating both the variability between species and the actual mechanisms themselves. This has highlighted a range of strategies including freeze tolerance, freeze avoidance, protective dehydration and rapid cold hardening, which are often associated with the production of specific chemicals such as antifreezes and polyol cryoprotectants. But we are still far from identifying the critical elements behind over-wintering success and how some species can regularly survive temperatures below −20°C. Molecular biology is the most recent tool to be added to the insect physiologist’s armoury. With the public availability of the genome sequence of model insects such as Drosophila and the production of custom-made molecular resources, such as EST libraries and microarrays, we are now in a position to start dissecting the molecular mechanisms behind some of these well-characterised physiological responses. This review aims to provide a state-of-the-art snapshot of the molecular work currently being conducted into insect cold tolerance and the very interesting preliminary results from such studies, which provide great promise for the future.


ESTs Microarray Proteomics Stress Cryoprotection 



This paper was produced within the BAS BIOREACH/BIOFLAME core programmes and also contributes to the SCAR EBA programme. The authors would like to thank Peter Convey for critical reading of the manuscript.


  1. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF et al (2000) The genome sequence of Drosophila melanogaster. Science 287:2185–2195PubMedCrossRefGoogle Scholar
  2. Agre P, Preston GM, Smith BL, Jung JS, Raina S, Moon c, Guggino WB, Nielson S (1993) Aquaporin chip—the archetypal molecular water channel. Am J Sci 265:F463–F476Google Scholar
  3. Andorfer CA, Duman JG (2000) Isolation and characterization of cDNA clones encoding antifreeze proteins of the pyrochroid beetle Dendroides canadensis. J Insect Physiol 46:365–372PubMedCrossRefGoogle Scholar
  4. Arber S, Halder G, Caroni P (1994) Muscle LIM protein, a novel regulator of myogenesis, promotes myogenic differentiation. Cell 79:221–231PubMedCrossRefGoogle Scholar
  5. Bale JS (1993) Classes of insect cold hardiness. Funct Ecol 7:751–753Google Scholar
  6. Bale JS (2002) Insects and low temperatures: from molecular biology to distributions and abundance. Philos Trans R Soc B 357:849–861CrossRefGoogle Scholar
  7. Bayley M, Peterson SO, Knigge T, Kohler HR, Holmstrup M (2001) Drought acclimation confers cold tolerance in the soil collembolan Folsomia candida. J Insect Physiol 47:1197–1204PubMedCrossRefGoogle Scholar
  8. Bennett VA, Pruitt NL, Lee RE (1997) Seasonal changes in fatty acid composition associated with cold-hardening in third instar larvae of Eurosta solidaginis. J Comp Physiol B 167:249–255CrossRefGoogle Scholar
  9. Bennett VA, Lee RE, Nauman JS, Kukal O (2003) Selection of overwintering microhabitats used by the Arctic woolybear caterpillar, Gynaephora groenlandica. Cryoletters 24:191–200PubMedGoogle Scholar
  10. Bilgen T, English TE, McMullen DC, Storey KB (2001) EsMlp, a muscle-LIM protein gene, is up-regulated during cold exposure in the freeze-avoiding larvae of Epiblema scudderiana. Cryobiology 3:11–20CrossRefGoogle Scholar
  11. Cannon RJC, Block W (1988) Cold tolerance of microarthropods. Biol Rev 63:23–77CrossRefGoogle Scholar
  12. Chen CP, Denlinger DL (1992) Reduction of cold injury in flies using an intermittent pulse of high-temperature. Cryobiology 29:138–143CrossRefGoogle Scholar
  13. Chen CP, Denlinger DL, Lee RE (1987) Cold-shock injury and rapid cold hardening in the flesh fly, Sarcophaga crassipalpis. Physiol Zool 60:297–304Google Scholar
  14. Chen LB, DeVries AL, Cheng CHC (1997) Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod. Proc Natl Acad Sci USA 94:3817–3822PubMedCrossRefGoogle Scholar
  15. Chen B, Kayukawa T, Monteiro A, Ishikawa Y (2005) The expression of the HSP90 gene in response to winter and summer diapauses and thermal-stress in the onion maggot, Delia antiqua. Insect Mol Biol 14:697–702PubMedCrossRefGoogle Scholar
  16. Chino CP (1957) Conversion of glycogen to sorbitol and glycerol in the diapause egg of the Bombyx silkworm. Nature 180:606–607CrossRefGoogle Scholar
  17. Chown SL, Terblanche JS (2007) Physiological diversity in insects: ecological and evolutionary contexts. Adv Insect Physiol 33:50–152CrossRefGoogle Scholar
  18. Clark MS, Fraser KPPF, Peck LS (2008) Antarctic marine molluscs do have an HSP70 heat shock response. Cell Stress Chaperone 13. doi:  10.1007/s12192-008-0014-8
