Skip to main content
Log in

How insects survive the cold: molecular mechanisms—a review

  • Review
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • 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 287:2185–2195

    Article  PubMed  Google Scholar 

  • 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–F476

    CAS  Google Scholar 

  • Andorfer CA, Duman JG (2000) Isolation and characterization of cDNA clones encoding antifreeze proteins of the pyrochroid beetle Dendroides canadensis. J Insect Physiol 46:365–372

    Article  PubMed  CAS  Google Scholar 

  • Arber S, Halder G, Caroni P (1994) Muscle LIM protein, a novel regulator of myogenesis, promotes myogenic differentiation. Cell 79:221–231

    Article  PubMed  CAS  Google Scholar 

  • Bale JS (1993) Classes of insect cold hardiness. Funct Ecol 7:751–753

    Google Scholar 

  • Bale JS (2002) Insects and low temperatures: from molecular biology to distributions and abundance. Philos Trans R Soc B 357:849–861

    Article  CAS  Google Scholar 

  • 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 47:1197–1204

    Article  PubMed  CAS  Google Scholar 

  • 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 167:249–255

    Article  CAS  Google Scholar 

  • Bennett VA, Lee RE, Nauman JS, Kukal O (2003) Selection of overwintering microhabitats used by the Arctic woolybear caterpillar, Gynaephora groenlandica. Cryoletters 24:191–200

    PubMed  Google Scholar 

  • 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 3:11–20

    Article  CAS  Google Scholar 

  • Cannon RJC, Block W (1988) Cold tolerance of microarthropods. Biol Rev 63:23–77

    Article  Google Scholar 

  • Chen CP, Denlinger DL (1992) Reduction of cold injury in flies using an intermittent pulse of high-temperature. Cryobiology 29:138–143

    Article  Google Scholar 

  • Chen CP, Denlinger DL, Lee RE (1987) Cold-shock injury and rapid cold hardening in the flesh fly, Sarcophaga crassipalpis. Physiol Zool 60:297–304

    Google Scholar 

  • Chen LB, DeVries AL, Cheng CHC (1997) Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod. Proc Natl Acad Sci USA 94:3817–3822

    Article  PubMed  CAS  Google Scholar 

  • 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 14:697–702

    Article  PubMed  CAS  Google Scholar 

  • Chino CP (1957) Conversion of glycogen to sorbitol and glycerol in the diapause egg of the Bombyx silkworm. Nature 180:606–607

    Article  CAS  Google Scholar 

  • Chown SL, Terblanche JS (2007) Physiological diversity in insects: ecological and evolutionary contexts. Adv Insect Physiol 33:50–152

    Article  Google Scholar 

  • 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

  • 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

  • Cohet Y, Vouidibio J, David JR (1980) Thermal tolerance and geographical-distribution: a comparison of cosmopolitan and tropical endemic Drosophila species. J Therm Biol 5:69–74

    Article  Google Scholar 

  • 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 37:1177–1188

    Article  CAS  Google Scholar 

  • Convey P (1996) The influence of environmental characteristics on life history attributes of Antarctic terrestrial biota. Biol Rev 71:191–225

    Article  Google Scholar 

  • Convey P (2000) How does cold constrain life cycles of terrestrial plants and animals? Cryoletters 21:73–82

    Google Scholar 

  • Cossins AR (ed) (1994) Temperature adaptations of biological membranes. Portland Press, London

  • Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599

    Article  PubMed  CAS  Google Scholar 

  • Czajka MC, Lee RE (1990) A rapid cold-hardening response protecting against cold shock injury in Drosophila melanogaster. J Exp Biol 148:245–254

    PubMed  CAS  Google Scholar 

  • 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 97:9449–9454

    Article  PubMed  CAS  Google Scholar 

  • Danks HV (2005) Key themes in the study of seasonal adaptations in insects I. Patterns of cold hardiness. Appl Entomol Zool 40:199–211

    Article  Google Scholar 

  • Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93–122

    Article  PubMed  CAS  Google Scholar 

  • DeVries AL (1971) Glycoproteins as biological antifreeze agents in Antarctic fishes. Science 172:1152

