Cold tolerance is important in defining the distribution of insects. Here, we review the principal physiological mechanisms underlying homeostatic failure during cold exposure in this diverse group of ectotherms. When insects are cooled sufficiently, they suffer an initial loss of neuromuscular function (chill coma) that is caused by decreased membrane potential and reduced excitability of the neuromuscular system. For chill-susceptible insects, chronic or severe chilling causes a disruption of ion and water homeostasis across membranes and epithelia that exacerbate the initial effects of chilling on membrane potential and cellular function, and these perturbations are tightly associated with the development of chill injury and mortality. The adaptation and acclimation responses that allow some insects to tolerate low temperatures are multifactorial and involve several physiological systems and biochemical adjustments. In this review, we outline a physiological model that integrates several of these responses and discuss how they collectively help to preserve cellular, organ, and organismal homeostasis at low temperature.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Chown SL, Terblanche JS. 1.  2006. Physiological diversity in insects: ecological and evolutionary contexts. Adv. Insect Physiol. 33:50–152 [Google Scholar]
  2. Harrison JF, Woods HA, Roberts SP. 2.  2012. Ecological and Environmental Physiology of Insects New York: Oxford Univ. Press
  3. Chown SL, Nicolson S. 3.  2004. Insect Physiological Ecology New York: Oxford Univ. Press
  4. Addo-Bediako A, Chown SL, Gaston KJ. 4.  2000. Thermal tolerance, climatic variability and latitude. Proc. R. Soc. B 267:739–45 [Google Scholar]
  5. Bale JS. 5.  2002. Insects and low temperatures: from molecular biology to distributions and abundance. Phil. Trans. R. Soc. B 357:849–62 [Google Scholar]
  6. Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK. 6.  et al. 2008. Impacts of climate warming on terrestrial ectotherms across latitude. PNAS 105:6668–72 [Google Scholar]
  7. Kimura MT. 7.  2004. Cold and heat tolerance of drosophilid flies with reference to their latitudinal distributions. Oecologia 140:442–49 [Google Scholar]
  8. Overgaard J, Kearney MR, Hoffmann AA. 8.  2014. Sensitivity to thermal extremes in Australian Drosophila implies similar impacts of climate change on the distribution of widespread and tropical species. Glob. Change Biol 20:1738–50 [Google Scholar]
  9. Sunday JM, Bates AE, Dulvy NK. 9.  2010. Global analysis of thermal tolerance and latitude in ectotherms. Proc. R. Soc. B 278:1823–30 [Google Scholar]
  10. Hazell SP, Groutides C, Neve BP, Blackburn TM, Bale JS. 10.  2010. A comparison of low temperature tolerance traits between closely related aphids from the tropics, temperate zone, and Arctic. J. Insect Physiol. 56:115–22 [Google Scholar]
  11. Kellermann V, Loeschcke V, Hoffmann AA, Kristensen TN, Fløjgaard C. 11.  et al. 2012. Phylogenetic constraints in key functional traits behind species’ climate niches: patterns of desiccation and cold resistance across 95 Drosophila species. Evolution 66:3377–89 [Google Scholar]
  12. Payne NM. 12.  1926. The effect of environmental temperatures upon insect freezing points. Ecology 7:99–106 [Google Scholar]
  13. Mellanby K. 13.  1939. Low temperature and insect activity. Proc. R. Soc. B 127:473–87 [Google Scholar]
  14. Salt RW. 14.  1961. Principles of insect cold-hardiness. Annu. Rev. Entomol. 6:55–74 [Google Scholar]
  15. Zachariassen KE. 15.  1985. Physiology of cold tolerance in insects. Physiol. Rev. 65:799–832 [Google Scholar]
  16. Bale J. 16.  1987. Insect cold hardiness: freezing and supercooling—an ecophysiological perspective. J. Insect Physiol. 33:899–908 [Google Scholar]