  19. Clark MS, Thorne MAS, Purać J, Grubor-Lajšić G, Kube M, Reinhardt R, Worland MR (2007) Surviving extreme polar winters by desiccation: clues from Arctic springtail (Onychiurus arcticus) EST libraries. BMC Genomics doi: 10.1186/1471-2164-8-475
  20. Cohet Y, Vouidibio J, David JR (1980) Thermal tolerance and geographical-distribution: a comparison of cosmopolitan and tropical endemic Drosophila species. J Therm Biol 5:69–74CrossRefGoogle Scholar
  21. Colinet H, Nguyen TTA, Cloutier C, Michaud D, Hance T (2007) Proteomic profiling of a parasitic wasp exposed to constant and fluctuating cold exposure. Insect Biochem Mol 37:1177–1188CrossRefGoogle Scholar
  22. Convey P (1996) The influence of environmental characteristics on life history attributes of Antarctic terrestrial biota. Biol Rev 71:191–225CrossRefGoogle Scholar
  23. Convey P (2000) How does cold constrain life cycles of terrestrial plants and animals? Cryoletters 21:73–82Google Scholar
  24. Cossins AR (ed) (1994) Temperature adaptations of biological membranes. Portland Press, LondonGoogle Scholar
  25. Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599PubMedCrossRefGoogle Scholar
  26. Czajka MC, Lee RE (1990) A rapid cold-hardening response protecting against cold shock injury in Drosophila melanogaster. J Exp Biol 148:245–254PubMedGoogle Scholar
  27. Dallerac R, Labeur C, Jallon JM, Knippie DC, Roelofs WL, Wicker-Thomas C (2000) A Delta 9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster. Proc Natl Acad Sci USA 97:9449–9454PubMedCrossRefGoogle Scholar
  28. Danks HV (2005) Key themes in the study of seasonal adaptations in insects I. Patterns of cold hardiness. Appl Entomol Zool 40:199–211CrossRefGoogle Scholar
  29. Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93–122PubMedCrossRefGoogle Scholar
  30. DeVries AL (1971) Glycoproteins as biological antifreeze agents in Antarctic fishes. Science 172:1152PubMedCrossRefGoogle Scholar
  31. Diabo S, Kimura MT, Goto SG (2001) Upregulation of genes belonging to the drosomycin family in diapausing adults of Drosophila triauraria. Gene 278:177–184CrossRefGoogle Scholar
  32. Doucet D, Tyshenko MG, Davies PL, Walker VK (2002) A family of expressed antifreeze protein genes from the moth, Choristoneura fumiferana. Eur J Biochem 269:38–46PubMedCrossRefGoogle Scholar
  33. Drobnis EZ, Crowe LM, Berger T, Anchordoguy TJ, Overstreet JW, Crowe JH (1993) Cold shock damage is due to lipid phase-transition in cell membranes—a demonstration using sperm as a model. J Exp Zool 265:432–437PubMedCrossRefGoogle Scholar
  34. Duman JG (1977) Role of macromolecular antifreeze in the darkling beetle Meracantha contracta. J Comp Physiol 115:279–286Google Scholar
  35. Duman JG (2001) Antifreeze and ice nucleator proteins in terrestrial arthropods. Annu Rev Physiol 63:327–357PubMedCrossRefGoogle Scholar
  36. Duman JG, Bennett T, Sformo T, Hochstrasser R, Barnes BM (2004) Antifreeze proteins in Alaskan insects and spiders. J Insect Physiol 50:259–266PubMedCrossRefGoogle Scholar
  37. Duman JG, DeVries AL (1974) Effects of temperature and photoperiod on antifreeze production in cold water fishes. J Exp Biol 190:89–97Google Scholar
  38. Duman JG, Li N, Verleye D, Goetz FW, Wu DW, Andorfer CA, Benjamin T, Parmelee DC (1998) Molecular characterization and sequencing of antifreeze proteins from larvae of the beetle Dendroides canadensis. J Comp Physiol B 168:225–232PubMedCrossRefGoogle Scholar
  39. Eigenheer AL, Young S, Blomquist GJ, Borgeson CE, Tillman JA, Tittiger C (2002) Isolation and molecular characterization of Musca domestica delta-9 desaturase sequences. Insect Mol Biol 11:533–542PubMedCrossRefGoogle Scholar
  40. Ellers J, Marien J, Driessen G, Van Straalen N (2008) Temperature induced gene expression associated with different thermal reaction norms and growth rate. J Exp Zool (Mol Dev Evol) 310B:137–147CrossRefGoogle Scholar
  41. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282PubMedCrossRefGoogle Scholar
  42. Fink AL (1999) Chaperone-mediated protein folding. Physiol Rev 79:425–449PubMedGoogle Scholar
  43. Forge TA, MacGuidwin AE (1992) Effects of water potential and temperature on survival of the nematode Meloidogyne hapla in frozen soil. Can J Zool 70:1553–1560CrossRefGoogle Scholar
  44. Frenot Y, Chown SL, Whinam J, Selkirk PM, Convey P, Skotnicki M, Bergstrom DM (2005) Biological invasions in the Antarctic: extent, impacts and implications. Biol Rev 80:45–72PubMedCrossRefGoogle Scholar