    Article  PubMed  CAS  Google Scholar 

  • Diabo S, Kimura MT, Goto SG (2001) Upregulation of genes belonging to the drosomycin family in diapausing adults of Drosophila triauraria. Gene 278:177–184

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 265:432–437

    Article  PubMed  CAS  Google Scholar 

  • Duman JG (1977) Role of macromolecular antifreeze in the darkling beetle Meracantha contracta. J Comp Physiol 115:279–286

    CAS  Google Scholar 

  • Duman JG (2001) Antifreeze and ice nucleator proteins in terrestrial arthropods. Annu Rev Physiol 63:327–357

    Article  PubMed  CAS  Google Scholar 

  • Duman JG, Bennett T, Sformo T, Hochstrasser R, Barnes BM (2004) Antifreeze proteins in Alaskan insects and spiders. J Insect Physiol 50:259–266

    Article  PubMed  CAS  Google Scholar 

  • Duman JG, DeVries AL (1974) Effects of temperature and photoperiod on antifreeze production in cold water fishes. J Exp Biol 190:89–97

    CAS  Google Scholar 

  • 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 168:225–232

    Article  PubMed  CAS  Google Scholar 

  • 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 11:533–542

    Article  PubMed  CAS  Google Scholar 

  • 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:137–147

    Article  CAS  Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282

    Article  PubMed  CAS  Google Scholar 

  • Fink AL (1999) Chaperone-mediated protein folding. Physiol Rev 79:425–449

    PubMed  CAS  Google Scholar 

  • Forge TA, MacGuidwin AE (1992) Effects of water potential and temperature on survival of the nematode Meloidogyne hapla in frozen soil. Can J Zool 70:1553–1560

    Article  Google Scholar 

  • 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 80:45–72

    Article  PubMed  Google Scholar 

  • 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 210:3295–3300

    Article  PubMed  CAS  Google Scholar 

  • 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 36:47–53

    Article  PubMed  CAS  Google Scholar 

  • Gaston KJ, Chown SL, Evans KL (2008) Ecogeographical rules: elements of a synthesis. J Biogeogr 35:483–500

    Article  Google Scholar 

  • 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 47:759–766

    Article  PubMed  CAS  Google Scholar 

  • Goto SG (2000) Expression of Drosophila homologue of senescence marker protein-30 during cold acclimation. J Insect Physiol 46:1111–1120

    Article  PubMed  CAS  Google Scholar 

  • Goto SG (2001) A novel gene that is upregulated during recovery from cold shock in Drosophila melanogaster. Gene 270:259–264

    Article  PubMed  CAS  Google Scholar 

  • Goto SG, Kimura MT (1998) Heat and cold-shock responses and temperature adaptations in subtropical and temperate species of Drosophila. J Insect Physiol 44:1233–1239

    Article  PubMed  CAS  Google Scholar 

  • Goto SG, Kimura MT (2004) Heat shock responsive gene are not involved in the adult diapause of Drosophila triauraria. Gene 326:117–122

    Article  PubMed  CAS  Google Scholar 

  • 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 44:1009–1015

    Article  PubMed  CAS  Google Scholar 

  • Graham LA, Davies PL (2005) Glycine-rich antifreeze proteins from snow fleas. Science 310:461

    Article  PubMed  Google Scholar 

  • Graham LA, Bendena WG, Walker VK (1996) Juvenile hormone regulation and developmental expression of a Tenebrio desiccation stress protein gene. Dev Genet 18:296–305

    Article  PubMed  CAS  Google Scholar 

  • Graham LA, Liou YC, Walker VK, Davies PL (1997) Hyperactive antifreeze protein from beetles. Nature 388:727–728

    Article  PubMed  CAS  Google Scholar 

  • 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 38:54–65

    Article  CAS  Google Scholar 

  • Hayakawa Y (1985) Activation of insect fat-body phosphorylase by cold-phosphorylase-kinase, phosphatase and ATP level. Insect Biochem 15:123–128