  17. MacMillan HA, Sinclair BJ. 17.  2011. Mechanisms underlying insect chill-coma. J. Insect Physiol. 57:12–20 [Google Scholar]
  18. Sinclair BJ, Vernon P, Jaco Klok C, Chown SL. 18.  2003. Insects at low temperatures: an ecological perspective. Trends Ecol. Evol. 18:257–62 [Google Scholar]
  19. Holmstrup M, Bayley M, Ramløv H. 19.  2002. Supercool or dehydrate? An experimental analysis of overwintering strategies in small permeable arctic invertebrates. PNAS 99:5716–20 [Google Scholar]
  20. Teets NM, Denlinger DL. 20.  2013. Physiological mechanisms of seasonal and rapid cold-hardening in insects. Physiol. Entomol. 38:105–16A comprehensive review on the molecular mechanisms of cold-tolerance plasticity in insects. [Google Scholar]
  21. Hayward SAL, Manso B, Cossins AR. 21.  2014. Molecular basis of chill resistance adaptations in poikilothermic animals. J. Exp. Biol. 217:6–15 [Google Scholar]
  22. Sømme L. 22.  1982. Supercooling and winter survival in terrestrial arthropods. Comp. Biochem. Physiol. 73A:519–43 [Google Scholar]
  23. Lee RE, Denlinger DL. 23.  1991. Insects at Low Temperature New York/London: Chapman & Hall
  24. Duman JG. 24.  2001. Antifreeze and ice nucleator proteins in terrestrial arthropods. Annu. Rev. Physiol. 63:327–35 [Google Scholar]
  25. Bale JS. 25.  1996. Insect cold hardiness: a matter of life and death. Eur. J. Entomol. 93:369–82One of the first reviews to discuss the separation of insect cold-tolerance strategies. [Google Scholar]
  26. Sinclair BJ. 26.  1999. Insect cold tolerance: How many kinds of frozen?. Eur. J. Entomol. 96:157–64 [Google Scholar]
  27. Nedved O. 27.  2000. Snow White and the Seven Dwarfs: a multivariate approach to classification of cold tolerance. Cryo Lett 21:339–48 [Google Scholar]
  28. Sinclair BJ, Coello Alvarado LE, Ferguson LV. 28.  2015. An invitation to measure insect cold tolerance: methods, approaches, and workflow. J. Therm. Biol. 53:180–97 [Google Scholar]
  29. Hazell SP, Bale JS. 29.  2011. Low temperature thresholds: Are chill coma and CTmin synonymous?. J. Insect Physiol. 57:1085–89 [Google Scholar]
  30. Andersen JL, Manenti T, Sørensen JG, MacMillan HA, Loeschcke V, Overgaard J. 30.  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]
  31. Goller F, Esch H. 31.  1990. Comparative study of chill-coma temperatures and muscle potentials in insect flight muscles. J. Exp. Biol. 150:221–231Demonstrates how cooling is associated with loss of action potential amplitude in various insect species. [Google Scholar]
  32. Gibert P, Moreteau B, Pétavy G, Karan D, David JR. 32.  2001. Chill-coma tolerance, a major climatic adaption among Drosophila species. Evolution 55:1063–68 [Google Scholar]
  33. Powell SJ, Bale JS. 33.  2004. Cold shock injury and ecological costs of rapid cold hardening in the grain aphid Sitobion avenae (Hemiptera: Aphididae). J. Insect Physiol 50:277–84 [Google Scholar]
  34. Koštál V, Vambera J, Bastl J. 34.  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. 207:1509–21Clearly describes the association between ion balance disruption and onset of chill injury in insects. [Google Scholar]
  35. Jing X-H, Wang X-H, Kang L. 35.  2005. Chill injury in the eggs of the migratory locust, Locusta migratoria (Orthoptera: Acrididae): the time-temperature relationship with high-temperature interruption. Insect Sci 12:171–78 [Google Scholar]
  36. Koštál V, Yanagimoto M, Bastl J. 36.  2006. Chilling-injury and disturbance of ion homeostasis in the coxal muscle of the tropical cockroach (Nauphoeta cinerea). Comp. Biochem. Physiol. B 143:171–79 [Google Scholar]