  45. 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 210:3295–3300PubMedCrossRefGoogle Scholar
  46. Fujiwara Y, Shindome C, Takeda M, Shiomi K (2006) The roles of ERK and p38 MAPK signalling cascades on embryonic diapause initiation and termination of the silkworm, Bombyx mori. Insect Biochem Mol Biol 36:47–53PubMedCrossRefGoogle Scholar
  47. Gaston KJ, Chown SL, Evans KL (2008) Ecogeographical rules: elements of a synthesis. J Biogeogr 35:483–500CrossRefGoogle Scholar
  48. Godlewski J, Kudkiewicz B, Grzelak K, Cymborowski B (2001) Expression of larval hemolymph proteins (lhp) genes and protein synthesis in the fat body of the greater wax moth (Galleria mellonella) larvae during diapause. J Insect Physiol 47:759–766PubMedCrossRefGoogle Scholar
  49. Goto SG (2000) Expression of Drosophila homologue of senescence marker protein-30 during cold acclimation. J Insect Physiol 46:1111–1120PubMedCrossRefGoogle Scholar
  50. Goto SG (2001) A novel gene that is upregulated during recovery from cold shock in Drosophila melanogaster. Gene 270:259–264PubMedCrossRefGoogle Scholar
  51. Goto SG, Kimura MT (1998) Heat and cold-shock responses and temperature adaptations in subtropical and temperate species of Drosophila. J Insect Physiol 44:1233–1239PubMedCrossRefGoogle Scholar
  52. Goto SG, Kimura MT (2004) Heat shock responsive gene are not involved in the adult diapause of Drosophila triauraria. Gene 326:117–122PubMedCrossRefGoogle Scholar
  53. Goto SG, Yoshida KM, Kimura MT (1998) Accumulation of Hsp70 mRNA under environmental stress in diapausing and nondiapausing adults of Drosophila triauraria. J Insect Physiol 44:1009–1015PubMedCrossRefGoogle Scholar
  54. Graham LA, Davies PL (2005) Glycine-rich antifreeze proteins from snow fleas. Science 310:461PubMedCrossRefGoogle Scholar
  55. Graham LA, Bendena WG, Walker VK (1996) Juvenile hormone regulation and developmental expression of a Tenebrio desiccation stress protein gene. Dev Genet 18:296–305PubMedCrossRefGoogle Scholar
  56. Graham LA, Liou YC, Walker VK, Davies PL (1997) Hyperactive antifreeze protein from beetles. Nature 388:727–728PubMedCrossRefGoogle Scholar
  57. Grewal PS, Bornstein-Forest S, Burnell AM, Glazer I, Jagdale GB (2006) Physiological, genetic, and molecular mechanisms of chemoreception, thermobiosis, and anhydrobiosis in entomopathogenic nematodes. Biol Control 38:54–65CrossRefGoogle Scholar
  58. Hayakawa Y (1985) Activation of insect fat-body phosphorylase by cold-phosphorylase-kinase, phosphatase and ATP level. Insect Biochem 15:123–128CrossRefGoogle Scholar
  59. Hayward SAL, Rinehart JP, Denlinger DL (2004) Desiccation and rehydration elicit distinct heat shock protein transcript response in flesh fly. J Exp Biol 207:963–971PubMedCrossRefGoogle Scholar
  60. Hayward SAL, Pavlides SC, Tammariello SP, Rinehart JP, Denlinger DL (2005) Temporal expression patterns of diapause-associated genes in flesh fly pupae from the onset of diapause through post-diapause quiescence. J Insect Physiol 51:631–640PubMedCrossRefGoogle Scholar
  61. Hayward SAL, Rinehart JP, Sandro LH, Lee RE, Denlinger DL (2007) Slow dehydration promotes desiccation and freeze tolerance in the Antarctic midge Belgica antarctica. J Exp Biol 210:836–844PubMedCrossRefGoogle Scholar
  62. Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381:571–580PubMedCrossRefGoogle Scholar
  63. Hengherr S, Heyer AG, Kohler HR, Schill RO (2007) Trehalose and anhydrobiosis in tardigrades—evidence for divergence in response to dehydration. FEBS J doi:  10.1111/j.1742-4658.2007.06198.x
  64. Hoffmann AA (1990) Acclimation for desiccation resistance in Drosophila melanogaster and the association between acclimation response and genetic-variation. J Insect Physiol 36:885–891CrossRefGoogle Scholar
  65. Hofmann GE (2005) Patterns of Hsp gene expression in exothermic marine organisms on small to large biogeographic scales. Integr Comp Biol 45:247–255CrossRefGoogle Scholar
  66. Hoffmann AA, Parsons PA (1993) Selection for adult desiccation resistance in Drosophila melanogaster—fitness components, larval resistance and stress tolerance. Biol J Linn Soc 48:43–54CrossRefGoogle Scholar
  67. Hoffmann AA, Sørensen JG, Loeschoke V (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J Therm Biol 28:175–213CrossRefGoogle Scholar
  68. Holmstrup M, Hedlund K, Boriss H (2002) Drought acclimation and lipid composition in Folsomia candida: implications for cold shock, heat shock and acute desiccation stress. J Insect Physiol 48:961–970PubMedCrossRefGoogle Scholar