    Article  CAS  Google Scholar 

  • Hayward SAL, Rinehart JP, Denlinger DL (2004) Desiccation and rehydration elicit distinct heat shock protein transcript response in flesh fly. J Exp Biol 207:963–971

    Article  PubMed  CAS  Google Scholar 

  • 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 51:631–640

    Article  PubMed  CAS  Google Scholar 

  • 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 210:836–844

    Article  PubMed  CAS  Google Scholar 

  • Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381:571–580

    Article  PubMed  CAS  Google Scholar 

  • 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

  • Hoffmann AA (1990) Acclimation for desiccation resistance in Drosophila melanogaster and the association between acclimation response and genetic-variation. J Insect Physiol 36:885–891

    Article  Google Scholar 

  • Hofmann GE (2005) Patterns of Hsp gene expression in exothermic marine organisms on small to large biogeographic scales. Integr Comp Biol 45:247–255

    Article  CAS  Google Scholar 

  • Hoffmann AA, Parsons PA (1993) Selection for adult desiccation resistance in Drosophila melanogaster—fitness components, larval resistance and stress tolerance. Biol J Linn Soc 48:43–54

    Article  Google Scholar 

  • Hoffmann AA, Sørensen JG, Loeschoke V (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J Therm Biol 28:175–213

    Article  Google Scholar 

  • 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 48:961–970

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hosier JS, Burns JE, Esch HE (2000) Flight muscle resting potential and species-specific differences in chill coma. J Insect Physiol 46:621–627

    Article  Google Scholar 

  • 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 16:491–500

    Article  PubMed  CAS  Google Scholar 

  • 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 50:333–344

    Article  PubMed  CAS  Google Scholar 

  • Joanisse DR, Storey KB (1994a) Enzyme-activity profiles in and overwintering population of freeze-avoiding gall moth larvae, Epiblema scudderiana. Can J Zool 72:1079–1086

    Article  CAS  Google Scholar 

  • 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 164:247–255

    Article  CAS  Google Scholar 

  • 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 36:239–249

    Article  CAS  Google Scholar 

  • 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 10:204–210

    Article  CAS  Google Scholar 

  • 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 37:1160–1167

    Article  PubMed  CAS  Google Scholar 

  • 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 37:1160–1167

    Article  PubMed  CAS  Google Scholar 

  • Kelty JD, Lee RE (1999) Induction of rapid cold hardening by cooling at ecologically relevant rates in Drosophila melanogaster. J Insect Physiol 45:719–726

    Article  PubMed  CAS  Google Scholar 

  • Kelty JD, Lee RE (2001) Rapid cold-hardening of Drosophila melanogaster (Diptera: Drosophilidae) during ecologically based thermoperiodic cycles. J Exp Biol 204:1659–1666

    PubMed  CAS  Google Scholar 

  • 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 52:1189–1193

    Article  PubMed  CAS  Google Scholar 

  • 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 348:56–61

    Article  CAS  Google Scholar 

  • 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 52:1226–1233

    Article  PubMed  CAS  Google Scholar 

  • Knight CA, Duman JG (1986) Inhibition of recrystallization by insect thermal hysteresis proteins—a possible cryoprotective role. Cryobiol 23:256–262

    Article  CAS  Google Scholar 

  • 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 135:407–419

    Article  PubMed  CAS  Google Scholar 

  • 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 207:1509–1521

    Article  PubMed  Google Scholar 

  • 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 147:231–238

    Article  CAS  Google Scholar 

  • Kruse E, Uehlein N, Kaldenhoff R (2006) The aquaporins. Genome Biol 7:206. doi:10.1186/gb-2006-7-2-206

    Article  PubMed  CAS  Google Scholar 

  • 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 276–300

    Google Scholar 

  • Kukal O, Duman JG, Serianni AS (1989) Cold-induced mitochondrial degradation and cryoprotectants synthesis in freeze-tolerant Arctic caterpillars. J Comp Physiol B 158:661–671