  37. MacMillan HA, Sinclair BJ. 37.  2011. The role of the gut in insect chilling injury: cold-induced disruption of osmoregulation in the fall field cricket, Gryllus pennsylvanicus. J. Exp. Biol. 214:726–34Shows how water movement to the gut explains loss of ion balance in the hemolymph. [Google Scholar]
  38. Boardman L, Grout TG, Terblanche JS. 38.  2012. False codling moth Thaumatotibia leucotreta (Lepidoptera, Tortricidae) larvae are chill-susceptible. Insect Sci 19:315–28 [Google Scholar]
  39. Rinehart JP, Yocum GD, Denlinger DL. 39.  2000. Thermotolerance and rapid cold hardening ameliorate the negative effects of brief exposures to high or low temperatures on fecundity in the flesh fly, Sarcophaga crassipalpis. Physiol. Entomol. 25:330–36 [Google Scholar]
  40. Shreve SM, Kelty JD, Lee RE Jr. 40.  2004. Preservation of reproductive behaviors during modest cooling: rapid cold-hardening fine-tunes organismal response. J. Exp. Biol. 207:1797–802 [Google Scholar]
  41. Overgaard J, Malmendal A, Sørensen JG, Bundy JG, Loeschcke V. 41.  et al. 2007. Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. J. Insect Physiol. 53:1218–32 [Google Scholar]
  42. Chen C-P, Denlinger DL, Lee RE. 42.  1987. Cold-shock injury and rapid cold hardening in the flesh fly Sarcophaga crassipalpis. Physiol. Zool. 60:297–304 [Google Scholar]
  43. Huey RB, Crill WD, Kingsolver JG, Weber KE. 43.  1992. A method for rapid measurement of heat or cold resistance of small insects. Funct. Ecol. 6:489–94 [Google Scholar]
  44. Kelty JD, Lee REJ. 44.  2001. Rapid cold-hardening of Drosophila melanogaster (Diptera: Drosophiladae) during ecologically based thermoperiodic cycles. J. Exp. Biol 204:1659–66 [Google Scholar]
  45. Coleman PC, Bale JS, Hayward SAL. 45.  2015. Meat feeding restricts rapid cold hardening response and increases thermal activity thresholds of adult blow flies, Calliphora vicina (Diptera: Calliphoridae). PLOS ONE 10:e0131301 [Google Scholar]
  46. Rako L, Hoffmann AA. 46.  2006. Complexity of the cold acclimation response in Drosophila melanogaster. J. Insect Physiol. 52:94–104 [Google Scholar]
  47. Macdonald SS, Rako L, Batterham P, Hoffmann AA. 47.  2004. Dissecting chill coma recovery as a measure of cold resistance: evidence for a biphasic response in Drosophila melanogaster. J. Insect Physiol. 50:695–700 [Google Scholar]
  48. MacMillan HA, Andersen JL, Davies SA, Overgaard J. 48.  2015. The capacity to maintain ion and water homeostasis underlies interspecific variation in Drosophila cold tolerance. Sci. Rep. 5:18607Demonstrates a link between cold tolerance, K+ homeostasis, water balance, and capacity of Malpighian tubules in Drosophila. [Google Scholar]
  49. Hoffmann AA, Anderson A, Hallas R. 49.  2002. Opposing clines for high and low temperature resistance in Drosophila melanogaster. Ecol. Lett. 5:614–18 [Google Scholar]
  50. MacMillan HA, Findsen A, Pedersen TH, Overgaard J. 50.  2014. Cold-induced depolarization of insect muscle: differing roles of extracellular K+ during acute and chronic chilling. J. Exp. Biol. 217:2930–38 [Google Scholar]
  51. Slatyer RA, Schoville SD. 51.  2016. Physiological limits along an elevational gradient in a radiation of montane ground beetles. PLOS ONE 11:e0151959 [Google Scholar]
  52. Ransberry VE, MacMillan HA, Sinclair BJ. 52.  2011. The relationship between chill-coma onset and recovery at the extremes of the thermal window of Drosophila melanogaster. Physiol. Biochem. Zool. 84:553–59 [Google Scholar]
  53. Vannier G. 53.  1994. The thermobiological limits of some freezing intolerant insects: the supercooling and thermostupor points. Acta Oecol 15:31–42 [Google Scholar]
  54. Kohshima S. 54.  1984. A novel cold-tolerant insect found in a Himalayan glacier. Nature 310:225–27 [Google Scholar]