  69. Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JMC, Wides R et al (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129. doi: 10.1126/science.1076181 PubMedCrossRefGoogle Scholar
  70. Hosier JS, Burns JE, Esch HE (2000) Flight muscle resting potential and species-specific differences in chill coma. J Insect Physiol 46:621–627CrossRefGoogle Scholar
  71. Huang LH, Kang L (2007) Cloning and interspecific altered expression of heat shock protein genes in two leafminer species in response to thermal stress. Insect Mol Biol 16:491–500PubMedCrossRefGoogle Scholar
  72. Huang T, Nicodemus J, Zarka DG, Thomashow MF, Wisniewski M, Duman JG (2002) Expression of an insect (Dendroides canadensis) antifreeze protein in Arabidopsis thaliana results in a decrease in plant freezing temperature. Plant Mol Biol 50:333–344PubMedCrossRefGoogle Scholar
  73. Joanisse DR, Storey KB (1994a) Enzyme-activity profiles in and overwintering population of freeze-avoiding gall moth larvae, Epiblema scudderiana. Can J Zool 72:1079–1086CrossRefGoogle Scholar
  74. Joanisse DR, Storey KB (1994b) Enzyme-activity profiles in and overwintering population of freeze-tolerant larvae of the gall fly, Eurosta solidaginis. J Comp Physiol B 164:247–255CrossRefGoogle Scholar
  75. Joplin KH, Denlinger DL (1990) Development and tissue specific control of the heat-shock induced 70 kDa related proteins in the flesh fly Sarcophaga crassipalpis. J Insect Physiol 36:239–249CrossRefGoogle Scholar
  76. Kayukawa T, Chen B, Miyazaki S, Itoyama K, Shinoda T, Ishikawa Y (2005) Expression of the mRNA for the t-complex polypeptide-1, a subunit of chaperonin CCT, is upregulated in association with increased cold hardiness in Delia antiqua. Cell Stress Chaperone 10:204–210CrossRefGoogle Scholar
  77. Kayukawa T, Chen B, Hoshizaki S, Ishikawa Y (2007a) Upregulation of a desaturase is associated with enhancement of cold hardiness in the onion maggot Delia antiqua. Insect Biochem Mol Biol 37:1160–1167PubMedCrossRefGoogle Scholar
  78. Kayukawa T, Chen B, Hoshizaki S, Ishikawa Y (2007b) Upregulation of a desaturase is associated with the enhancement of cold hardiness in the onion maggot, Delia antiqua. Insect Biochem Mol Biol 37:1160–1167PubMedCrossRefGoogle Scholar
  79. Kelty JD, Lee RE (1999) Induction of rapid cold hardening by cooling at ecologically relevant rates in Drosophila melanogaster. J Insect Physiol 45:719–726PubMedCrossRefGoogle Scholar
  80. Kelty JD, Lee RE (2001) Rapid cold-hardening of Drosophila melanogaster (Diptera: Drosophilidae) during ecologically based thermoperiodic cycles. J Exp Biol 204:1659–1666PubMedGoogle Scholar
  81. Kidokoro K, Iwata K-I, Takeda M, Fujiwara Y (2006) Involvement of ERK/MAPK in regulation of diapuase intensity in the false melon beetle, Atrachya menetriesi. J Insect Physiol 52:1189–1193PubMedCrossRefGoogle Scholar
  82. Kikawada T, Nakahara Y, Kanamori Y, Iwata K-I, Watanabe M, McGee B, Tunnacliffe A, Okuda T (2006) Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid. Biochem Bioph Res Co 348:56–61CrossRefGoogle Scholar
  83. Kim M, Robich RM, Rinehart JP, Denlinger DL (2006) Upregulation of two actin genes and redistribution of actin during dipause and cold stress in the northern house mosquito, Culex pipiens. J Insect Physiol 52:1226–1233PubMedCrossRefGoogle Scholar
  84. Knight CA, Duman JG (1986) Inhibition of recrystallization by insect thermal hysteresis proteins—a possible cryoprotective role. Cryobiol 23:256–262CrossRefGoogle Scholar
  85. Koštál V, Berková P, Šimek P (2003) Remodelling of membrane phospholipids during transition to diapause and cold-acclimation in the larvae of Chymomyza costata (Drosophila). Comp Biochem Physiol B 135:407–419PubMedCrossRefGoogle Scholar
  86. Koštál V, Vambera J, Bastl J (2004) On the nature of pre-freeze mortality in insects: water balance, ion homeostasis and energy charge in the adults of Pyrrhocoris apterus. J Exp Biol 207:1509–1521PubMedCrossRefGoogle Scholar
  87. Koštál V, Renault D, Mehrabianová A, Bastl J (2007) Insect cold tolerance and repair of chill-injury at fluctuating thermal regimes: role of homeostasis. Comp Biochem Physiol A 147:231–238CrossRefGoogle Scholar
  88. Kruse E, Uehlein N, Kaldenhoff R (2006) The aquaporins. Genome Biol 7:206. doi: 10.1186/gb-2006-7-2-206 PubMedCrossRefGoogle Scholar
