Journal of Biosciences

, Volume 32, Issue 3, pp 477–488 | Cite as

The role of stress proteins in responses of a montane willow leaf beetle to environmental temperature variation



The heat shock response is a critical mechanism by which organisms buffer effects of variable and unpredictable environmental temperatures. Upregulation of heat shock proteins (Hsps) increases survival after exposure to stressful conditions in nature, although benefits of Hsp expression are often balanced by costs to growth and reproductive success. Hsp-assisted folding of variant polypeptides may prevent development of unfit phenotypes; thus, some differences in Hsp expression among natural populations of ectotherms may be due to interactions between enzyme variants (allozymes) and Hsps. In the Sierra willow leaf beetle Chrysomela aeneicollis, which lives in highly variable thermal habitats at the southern edge of their range in the Eastern Sierra Nevada, California, allele frequencies at the enzyme locus phosphoglucose isomerase (PGI) vary across a climatic latitudinal gradient. PGI allozymes differ in kinetic properties, and expression of a 70 kDa Hsp differs between populations, along elevation gradients, and among PGI genotypes. Differences in Hsp 70 expression among PGI genotypes correspond to differences in thermal tolerance and traits important for reproductive success, such as running speed, survival and fecundity. Thus, differential Hsp expression among genotypes may allow functionally important genetic variation to persist, allowing populations to respond effectively to environmental change.