  55. Terblanche JS, Deere JA, Clusella-Trullas S, Janion C, Chown SL. 55.  2007. Critical thermal limits depend on methodological context. Proc. R. Soc. B 274:2935–43 [Google Scholar]
  56. Slatyer RA, Nash MA, Hoffmann AA. 56.  2015. Scale-dependent thermal tolerance variation in Australian mountain grasshoppers. Ecography 39:575–82 [Google Scholar]
  57. Hosler JS, Burns JE, Esch HE. 57.  2000. Flight muscle resting potential and species-specific differences in chill-coma. J. Insect Physiol. 46:621–27Links depolarization of resting potential to reductions in action potentials and onset of chill coma in bees and fruit flies. [Google Scholar]
  58. Andersen JL, MacMillan HA, Overgaard J. 58.  2015. Muscle membrane potential and insect chill coma. J. Exp. Biol. 218:2492–95 [Google Scholar]
  59. Wareham A, Duncan C, Bowler K. 59.  1975. Resting potential of muscle membrane of moths. Comp. Biochem. Physiol. 52A:295–98 [Google Scholar]
  60. Wareham A, Duncan C, Bowler K. 60.  1974. Resting potential of cockroach muscle membrane. Comp. Biochem. Physiol. 48A:765–97 [Google Scholar]
  61. Kelty JD, Killian KA, Lee R Jr. 61.  1996. Cold shock and rapid cold-hardening of pharate adult flesh flies (Sarcophaga crassipalpis): effects on behaviour and neuromuscular function following eclosion. Physiol Entomol 21:283–88 [Google Scholar]
  62. Esch H. 62.  1988. The effects of temperature on flight-muscle potentials in honeybees and cuculiinid winter moths. J. Exp. Biol. 135:109–17 [Google Scholar]
  63. Salkoff LB, Wyman RJ. 63.  1983. Ion currents in Drosophila flight muscles. J. Physiol. 337:687–709 [Google Scholar]
  64. Findsen A, Overgaard J, Thomas TH. 64.  2016. Reduced L-type Ca2+ current and compromised excitability induce loss of skeletal muscle function during acute cooling in locust. J. Exp. Biol. 219:2340–48 [Google Scholar]
  65. Findsen A, Pedersen TH, Petersen AG, Nielsen OB, Overgaard J. 65.  2014. Why do insects enter and recover from chill coma? Low temperature and high extracellular potassium compromise muscle function in Locusta migratoria. J. Exp. Biol. 217:1297–306Discusses processes involved in CCRT and chill coma and separate, interacting effects of low temperature and [K+] on muscle force production. [Google Scholar]
  66. Hoyle G. 66.  1953. Potassium ions and insect nerve muscle. J. Exp. Biol. 30:121–35 [Google Scholar]
  67. Frolov RV, Singh S. 67.  2013. Temperature and functional plasticity of L-type Ca2+ channels in Drosophila. Cell Calcium 54:287–94 [Google Scholar]
  68. Anderson RL, Mutchmor JA. 68.  1968. Temperature acclimation and its influence on the electrical activity of the nervous system in three species of cockroaches. J. Insect Physiol. 14:243–51 [Google Scholar]
  69. Armstrong GAB, Rodríguez EC, Robertson M. 69.  2012. Cold hardening modulates K+ homeostasis in the brain of Drosophila melanogaster during chill coma. J. Insect Physiol. 58:1511–16 [Google Scholar]
  70. Bradfisch G, Drewes C, Mutchmor J. 70.  1982. The effects of cooling on an identified reflex pathway in the cockroach (Periplaneta americana), in relation to chill-coma. J. Exp. Biol. 96:131–41 [Google Scholar]
  71. Rodgers CI, Armstrong GAB, Robertson RM. 71.  2010. Coma in response to environmental stress in the locust: a model for cortical spreading depression. J. Insect Physiol. 56:980–90Discusses how loss of ion balance in the CNS during cold exposure can cause a chill coma. [Google Scholar]
  72. Stork T, Engelen D, Krudewig A, Silies M, Bainton RJ, Klämbt C. 72.  2008. Organization and function of the blood-brain barrier in Drosophila. J. Neurosci. 28:587–97 [Google Scholar]
  73. Robertson RM. 73.  2004. Thermal stress and neural function: adaptive mechanisms in insect model systems. J. Therm. Biol. 29:351–58 [Google Scholar]