  89. Kukal O (1991) Behavioral and physiological adaptations to cold in a freeze-tolerant arctic insect. In: Lee RE, Denlinger DL (eds) Insects at low temperature. Chapman and Hall, London, pp 276–300Google Scholar
  90. Kukal O, Duman JG, Serianni AS (1989) Cold-induced mitochondrial degradation and cryoprotectants synthesis in freeze-tolerant Arctic caterpillars. J Comp Physiol B 158:661–671PubMedCrossRefGoogle Scholar
  91. Lalouette L, Kostal V, Colinet H, Gagneul D, Renault D (2007) Cold exposure and associated metabolic changes in adult tropical beetles exposed to fluctuating thermal regimes. FEBS J 274:1759–1767PubMedCrossRefGoogle Scholar
  92. Lee RE, Denlinger DL (1991) Insects at low temperature. Chapman and Hall, LondonGoogle Scholar
  93. Lee RE, Chen CP, Meacham MH, Denlinger DL (1987) Ontogenic patterns of cold-hardiness and glycerol production in Sarcophaga crassipalpis. J Insect Physiol 33:587–592CrossRefGoogle Scholar
  94. Lee RE, Strong-Gunderson JM, Lee MR, Grove KS, Riga TJ (1991) Isolation of ice nucleating active bacteria from insects. J Exp Zool 257:124–127CrossRefGoogle Scholar
  95. Levin DB, Danks HV, Barber SA (2003) Variation in mitochondrial DNA and gene transcription in freezing-tolerant larvae of Eurosta solidaginis (Diptera: Tephritidae) and Gynaephora groenlandica (Lepidoptera: Lymantriidae). Insect Mol Biol 12:281–289PubMedCrossRefGoogle Scholar
  96. Lewis DK, Spurgeon D, Sappington TW, Keeley LL (2002) A hexamerin protein AgSP-1 is associated with diapause in the boll weevil. J Insect Physiol 48:887–901PubMedCrossRefGoogle Scholar
  97. Li AQ, Popova-Butler A, Dean DH, Denlinger DL (2007) Proteomics of the flesh fly brain reveals an abundance of upregulated heat shock proteins during pupal diapause. J Insect Physiol 53:385–391PubMedCrossRefGoogle Scholar
  98. Liu W, Ma PWK, Marsella-Herrick P, Rosenfield CL, Knipple DC, Roelofs T (1999) Cloning and functional expression of a cDNA encoding a metabolic acyl-CoA Delta 9-desaturase of the cabbage looper moth, Trichoplusia ni. Insect Biochem Mol Biol 29:435–443PubMedCrossRefGoogle Scholar
  99. Michaud MR, Denlinger DL (2004) Molecular modalities of insect cold survival: current understanding and future trends. Int Congress Ser 1275:32–46CrossRefGoogle Scholar
  100. Michaud MR, Denlinger DL (2006) Oleic acid is elevated in cell membranes during rapid cold-hardening and pupal diapause in the flesh fly, Sarcophaga crassipalpis. J Insect Physiol 52:1073–1082PubMedCrossRefGoogle Scholar
  101. Michaud MR, Denlinger DL (2007) Shifts in the carbohydrate, polyol and amino acid pools during rapid cold-hardening and diapause-associated cold-hardening in flesh flies (Sarcophaga crassipalpis): a metabolomic comparison. J Comp Physiol B 177:753–763PubMedCrossRefGoogle Scholar
  102. Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Gene Dev 12:3788–3796PubMedCrossRefGoogle Scholar
  103. P Morin Jr, McMullen DC, Storey KB (2005) HIF-1α involvement in low temperature and anoxia survival by a freeze tolerant insect. Mol Cell Biochem 280:99–106PubMedCrossRefGoogle Scholar
  104. Nene V, Wortman JR, Lawson D, Haas B, Kodira C, Tu Z, Loftus B, Xi Z, Megy K, Grabherr M (2007) Genome sequence of Aedes aegypti, a major arbovirus vector. Science 316:1718. doi: 10.1126/science.1138878 PubMedCrossRefGoogle Scholar
  105. Nenev LG, Duman JG, Low MG, Sehl LC, Castellino FJ (1989) Purification and characterization of an insect hemolymph lipoprotein ice nucleator: evidence for the importance of phosphatidylinositol and apolipoprotein in the ice nucleator activity. Cryobiology 27:416–422Google Scholar
  106. Nicodemus J, O’Tousa JE, Duman JG (2006) Expression of a beetle, Dendroides canadensis, antifreeze protein in Drosophila melanogaster. J Insect Physiol 52:888–896PubMedCrossRefGoogle Scholar
  107. Nielsen MM, Overgaard J, Sørensen JG, Holmstrup M, Justesen J, Loeschcke V (2005) Role of HSF activation for resistance to heat, cold and high-temperature knock-down. J Insect Physiol 51:1320–1329PubMedCrossRefGoogle Scholar
  108. Nordin JH, Cui Z, Yin C-M (1984) Cold-induced glycerol accumulation by Ostrinia nubilalis larvae is developmentally regulated. J Insect Physiol 30:563–566CrossRefGoogle Scholar
  109. Norry FM, Gomez FH, Loeschcke V (2007) Knockdown resistance to heat stress and slow recovery from chill coma are genetically associated in a quantitative trait locus region of chromosome 2 in Drosophila melanogaster. Mol Ecol 16:3274–3284PubMedCrossRefGoogle Scholar