Adaptation Chrysomelidae Hsp 70 insect PGI 


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  1. Angilletta M J, Niewiarowski P H and Navas C A 2002 The evolution of thermal physiology in ectotherms; Thermal Biol. 27 249–268Google Scholar
  2. Asea A 2005 Stress proteins and initiation of immune response: Chaperokine activity of Hsp72; Exercise Immunol. Rev. 11 34–45Google Scholar
  3. Balanya J, Oller J M, Huey R B, Gilchrist G W and Serra L 2006 Global genetic change tracks global climate warming in Drosophila subobscura; Science 313 1773–1775PubMedGoogle Scholar
  4. Barnosky A D, Hadly E A and Bell C J 2003 Mammalian response to global warming on varied temporal scales; J. Mammal. 84 354–368Google Scholar
  5. Bettencourt B R, Kim I, Hoffmann A A and Feder M E 2002 Response to natural and laboratory selection at the Drosophila hsp70 genes; Evolution 56 1796–1801PubMedGoogle Scholar
  6. Bradshaw W E, Zani P A and Holzapfel C M 2004 Adaptation to temperate climates; Evolution 58 1748–1762PubMedGoogle Scholar
  7. Brown W J 1956 The New World species of Chrysomela L. (Coleoptera: Chrysomelidae); Can. Entomol. 88 1–54Google Scholar
  8. Bruce D A 2005 Effects of PGI genotype and temperature on fecundity, mating success and running speed of a Sierra willow leaf beetle; Masters Thesis, Department of Biology, Sonoma State University, Rohnert Park. C A, USAGoogle Scholar
  9. Cavicchi S, Guerra D, Latorre V and Huey R B 1995 Chromosomal Analysis of Heat-Shock Tolerance in Drosophila melanogaster Evolving at Different Temperatures in the Laboratory; Evolution 49 676–684Google Scholar
  10. Chown S L 2001 Physiological variation in insects: hierarchical levels and implications; J. Insect Physiol. 47 649–660PubMedGoogle Scholar
  11. Clarke A 2003 Costs and consequences of evolutionary temperature adaptation; Trends in Ecol. and Evol. 18 573–581Google Scholar
  12. Dahlhoff E P 2004 Biochemical indicators of stress and metabolism: Applications for marine ecological studies; Annu. Rev. Physiol. 66 183–207PubMedGoogle Scholar
  13. Dahlhoff E P, Buckley B A and Menge B A 2001 Physiology of the rocky intertidal predator Nucella ostrina along an environmental stress gradient; Ecology 82 2816–2829Google Scholar
  14. Dahlhoff E P and Rank N E 2000 Functional and physiological consequences of genetic variation at phosphoglucose isomerase: heat shock protein expression is related to enzyme genotype in a montane beetle; Proc. Natl. Acad. Sci. USA 97 10056–10061PubMedGoogle Scholar
  15. de Jong P W, Gussekloo S W S and Brakefield P M 1996 Differences in thermal balance, body temperature and activity between non-melanic and melanic two-spot ladybird beetles (Adalia bipunctata) under controlled conditions; J. Exp. Biol. 199 2655–2666PubMedGoogle Scholar
  16. Denny M W, Miller L P and Harley C D G 2006 Thermal stress on intertidal limpets: long-term hindcasts and lethal limits; J. Exp. Biol. 209 2420–2431PubMedGoogle Scholar
  17. Duffy J E and Stachowicz J J 2006 Why biodiversity is important to oceanography: potential roles of genetic, species, and trophic diversity in pelagic ecosystem processes; Mar. Ecol. Prog. Series 311 179–189Google Scholar
  18. Easterling D R, Meehl G A, Parmesan C, Changnon S A, Karl T R and Mearns L O 2000 Climate extremes: observations, modeling, and impacts; Science 289 2068–2074PubMedGoogle Scholar
  19. Ellers J and Boggs C L 2004 Functional ecological implications of intraspecific differences in wing melanization in Colias butterflies; Biol. J. Linn. Soc. 82 79–87Google Scholar
  20. Fearnley S L 2003 Adaptation at an enzyme locus in Chrysomela aeneicollis: situating the PGI polymorphism in a functional and historical context; Masters Thesis, Department of Biology, Sonoma State University, Rohnert Park, C A, USAGoogle Scholar
  21. Feder M, Bedford T, Albright D and Michalak P 2002 Evolvability of Hsp70 expression under artificial selection for inducible thermotolerance in independent populations of Drosophila melanogaster; Physiol. Biochem. Zool. 75 325–334PubMedGoogle Scholar
  22. Feder M E, Cartano N V, Milos L, Krebs R A and Lindquist S L 1996 Effect of engineering Hsp70 copy number on Hsp70 expression and tolerance of ecologically relevant heat shock in larvae and pupae of Drosophila melanogaster; J. Exp. Biol. 199 1837–1844PubMedGoogle Scholar
  23. Feder M E and Hofmann G E 1999 Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology; Annu. Rev. Physiol. 61 243–282PubMedGoogle Scholar
  24. Feder M E and Watt W B 1993 Functional biology of adaptation; in Genes in ecology (eds) R J Berry, T J Crawford and G M Hewitt (Oxford: Blackwell) pp 365–392Google Scholar
  25. Fitzhenry T, Halpin P M and Helmuth B 2004 Testing the effects of wave exposure, site, and behavior on intertidal mussel body temperatures: applications and limits of temperature logger design; Mar. Biol. 145 339–349Google Scholar
  26. Folk D G and Gilchrist G W 2005 Heat-shock response and locomotory performance in Drosophila populations selected for divergent knockdown temperatures; Integr. Comp. Biol. 45 955–1103 doi: 10.1093/icb/45.6.955Google Scholar
  27. Forsman A, Ringblom K, Civantos E and Ahnesjo J 2002 Coevolution of color pattern and thermoregulatory behavior in polymorphic pygmy grasshoppers Tetrix undulata; Evolution 56 349–360PubMedGoogle Scholar
  28. Funasaka T, Yanagawa T, Hogan V and Raz A 2005 Regulation of phosphoglucose isomerase/autocrine motility factor expression by hypoxia; FASEB J. 19 1422–1430PubMedGoogle Scholar