  74. Rodríguez EC, Robertson RM. 74.  2012. Protective effect of hypothermia on brain potassium homeostasis during repetitive anoxia in Drosophila melanogaster. J. Exp. Biol. 215:4157–65 [Google Scholar]
  75. Spong KE, Robertson RM. 75.  2013. Pharmacological blockade of gap junctions induces repetitive surging of extracellular potassium within the locust CNS. J. Insect Physiol. 59:1031–40 [Google Scholar]
  76. Garrett S, Rosenthal JJC. 76.  2012. RNA editing underlies temperature adaptation in K+ channels from polar octopuses. Science 335:848–51 [Google Scholar]
  77. Colinet H, Overgaard J, Com E, Sørensen JG. 77.  2013. Proteomic profiling of thermal acclimation in Drosophila melanogaster. Insect Biochem. Mol. Biol. 43:352–65 [Google Scholar]
  78. Zhang J, Marshall KE, Westwood JT, Clark MS, Sinclair BJ. 78.  2011. Divergent transcriptomic responses to repeated and single cold exposures in Drosophila melanogaster. J. Exp. Biol. 214:4021–29 [Google Scholar]
  79. MacMillan H, Knee JM, Dennis AB, Udaka H, Marshall KE. 79.  et al. 2016. Cold acclimation wholly reorganizes the Drosophila melanogaster transcriptome and metabolome. Sci. Rep 6:28999 [Google Scholar]
  80. Dawson J, Djamgoz M, Hardie J, Irving S. 80.  1989. Components of resting membrane electrogenesis in Lepidopteran skeletal-muscle. J. Insect Physiol. 35:659–66 [Google Scholar]
  81. Djamgoz M. 81.  1987. Insect muscle: intracellular ion concentrations and mechanisms of resting potential generation. J. Insect Physiol. 33:287–314 [Google Scholar]
  82. Rheuben MB. 82.  1972. The resting potential of moth muscle fibre. J. Physiol. 225:529–54Describes how membrane potential is composed of diffusion potential and electrogenic potential in the moth. [Google Scholar]
  83. Fitzgerald EM, Djamgoz MBA, Dunbar SJ. 83.  1996. Maintenance of the K+ activity gradient in insect muscle compared in Diptera and Lepidoptera: contributions of metabolic and exchanger mechanisms. J. Exp. Biol 199:1857–72 [Google Scholar]
  84. Coello Alvarado LE, MacMillan HA, Sinclair BJ. 84.  2015. Chill-tolerant Gryllus crickets maintain ion balance at low temperatures. J. Insect Physiol. 77:15–25 [Google Scholar]
  85. Des Marteaux LE, Sinclair BJ. 85.  2016. Ion and water balance in Gryllus crickets during the first twelve hours of cold exposure. J. Insect Physiol. 89:19–27 [Google Scholar]
  86. MacMillan HA, Andersen JL, Loeschcke V, Overgaard J. 86.  2015. Sodium distribution predicts the chill tolerance of Drosophila melanogaster raised in different thermal conditions. Am. J. Physiol. 308:R823–31 [Google Scholar]
  87. MacMillan HA, Williams CM, Staples JF, Sinclair BJ. 87.  2012. Reestablishment of ion homeostasis during chill-coma recovery in the cricket Gryllus pennsylvanicus. PNAS 109:20750–55 [Google Scholar]
  88. Zachariassen KE, Kristiansen E, Pedersen SA. 88.  2004. Inorganic ions in cold-hardiness. Cryobiology 48:126–33 [Google Scholar]
  89. Koštál V, Korbelová J, Štětina T, Poupardin R, Colinet H. 89.  et al. 2016. Physiological basis for low-temperature survival and storage of quiescent larvae of the fruit fly Drosophila melanogaster. Sci. Rep 6:32346 [Google Scholar]
  90. MacMillan HA, Schou MF, Kristensen TN, Overgaard J. 90.  2016. Preservation of potassium balance is strongly associated with insect cold tolerance in the field: a seasonal study of Drosophila subobscura. Biol. Lett. 12:20160123 [Google Scholar]
  91. Koštál V, Renault D, Mehrabianová A, Bastl J. 91.  2007. Insect cold tolerance and repair of chill-injury at fluctuating thermal regimes: role of ion homeostasis. Comp. Biochem. Physiol. 147A:231–38 [Google Scholar]
  92. MacMillan HA, Baatrup E, Overgaard J. 92.  2015. Concurrent effects of cold and hyperkalaemia cause insect chilling injury. Proc. R. Soc. B. 28220151483