  110. Nunamaker RA, Dean VC, Murphy KE, Lockwood JA (1996) Stress proteins elicited by cold shock in the midge Culicoides variipennis sonorensis Wirth and Jones. Comp Biochem Physiol B 113:73–77CrossRefGoogle Scholar
  111. Ohtsu T, Kimura MT, Katagiri C (1998) How Drosophila species acquire cold tolerance—qualitative changes of phospholipids. Eur J Biochem 252:608–611PubMedCrossRefGoogle Scholar
  112. Overgaard J, Malmendal A, Sorensen JG, Bundy JG, Loeschcke V, Nielson NC, Holmstrop M (2007) Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. J Insect Physiol 12:1218–1232CrossRefGoogle Scholar
  113. Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance, degradation and reactivation of damaged proteins. Ann Rev Genet 27:437–496PubMedCrossRefGoogle Scholar
  114. Pfister TD, Storey KB (2002) Protein kinase A: purification and characterization of the enzyme from two cold-hardy goldenrod gall insects. Insect Biochem Mol Biol 32:505–515PubMedCrossRefGoogle Scholar
  115. Pfister TD, Storey KB (2006) Insect freeze tolerance: roles of protein phosphatases and protein kinase A. Insect Biochem Mol Biol 36:18–24PubMedCrossRefGoogle Scholar
  116. Pietrantonio PV, Gibson GE, Strey AA, Petzel D, Hayes TK (2000) Characterization of a leucokinin binding protein in Aedes aegypti (Diptera : Culicidae) Malpighian tubule. Insect Biochem Mol Biol 30:1147–1159PubMedCrossRefGoogle Scholar
  117. Place SP, Zippay ML, Hofmann GE (2004) Constitutive roles for inducible genes: evidence for the alteration in expression of the inducible hsp70 gene in Antarctic notothenioid fish. Am J Physiol Reg I 287:R429–R436Google Scholar
  118. Privalov PL (1990) Cold denaturation of proteins. Crit Rev Biochem Mol Biol 25:281–305PubMedCrossRefGoogle Scholar
  119. Qin W, Neal SJ, Robertson RM, Westwood JT, Walker VK (2005) Cold hardening and transcriptional change in Drosophila melanogaster. Insect Mol Biol 14:607–613PubMedCrossRefGoogle Scholar
  120. Qin W, Doucet D, Tyshenko MG, Walker VK (2007) Transcription of antifreeze protein genes in Choristoneura fumiferana. Insect Mol Biol 16:423–434PubMedCrossRefGoogle Scholar
  121. Rako L, Blacket MJ, McKechnie SW, Stephen W, Hoffmann AA, Ary A (2007) Candidate genes and thermal phenotypes: identifying ecologically important genetic variation for thermotolerance in the Australian Drosophila melanogaster cline. Mol Biol 16:2948–2957Google Scholar
  122. Raymond JA, DeVries AL (1977) Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proc Natl Acad Sci USA 74:2589–2593PubMedCrossRefGoogle Scholar
  123. Rinehart JP, Denlinger DL (2000) Heat-shock protein 90 is down regulated during pupal diapause in the flesh fly, Sarcophagus crassipalpis, but remains responsive to thermal stress. Insect Mol Biol 9:641–645PubMedCrossRefGoogle Scholar
  124. Rinehart JP, Yocum GD, Denlinger DL (2000) Developmental upregulation of inducible hsp70 transcripts, but not the cognate form, during pupal diapause in the flesh fly, Sarcophagus crassipalpis. Insect Biochem Mol Biol 30:515–521PubMedCrossRefGoogle Scholar
  125. Rinehart JP, Hayward SAL, Elnitsky MA, Sandro LH, Lee RE (2006a) Continuous up-regulation of heat shock proteins in larvae, but not adults, in a polar insect. Proc Natl Acad Sci USA 103:14225–14227CrossRefGoogle Scholar
  126. Rinehart JP, Robich RM, Denlinger DL (2006b) Enhanced cold and desiccation tolerance in diapausing adults of Culex pipiens and a role for HSP70 in response to cold shock but not as a component of the diapause program. J Med Entomol 43:713–722PubMedCrossRefGoogle Scholar
  127. 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 dipause. Proc Natl Acad Sci USA 104:11130–11137PubMedCrossRefGoogle Scholar
  128. Ring RA, Riegert PW (1991) A tribute to R.W. Salt. In: Lee RE, Denlinger DL (eds) Insects at low temperature. Chapman and Hall, London, pp 3–16Google Scholar
  129. Ring RA, Danks HV (1994) Desiccation and cryoprotection—overlapping adaptations. Cryoletters 15:181–190Google Scholar
  130. Russell NJ (1997) Psychrophilic bacteria—molecular adaptations of membrane lipids. Comp Biochem Physiol A 118:489–493CrossRefGoogle Scholar
  131. Sakamoto T, Bryant DA (1997) Temperature-regulated mRNA accumulation and stabilization for fatty acid desaturase genes in the cyanobacterium Synechococcus sp. strain PCC 7002. Mol Microbiol 23:1281–1292PubMedCrossRefGoogle Scholar
  132. Salt RW (1957) Natural occurrence of glycerol in insects and its relation to their ability to survive freezing. Can Entomol 89:491–494CrossRefGoogle Scholar