    Article  PubMed  CAS  Google Scholar 

  • 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 274:1759–1767

    Article  PubMed  CAS  Google Scholar 

  • Lee RE, Denlinger DL (1991) Insects at low temperature. Chapman and Hall, London

    Google Scholar 

  • Lee RE, Chen CP, Meacham MH, Denlinger DL (1987) Ontogenic patterns of cold-hardiness and glycerol production in Sarcophaga crassipalpis. J Insect Physiol 33:587–592

    Article  CAS  Google Scholar 

  • Lee RE, Strong-Gunderson JM, Lee MR, Grove KS, Riga TJ (1991) Isolation of ice nucleating active bacteria from insects. J Exp Zool 257:124–127

    Article  Google Scholar 

  • 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 12:281–289

    Article  PubMed  CAS  Google Scholar 

  • 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 48:887–901

    Article  PubMed  CAS  Google Scholar 

  • 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 53:385–391

    Article  PubMed  CAS  Google Scholar 

  • 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 29:435–443

    Article  PubMed  CAS  Google Scholar 

  • Michaud MR, Denlinger DL (2004) Molecular modalities of insect cold survival: current understanding and future trends. Int Congress Ser 1275:32–46

    Article  CAS  Google Scholar 

  • 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 52:1073–1082

    Article  PubMed  CAS  Google Scholar 

  • 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 177:753–763

    Article  PubMed  CAS  Google Scholar 

  • 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 12:3788–3796

    Article  PubMed  CAS  Google Scholar 

  • 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 280:99–106

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 27:416–422

    Google Scholar 

  • Nicodemus J, O’Tousa JE, Duman JG (2006) Expression of a beetle, Dendroides canadensis, antifreeze protein in Drosophila melanogaster. J Insect Physiol 52:888–896

    Article  PubMed  CAS  Google Scholar 

  • 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 51:1320–1329

    Article  PubMed  CAS  Google Scholar 

  • Nordin JH, Cui Z, Yin C-M (1984) Cold-induced glycerol accumulation by Ostrinia nubilalis larvae is developmentally regulated. J Insect Physiol 30:563–566

    Article  CAS  Google Scholar 

  • 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 16:3274–3284

    Article  PubMed  CAS  Google Scholar 

  • 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 113:73–77

    Article  Google Scholar 

  • Ohtsu T, Kimura MT, Katagiri C (1998) How Drosophila species acquire cold tolerance—qualitative changes of phospholipids. Eur J Biochem 252:608–611

    Article  PubMed  CAS  Google Scholar 

  • 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 12:1218–1232

    Article  CAS  Google Scholar 

  • Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance, degradation and reactivation of damaged proteins. Ann Rev Genet 27:437–496

    Article  PubMed  CAS  Google Scholar 

  • 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 32:505–515

    Article  PubMed  CAS  Google Scholar 

  • Pfister TD, Storey KB (2006) Insect freeze tolerance: roles of protein phosphatases and protein kinase A. Insect Biochem Mol Biol 36:18–24

    Article  PubMed  CAS  Google Scholar 

  • 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 30:1147–1159

    Article  PubMed  CAS  Google Scholar 

  • 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–R436

    CAS  Google Scholar 

  • Privalov PL (1990) Cold denaturation of proteins. Crit Rev Biochem Mol Biol 25:281–305

    Article  PubMed  CAS  Google Scholar 

  • Qin W, Neal SJ, Robertson RM, Westwood JT, Walker VK (2005) Cold hardening and transcriptional change in Drosophila melanogaster. Insect Mol Biol 14:607–613

    Article  PubMed  CAS  Google Scholar 

  • Qin W, Doucet D, Tyshenko MG, Walker VK (2007) Transcription of antifreeze protein genes in Choristoneura fumiferana. Insect Mol Biol 16:423–434

    Article  PubMed  CAS  Google Scholar 

  • 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 16:2948–2957

    CAS  Google Scholar 

  • Raymond JA, DeVries AL (1977) Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proc Natl Acad Sci USA 74:2589–2593