  93. Hochachka PW. 93.  1986. Defense strategies against hypoxia and hypothermia. Science 231:234–41 [Google Scholar]
  94. Boutilier RG. 94.  2001. Mechanisms of cell survival in hypoxia and hypothermia. J. Exp. Biol. 204:3171–81 [Google Scholar]
  95. Yi S-X, Moore CW, Lee RE Jr. 95.  2007. Rapid cold-hardening protects Drosophila melanogaster from cold induced apoptosis. Apoptosis 12:1183–93 [Google Scholar]
  96. Bortner CD, Gómez-Angelats M, Cidlowski JA. 96.  2001. Plasma membrane depolarization without repolarization is an early molecular event in anti-fas-induced apoptosis. J. Biol. Chem. 276:4304–14 [Google Scholar]
  97. Teets NM, Yi S-X, Lee RE, Denlinger DL. 97.  2013. Calcium signaling mediates cold sensing in insect tissues. PNAS 110:9154–59 [Google Scholar]
  98. Teets NM, Elnitsky MA, Benoit JB, Lopez-Martinez G, Denlinger DL, Lee RE. 98.  2008. Rapid cold-hardening in larvae of the antarctic midge Belgica antarctica: cellular cold-sensing and a role for calcium. Am. J. Physiol. 294:R1938–46 [Google Scholar]
  99. Yi S-X, Lee RE. 99.  2011. Rapid cold-hardening blocks cold-induced apoptosis by inhibiting the activation of pro-caspases in the flesh fly Sarcophaga crassipalpis. Apoptosis 16:249–55 [Google Scholar]
  100. Gerken AR, Eller OC, Hahn DA, Morgan TJ. 100.  2015. Constraints, independence, and evolution of thermal plasticity: probing genetic architecture of long- and short-term thermal acclimation. PNAS 112:4399–404 [Google Scholar]
  101. Andersen JL, Findsen A, Overgaard J. 101.  2013. Feeding impairs chill coma recovery in the migratory locust (Locusta migratoria). J. Insect Physiol. 59:1041–48 [Google Scholar]
  102. Findsen A, Andersen JL, Calderon S, Overgaard J. 102.  2013. Rapid cold hardening improves recovery of ion homeostasis and chill coma recovery time in the migratory locust, Locusta migratoria. J. Exp. Biol. 216:1630–37 [Google Scholar]
  103. Hazel JR. 103.  1995. Thermal adaptation in biological membranes: Is homeoviscous adaptation the explanation?. Ann. Rev. Physiol. 57:19–42 [Google Scholar]
  104. Koštál V. 104.  2010. Cell structural modifications in insects at low temperatures. Low Temperature Biology of Insects DL Denlinger, RE Lee 116–40 Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  105. Quinn PJ. 105.  1985. A lipid-phase separation model of low-temperature damage to biological membranes. Cryobiology 22:128–46 [Google Scholar]
  106. Drobnis EZ, Crowe LM, Berger T, Anchordoguy TJ, Overstreet JW, Crowe JH. 106.  1993. Cold shock damage is due to lipid phase transitions in cell membranes: a demonstration using sperm as a model. J. Exp. Zool. 265:432–37 [Google Scholar]
  107. Edney E. 107.  1977. Water Balance in Land Arthropods Berlin: Springer-Verlag
  108. Maddrell SH, O'Donnell MJ. 108.  1992. Insect malpighian tubules: V-ATPase action in ion and fluid transport. J. Exp. Biol. 172:417–29 [Google Scholar]
  109. Ramsay JA. 109.  1954. Active transport of water by the Malpighian tubules of the stick insect, Dixippus morosus (Orthoptera, Phasmidae). J. Exp. Biol 31:104–13 [Google Scholar]
  110. Kobey RL, Montooth KL. 110.  2013. Mortality from desiccation contributes to a genotype–temperature interaction for cold survival in Drosophila melanogaster. J. Exp. Biol. 216:1174–82 [Google Scholar]
  111. Olsson T, MacMillan HA, Nyberg N, Staerk D, Malmendal A, Overgaard J. 111.  2016. Hemolymph metabolites and osmolality are tightly linked to cold tolerance of Drosophila species: a comparative study. J. Exp. Biol. 219:2504–13 [Google Scholar]
  112. MacMillan HA, Ferguson LV, Nicolai A, Donini A, Staples JF, Sinclair BJ. 112.  2015. Parallel ionoregulatory adjustments underlie phenotypic plasticity and evolution of Drosophila cold tolerance. J. Exp. Biol. 218:423–32 [Google Scholar]