  133. Salt RW (1959) Role of glycerol in the cold-hardening of Bracon cephi (Gahan). Can J Zool 37:59–69Google Scholar
  134. Salt RW (1961) Principles of insect cold hardiness. Annu Rev Entomol 6:55–74CrossRefGoogle Scholar
  135. Salt RW (1966) Factors influencing nucleation in supercooled insects. Can J Zool 44:117–133CrossRefGoogle Scholar
  136. Salvucci ME, Strecher DS, Henneberry TJ (2000) Heat shock proteins in whiteflies, an insect that accumulates sorbitol in response to heat stress. J Thermal Biol 25:363–371CrossRefGoogle Scholar
  137. Scotter AJ, Marshall CB, Graham LA, Gilbert JA, Garnham CP, Davies PL (2006) The basis for hyperactivity of antifreeze proteins. Cryobiology 53:229–239PubMedCrossRefGoogle Scholar
  138. Sinclair BJ, Stevens MI (2006) Terrestrial microarthropods of Victoria Land and Queen Maud Mountains, Antarctica: implications of climate change. Soil Biol Biochem 38:3158–3170CrossRefGoogle Scholar
  139. 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 16:435–443PubMedCrossRefGoogle Scholar
  140. Slachta M, Berkova P, Vambera J, Koštál V (2002) Physiology of cold-acclimation in non-diapausing adults of Pyrrhocoris apterus (Heteroptera). Eur J Entomol 99:181–187Google Scholar
  141. Sømme L (1982) Supercooling and winter survival in terrestrial arthropods. Comp Biochem Physiol A 73:519–543CrossRefGoogle Scholar
  142. Sømme L (1999) The physiology of cold hardiness in terrestrial arthropods. Eur J Entomol 96:1–10Google Scholar
  143. Sømme L, Block W (1982) Cold hardiness of Collembola at Signy Island, maritime Antarctic. Oikos 38:68–176CrossRefGoogle Scholar
  144. Sonoda S, Fukumoto K, Izumi Y, Ashfaq M, Yoshida H, Tsumuki H (2006a) Methionine-rich storage protein gene in the rice stem borer, Chilo suppressalis, is expressed during diapause in response to cold acclimation. Insect Mol Biol 15:853–859PubMedCrossRefGoogle Scholar
  145. Sonoda S, Fukumoto K, Izumi Y, Yoshida H, Tsumuki H (2006b) Cloning of heat shock protein genes (hsp90 and hsc70) and their expression during larval diapause and cold tolerance acquisition in the rice stem borer, Chilo suppressalis Walker. Arch Insect Biochem Physiol 63:36–47PubMedCrossRefGoogle Scholar
  146. Storey JM, Storey KB (1981) Biochemical strategies of overwintering in the gall fly larva, Eurosta solidaginis—effect of low-temperature acclimation on the activities of enzymes of intermediary metabolism. J Comp Physiol 144:191–199Google Scholar
  147. Storey JM, Storey KB (1986) Winter survival of the gall fly larvae, Eurosta solidaginis: profiles of fuel reserves and cryoprotectants in a natural population. J Insect Physiol 32:549–556CrossRefGoogle Scholar
  148. Storey KB (1997) Organic solutes if freeze tolerance. Comp Biochem Physiol A 117:319–326CrossRefGoogle Scholar
  149. Storey KB, Storey JM (1991) Glucose-6-phosphate-dehydrogenase in cold hardy insects—kinetic-properties, freezing stabilization, and control of hexose-monophosphate shunt activity. Insect Biochem 21:157–164CrossRefGoogle Scholar
  150. Storey KB, Storey JM (1996) Natural freezing survival in animals. Ann Rev Ecol Syst 27:365–386CrossRefGoogle Scholar
  151. Stronach BE, Siegrist SE, Beckerle MC (1996) Two muscle-specific LIM proteins in Drosophila. J Cell Biol 134:1179–1195PubMedCrossRefGoogle Scholar
  152. Tachibana SI, Numata H, Goto SG (2005) Gene expression of the heat shock proteins (Hsp23, Hsp70 and Hsp90) during and after larval diapause in the blow fly Lucilia sericata. J Insect Physiol 51:641–647PubMedCrossRefGoogle Scholar
  153. Tammariello SP, Rinehart JP, Denlinger DL (1999) Desiccation elicits heat shock protein transcription in the flesh fly Sarcophaga crassipalpis, but does not enhance tolerance to high or low temperatures. J Insect Physiol 45:933–938PubMedCrossRefGoogle Scholar
  154. The C. elegans Sequencing Consortium (1998) The genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282:2012–2018CrossRefGoogle Scholar
  155. Thibaud JM (1968) Cycle de tube digestif lors de l’intermue chez les Hypogastruridae (Collemboles) épigés et cavernicoles. Rev Ecol Biol Sol 4:647–655Google Scholar
  156. Tiku PE, Gracey AY, Macartney AI, Beynon RJ, Cossins AR (1996) Cold-induced expression of Delta(9)-desaturase in carp by transcriptional and posttranslational mechanisms. Science 271:815–818PubMedCrossRefGoogle Scholar
  157. Timmermans MJTN, Ellers J, Van Straalen NM (2007) Allelic diversity of metallothionein in Orchesella cincta (L): traces of natural selection by environmental pollution. Heredity 98:311–319PubMedCrossRefGoogle Scholar