    Article  PubMed  CAS  Google Scholar 

  • 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 9:641–645

    Article  PubMed  CAS  Google Scholar 

  • 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 30:515–521

    Article  PubMed  CAS  Google Scholar 

  • 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 103:14225–14227

    Article  CAS  Google Scholar 

  • 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 43:713–722

    Article  PubMed  CAS  Google Scholar 

  • 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 104:11130–11137

    Article  PubMed  CAS  Google Scholar 

  • 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 3–16

    Google Scholar 

  • Ring RA, Danks HV (1994) Desiccation and cryoprotection—overlapping adaptations. Cryoletters 15:181–190

    Google Scholar 

  • Russell NJ (1997) Psychrophilic bacteria—molecular adaptations of membrane lipids. Comp Biochem Physiol A 118:489–493

    Article  CAS  Google Scholar 

  • 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 23:1281–1292

    Article  PubMed  CAS  Google Scholar 

  • Salt RW (1957) Natural occurrence of glycerol in insects and its relation to their ability to survive freezing. Can Entomol 89:491–494

    Article  CAS  Google Scholar 

  • Salt RW (1959) Role of glycerol in the cold-hardening of Bracon cephi (Gahan). Can J Zool 37:59–69

    CAS  Google Scholar 

  • Salt RW (1961) Principles of insect cold hardiness. Annu Rev Entomol 6:55–74

    Article  Google Scholar 

  • Salt RW (1966) Factors influencing nucleation in supercooled insects. Can J Zool 44:117–133

    Article  Google Scholar 

  • 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 25:363–371

    Article  CAS  Google Scholar 

  • Scotter AJ, Marshall CB, Graham LA, Gilbert JA, Garnham CP, Davies PL (2006) The basis for hyperactivity of antifreeze proteins. Cryobiology 53:229–239

    Article  PubMed  CAS  Google Scholar 

  • Sinclair BJ, Stevens MI (2006) Terrestrial microarthropods of Victoria Land and Queen Maud Mountains, Antarctica: implications of climate change. Soil Biol Biochem 38:3158–3170

    Article  CAS  Google Scholar 

  • 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 16:435–443

    Article  PubMed  CAS  Google Scholar 

  • Slachta M, Berkova P, Vambera J, Koštál V (2002) Physiology of cold-acclimation in non-diapausing adults of Pyrrhocoris apterus (Heteroptera). Eur J Entomol 99:181–187

    Google Scholar 

  • Sømme L (1982) Supercooling and winter survival in terrestrial arthropods. Comp Biochem Physiol A 73:519–543

    Article  Google Scholar 

  • Sømme L (1999) The physiology of cold hardiness in terrestrial arthropods. Eur J Entomol 96:1–10

    Google Scholar 

  • Sømme L, Block W (1982) Cold hardiness of Collembola at Signy Island, maritime Antarctic. Oikos 38:68–176

    Article  Google Scholar 

  • 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 15:853–859

    Article  PubMed  Google Scholar 

  • 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 63:36–47

    Article  PubMed  CAS  Google Scholar 

  • 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 144:191–199

    CAS  Google Scholar 

  • 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 32:549–556

    Article  CAS  Google Scholar 

  • Storey KB (1997) Organic solutes if freeze tolerance. Comp Biochem Physiol A 117:319–326

    Article  CAS  Google Scholar 

  • 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 21:157–164

    Article  CAS  Google Scholar 

  • Storey KB, Storey JM (1996) Natural freezing survival in animals. Ann Rev Ecol Syst 27:365–386

    Article  Google Scholar 

  • Stronach BE, Siegrist SE, Beckerle MC (1996) Two muscle-specific LIM proteins in Drosophila. J Cell Biol 134:1179–1195

    Article  PubMed  CAS  Google Scholar 

  • 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 51:641–647

    Article  PubMed  CAS  Google Scholar 

  • 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 45:933–938

    Article  PubMed  CAS  Google Scholar 

  • The C. elegans Sequencing Consortium (1998) The genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282:2012–2018