  113. Terhzaz S, Teets NM, Cabrero P, Henderson L, Ritchie MG. 113.  et al. 2015. Insect capa neuropeptides impact desiccation and cold tolerance. PNAS 112:2882–87 [Google Scholar]
  114. Ruiz-Sanchez E, O'Donnell MJ. 114.  2015. The insect excretory system as a target for novel pest control strategies. Curr. Opin. Insect Sci. 11:14–20 [Google Scholar]
  115. Jonusaite S, Donini A, Kelly SP. 115.  2016. Occluding junctions of invertebrate epithelia. J. Comp. Physiol. 186B:17–43 [Google Scholar]
  116. Beyenbach KW, Piermarini PM. 116.  2011. Transcellular and paracellular pathways of transepithelial fluid secretion in Malpighian (renal) tubules of the yellow fever mosquito Aedes aegypti. Acta Physiol 202:387–407 [Google Scholar]
  117. Hoffmann AA, Sørensen JG, Loeschcke V. 117.  2003. Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J. Therm. Biol. 28:175–216 [Google Scholar]
  118. Colinet H, Hoffmann AA. 118.  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]
  119. Koštál V, Simek P. 119.  1998. Changes in fatty acid composition of phospholipids and triacylglycerols after cold-acclimation of an aestivating insect prepupa. J. Comp. Physiol. B 168:453–60 [Google Scholar]
  120. Lee RE, Damodaran K, Yi SX, Lorigan GA. 120.  2006. Rapid cold-hardening increases membrane fluidity and cold tolerance of insect cells. Cryobiology 52:459–63 [Google Scholar]
  121. Ohtsu T, Kimura MT, Katagiri C. 121.  1998. How Drosophila species acquire cold tolerance. Eur. J. Biochem. 252:608–11 [Google Scholar]
  122. Overgaard J, Sørensen JG, Petersen SO, Loeschcke V, Holmstrup M. 122.  2005. Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. J. Insect Physiol. 51:1173–82 [Google Scholar]
  123. Slotsbo S, Sørensen JG, Holmstrup M, Koštál V, Kellermann V, Overgaard J. 123.  2015. Tropical to subpolar gradient in phospholipid composition suggests adaptive tuning of biological membrane function in drosophilids. Funct. Ecol. 30:759–68 [Google Scholar]
  124. Tomčala A, Tollarová M, Overgaard J, Simek P, Koštál V. 124.  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. 209:4102–14 [Google Scholar]
  125. Cornelius F. 125.  2001. Modulation of Na,K-ATPase and Na-ATPase activity by phospholipids and cholesterol. I. Steady-state kinetics. Biochemistry 40:8842–51 [Google Scholar]
  126. Else PL, Wu BJ. 126.  1999. What role for membranes in determining the higher sodium pump molecular activity of mammals compared to ectotherms?. J. Comp. Physiol. 169B:296–302 [Google Scholar]
  127. Esmann M, Marsh D. 127.  2006. Lipid-protein interactions with the Na,K-ATPase. Chem. Phys. Lipids 141:94–104 [Google Scholar]
  128. Koštál V, Korbelová J, Rozsypal J, Zahradníčková H, Cimlová J. 128.  et al. 2011. Long-term cold acclimation extends survival time at 0°C and modifies the metabolomic profiles of the larvae of the fruit fly Drosophila melanogaster. PLOS ONE 6:e25025 [Google Scholar]
  129. Lalouette L, Koštál V, Colinet H, Gagneul D, Renault D. 129.  2007. Cold exposure and associated metabolic changes in adult tropical beetles exposed to fluctuating thermal regimes. FEBS J 274:1759–67 [Google Scholar]
  130. Michaud M, Denlinger D. 130.  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. 177B:753–63 [Google Scholar]
  131. Teets NM, Peyton JT, Ragland GJ, Colinet H, Renault D. 131.  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]
  132. Vesala L, Salminen TS, Laiho A, Hoikkala A, Kankare M. 132.  2012. Cold tolerance and cold-induced modulation of gene expression in two Drosophila virilis group species with different distributions. Insect Mol. Biol. 21:107–18 [Google Scholar]