  158. Tomanek L, Somero GN (1999) Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of thermotolerance and biogeography. J Exp Biol 202:2925–2936PubMedGoogle Scholar
  159. Tomcala A, Tollarova M, Overgaard J, Simek P, Koštál V (2006) Seasonal acquisition of chill tolerance and restructuring of membrane glycerophospholipids in an overwintering insect: triggering by low temperature, desiccation and diapause progression. J Exp Biol 209:4102–4114PubMedCrossRefGoogle Scholar
  160. Tursman D, Duman JG, Knight CA (1994) Freeze tolerance adaptations in the centipede, Lithobius forficatus. J Exp Zool 268:347–353CrossRefGoogle Scholar
  161. Tyshenko MG, Doucet D, Walker VK (2005) Analysis of antifreeze proteins within spruce budworm sister species. Insect Mol Biol 14:319–326PubMedCrossRefGoogle Scholar
  162. Tyshenko MG, Walker VK (2004) Hyperactive spruce budworm antifreeze expression in transgenic Drosophila does not confer cold shock tolerance. Cryobiology 49:28–36PubMedCrossRefGoogle Scholar
  163. Vega SE, del Rio AH, Bamberg JB, Palta JP (2004) Evidence for the up-regulation of stearoyl-ACP (A9) desaturase gene expression during cold acclimation. Am J Potato Res 81:125–135Google Scholar
  164. Whyard S, Wyatt GR, Walker VK (1986) The heat shock response in Locusta migratoria. J Comp Physiol B 156:813–817CrossRefGoogle Scholar
  165. Worland MR (2005) Factors that influence freezing in the sub-Antarctic springtail Tullbergia antarctica. J Insect Physiol 51:881–894PubMedCrossRefGoogle Scholar
  166. Worland MR, Lukešovà A (2000) The effect of feeding on specific soil algae on the cold hardiness of two Antarctic micro-arthropods (Alaskozetes antarcticus and Cryptopygus antarcticus). Polar Biol 23:766–774CrossRefGoogle Scholar
  167. Worland MR, Convey P (2001) Rapid cold hardening in Antarctic microarthropods. Funct Ecol 15:515–524CrossRefGoogle Scholar
  168. Worland MR, Grubor-Lajsic G, Montiel PO (1998) Partial desiccation induced by sub-zero temperatures as a component of the survival strategy of the Arctic collembolan Onychiurus arcticus (Tullberg). J Insect Physiol 44:211–219PubMedCrossRefGoogle Scholar
  169. Worland MR, Leinaas HP, Chown SL (2006) Supercooling point frequency distributions in Collembola are affected by moulting. Funct Ecol 20:323–329CrossRefGoogle Scholar
  170. Wu DW, Duman JG (1991) Activation of antifreeze proteins from larvae of the beetle Dendroides canadensis. J Com Physiol B 161:279–283CrossRefGoogle Scholar
  171. Wyatt GR (1963) The biochemistry of insect hemolymph. Annu Rev Entomol 6:75–102CrossRefGoogle Scholar
  172. Xu WH, Denlinger DL (2003) Molecular characterization of prothoracicotropic hormone and diapause hormone in Heliothis virescens during diapause, and a new role for diapause hormone. Insect Mol Biol 12:509–516PubMedCrossRefGoogle Scholar
  173. Yamashita O (1996) Diapause hormone of the silk moth Bombyx mori, structure, gene expression and function. J Insect Physiol 42:669–679CrossRefGoogle Scholar
  174. Yocum GD (2001) Differentiual expression of two HSP70 transcripts in response to cold shock, thermoperiod, and adult diapause in the Colorado potato beetle. J Insect Physiol 47:1139–1145PubMedCrossRefGoogle Scholar
  175. Yocum GD, Joplin KH, Denlinger DL (1998) Expression of heat-shock proteins in response to high and low temperature extremes in diapausing pharate larvae of the gypsy moth, Lymantria dispar. Arch Insect Biochem Physiol 18:239–249CrossRefGoogle Scholar
  176. Yocum GD, Kemp WP, Bosch J, Knoblett JN (2005) Temporal variation in overwintering gene expression and respiration in the solitary bee Megachile rotundata. J Insect Physiol 51:621–629PubMedCrossRefGoogle Scholar
  177. Yoshiga T, Okano K, Mita K, Shimada T, Matsumoto S (2000) cDNA cloning of acyl-CoA desaturase homologs in the silkworm, Bombyx mori. Gene 246:339–345PubMedCrossRefGoogle Scholar
  178. Zachariassen KE (1991) The water relations of overwintering insects. In: Lee RE, Denlinger DL (eds) Insects at low temperature. Chapman and Hall, London, pp 47–63Google Scholar
  179. Zachariassen KE, Hammel HT (1976) Nucleating agents in the haemolymph of insects tolerant to freezing. Nature 262:285–287PubMedCrossRefGoogle Scholar

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© Springer-Verlag 2008

Authors and Affiliations

  1. 1.British Antarctic SurveyNatural Environment Research CouncilCambridgeUK

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