    Article  Google Scholar 

  • Thibaud JM (1968) Cycle de tube digestif lors de l’intermue chez les Hypogastruridae (Collemboles) épigés et cavernicoles. Rev Ecol Biol Sol 4:647–655

    Google Scholar 

  • 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 271:815–818

    Article  PubMed  CAS  Google Scholar 

  • Timmermans MJTN, Ellers J, Van Straalen NM (2007) Allelic diversity of metallothionein in Orchesella cincta (L): traces of natural selection by environmental pollution. Heredity 98:311–319

    Article  PubMed  CAS  Google Scholar 

  • 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 202:2925–2936

    PubMed  Google Scholar 

  • 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 209:4102–4114

    Article  PubMed  CAS  Google Scholar 

  • Tursman D, Duman JG, Knight CA (1994) Freeze tolerance adaptations in the centipede, Lithobius forficatus. J Exp Zool 268:347–353

    Article  Google Scholar 

  • Tyshenko MG, Doucet D, Walker VK (2005) Analysis of antifreeze proteins within spruce budworm sister species. Insect Mol Biol 14:319–326

    Article  PubMed  CAS  Google Scholar 

  • Tyshenko MG, Walker VK (2004) Hyperactive spruce budworm antifreeze expression in transgenic Drosophila does not confer cold shock tolerance. Cryobiology 49:28–36

    Article  PubMed  CAS  Google Scholar 

  • 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 81:125–135

    CAS  Google Scholar 

  • Whyard S, Wyatt GR, Walker VK (1986) The heat shock response in Locusta migratoria. J Comp Physiol B 156:813–817

    Article  Google Scholar 

  • Worland MR (2005) Factors that influence freezing in the sub-Antarctic springtail Tullbergia antarctica. J Insect Physiol 51:881–894

    Article  PubMed  CAS  Google Scholar 

  • 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 23:766–774

    Article  Google Scholar 

  • Worland MR, Convey P (2001) Rapid cold hardening in Antarctic microarthropods. Funct Ecol 15:515–524

    Article  Google Scholar 

  • 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 44:211–219

    Article  PubMed  CAS  Google Scholar 

  • Worland MR, Leinaas HP, Chown SL (2006) Supercooling point frequency distributions in Collembola are affected by moulting. Funct Ecol 20:323–329

    Article  Google Scholar 

  • Wu DW, Duman JG (1991) Activation of antifreeze proteins from larvae of the beetle Dendroides canadensis. J Com Physiol B 161:279–283

    Article  CAS  Google Scholar 

  • Wyatt GR (1963) The biochemistry of insect hemolymph. Annu Rev Entomol 6:75–102

    Article  Google Scholar 

  • 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 12:509–516

    Article  PubMed  CAS  Google Scholar 

  • Yamashita O (1996) Diapause hormone of the silk moth Bombyx mori, structure, gene expression and function. J Insect Physiol 42:669–679

    Article  CAS  Google Scholar 

  • 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 47:1139–1145

    Article  PubMed  CAS  Google Scholar 

  • 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 18:239–249

    Article  Google Scholar 

  • 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 51:621–629

    Article  PubMed  CAS  Google Scholar 

  • Yoshiga T, Okano K, Mita K, Shimada T, Matsumoto S (2000) cDNA cloning of acyl-CoA desaturase homologs in the silkworm, Bombyx mori. Gene 246:339–345

    Article  PubMed  CAS  Google Scholar 

  • Zachariassen KE (1991) The water relations of overwintering insects. In: Lee RE, Denlinger DL (eds) Insects at low temperature. Chapman and Hall, London, pp 47–63

    Google Scholar 

  • Zachariassen KE, Hammel HT (1976) Nucleating agents in the haemolymph of insects tolerant to freezing. Nature 262:285–287

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Melody S. Clark.

Additional information

Communicated by I.D. Hume.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Clark, M.S., Worland, M.R. How insects survive the cold: molecular mechanisms—a review. J Comp Physiol B 178, 917–933 (2008). https://doi.org/10.1007/s00360-008-0286-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-008-0286-4

Keywords

Navigation