  133. Yoder JA, Benoit JB, Denlinger DL, Rivers DB. 133.  2006. Stress-induced accumulation of glycerol in the flesh fly, Sarcophaga bullata: evidence indicating anti-desiccant and cryoprotectant functions of this polyol and a role for the brain in coordinating the response. J. Insect Physiol. 52:202–14 [Google Scholar]
  134. Koštál V, Slachta M, Simek P. 134.  2001. Cryoprotective role of polyols independent of the increase in supercooling capacity in diapausing adults of Pyrrhocoris apterus (Heteroptera: Insecta). Comp. Biochem. Physiol 130B:365–74 [Google Scholar]
  135. Arakawa T, Timasheff SN. 135.  1983. Preferential interactions of proteins with solvent components in aqueous amino acid solutions. Arch. Biochem. Biophys. 224:169–77 [Google Scholar]
  136. Benaroudj N, Lee DH, Goldberg AL. 136.  2001. Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J. Biol. Chem. 276:24261–67 [Google Scholar]
  137. Viner RI, Clegg JS. 137.  2001. Influence of trehalose on the molecular chaperone activity of p26, a small heat shock/α-crystallin protein. Cell Stress Chaperones 6:126–35 [Google Scholar]
  138. Misener SR, Chen C-P, Walker VK. 138.  2001. Cold tolerance and proline metabolic gene expression in Drosophila melanogaster. J. Insect Physiol. 47:393–400 [Google Scholar]
  139. Colinet H, Lee SF, Hoffmann A. 139.  2010. Temporal expression of heat shock genes during cold stress and recovery from chill coma in adult Drosophila melanogaster. FEBS J 277:174–85 [Google Scholar]
  140. Koštál V, Tollarová-Borovanská M. 140.  2009. The 70 kDa heat shock protein assists during the repair of chilling injury in the insect, Pyrrhocoris apterus. PLOS ONE 4:e4546 [Google Scholar]
  141. Rinehart JP, Hayward SAL, Elnitsky MA, Sandro LH, Lee RE, Denlinger DL. 141.  2006. Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect. PNAS 103:14223–27 [Google Scholar]
  142. Sinclair BJ, Gibbs AG, Roberts SP. 142.  2007. Gene transcription during exposure to, and recovery from, cold and desiccation stress in Drosophila melanogaster. Insect Mol. Biol. 16:435–43 [Google Scholar]
  143. Štětina T, Koštál V, Korbelová J. 143.  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]
  144. Colinet H, Lee SF, Hoffmann A. 144.  2010. Functional characterization of the frost gene in Drosophila melanogaster: importance for recovery from chill coma. PLOS ONE 5:e10925 [Google Scholar]
  145. Udaka H, Percival-Smith A, Sinclair BJ. 145.  2013. Increased abundance of frost mRNA during recovery from cold stress is not essential for cold tolerance in adult Drosophila melanogaster. Insect Mol. Biol. 22:541–50 [Google Scholar]
  146. Clowers KJ, Lyman RF, Mackay TFC, Morgan TJ. 146.  2010. Genetic variation in senescence marker protein-30 is associated with natural variation in cold tolerance in Drosophila. Genet. Res. 92:103–13 [Google Scholar]
  147. Goto SG. 147.  2000. Expression of Drosophila homologue of senescence marker protein-30 during cold acclimation. J. Insect Physiol. 46:1111–20 [Google Scholar]
  148. Lalouette L, Williams CM, Hervant F, Sinclair BJ, Renault D. 148.  2011. Metabolic rate and oxidative stress in insects exposed to low temperature thermal fluctuations. Comp. Biochem. Physiol. 158A:229–34 [Google Scholar]
  149. Rojas RR, Leopold RA. 149.  1996. Chilling injury in the housefly: evidence for the role of oxidative stress between pupariation and emergence. Cryobiology 33:447–58 [Google Scholar]
  150. Parker DJ, Vesala L, Ritchie MG, Laiho A, Hoikkala A, Kankare M. 150.  2015. How consistent are the transcriptome changes associated with cold acclimation in two species of the Drosophila virilis group?. Heredity 115:13–21 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
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