  29. Garbuz D, Evgenev M, Feder M E and Zatsepina O 2003 Evolution of thermotolerance and the heat-shock response: evidence from inter/intraspecific comparison and interspecific hybridization in the virilis species group of Drosophila. I. Thermal phenotype; J. Exp. Biol. 206 2399–2408PubMedGoogle Scholar
  30. Gilchrist G W and Huey R B 2003 Is plasticity an adaptation? Body size as a function of temperature within and among parallel clines in Drosophila subobscura; Integr. Comp. Biol. 43 841Google Scholar
  31. Gilman S E, Wethey D S and Helmuth B 2006 Variation in the sensitivity of organismal body temperature to climate change over local and geographic scales; Proc. Natl. Acad. Sci. USA 103 9560–9565PubMedGoogle Scholar
  32. Harley C D G, Hughes A R, Hultgren K M, Miner B G, Sorte C J B, Thornber C S, Rodriguez L F, Tomanek L and Williams S L 2006 The impacts of climate change in coastal marine systems; Ecol. Lett. 9 228–241PubMedGoogle Scholar
  33. Hazel J R 1995 Thermal adaptation in biological membranes: Is homeoviscous adaptation the explanation?; Annu. Rev. Physiol. 57 19–42PubMedGoogle Scholar
  34. Hazel W N 2002 The environmental and genetic control of seasonal polyphenism in larval color and its adaptive significance in a swallowtail butterfly; Evolution 56 342–348PubMedGoogle Scholar
  35. Helmuth B 1999 Thermal biology of rocky intertidal mussels: Quantifying body temperatures using climatological data; Ecology 80 15–34Google Scholar
  36. Helmuth B 2002 How do we measure the environment? Linking intertidal thermal physiology and ecology through biophysics; Integr. Comp. Biol. 42 837–845Google Scholar
  37. Helmuth B, Broitman B R, Blanchette C A, Gilman S, Halpin P, Harley C D G, O’Donnell M J, Hofmann G E, Menge B A and Strickland D 2006 Mosaic patterns of thermal stress in the rocky intertidal zone: Implications for climate change; Ecol. Monogr. 76 461–479Google Scholar
  38. Helmuth B, Harley C D G, Halpin P M, O’Donnell M, Hofmann G E and Blanchette C A 2002 Climate change and latitudinal patterns of intertidal thermal stress; Science 298 1015–1017PubMedGoogle Scholar
  39. Helmuth B, Kingsolver J G and Carrington E 2005 Biophysics, physiological ecology, and climate change: Does mechanism matter?; Annu. Rev. Physiol. 67 177–201PubMedGoogle Scholar
  40. Helmuth B S T and Hofmann G E 2001 Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone; Biol. Bull 201 374–384PubMedGoogle Scholar
  41. Hill J K, Hughes C L, Dytham C and Searle J B 2006 Genetic diversity in butterflies: interactive effects of habitat fragmentation and climate-driven range expansion; Biol. Lett. 2 152–154PubMedGoogle Scholar
  42. Hill J K, Thomas C D, Fox R, Telfer M G, Willis S G, Asher J and Huntley B 2002 Responses of butterflies to twentieth century climate warming: implications for future ranges; Proc. R. Soc. London Series B Biol. Sci. 269 2163–2171Google Scholar
  43. Hoffmann A A, Hallas R J, Dean J A and Schiffer M 2003 Low potential for climatic stress adaptation in a rainforest Drosophila species; Science 301 100–102PubMedGoogle Scholar
  44. Hoffmann R J 1981a Evolutionary genetics of Metridium senile. I. Kinetic differences in phosphoglucose isomerase E.C. allozymes; Biochem. Genet. 19 129–144PubMedGoogle Scholar
  45. Hoffmann R J 1981b. Evolutionary genetics of Metridium senile. II. Geographic patterns of allozyme variation; Biochem. Genet. 19 145–154PubMedGoogle Scholar
  46. Hofmann G E 2005 Patterns of Hsp gene expression in ectothermic marine organisms on small to large biogeographic scales; Integr. Comp. Biol. 45 247–255Google Scholar
  47. Huey R B 1991 Physiological Consequences of Habitat Selection; Am. Nat. 137 S91–S115Google Scholar
  48. Inouye D W, Barr B, Armitage K B and Inouye B D 2000 Climate change is affecting altitudinal migrants and hibernating species; Proc. Nat. Acad. Sci. USA 97 1630–1633PubMedGoogle Scholar
  49. Jump A S, Hunt J M, Martinez-Izquierdo J A and Penuelas J 2006 Natural selection and climate change: temperature-linked spatial and temporal trends in gene frequency in Fagus sylvatica; Mol. Ecol. 15 3469–3480PubMedGoogle Scholar
  50. Kelty J D and Lee R E 1999 Induction of rapid cold hardening by cooling at ecologically relevant rates in Drosophila melanogaster; J. Insect Physiol. 45 719–726PubMedGoogle Scholar
  51. Kingsolver J G 1979 Thermal and Hydric Aspects of Environmental Heterogeneity in the Pitcher Plant Mosquito; Ecol. Monogr. 49 357–376Google Scholar
  52. Kingsolver J G and Huey R B 1998 Evolutionary analyses of morphological and physiological plasticity in thermally variable environments; Am. Zool. 38 545–560Google Scholar
  53. Kingsolver J G, Izem R and Ragland G J 2004 Plasticity of size and growth in fluctuating thermal environments: Comparing reaction norms and performance curves; Integr. Comp. Biol. 44 450–460Google Scholar
  54. Kingsolver J G and Wiernasz D C 1991 Seasonal Polyphenism in Wing-Melanin Pattern and Thermoregulatory Adaptation in Pieris Butterflies; Am. Nat. 137 816–830Google Scholar
  55. Krebs R A 1999 A comparison of Hsp70 expression and thermotolerance in adults and larvae of three Drosophila species; Cell Stress Chaperones 4 243–249PubMedGoogle Scholar
  56. Krebs R A and Bettencourt B R 1999 Evolution of thermotolerance and variation in the heat shock protein, Hsp70; Am. Zool. 39 910–919Google Scholar
  57. Krebs R A and Feder M E 1997 Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae; Cell Stress Chaperones 2 60–71PubMedGoogle Scholar
  58. Krebs R A and Feder M E 1998 Hsp70 and larval thermotolerance in Drosophila melanogaster: how much is enough and when is more too much?; J. Insect Physiol. 44 1091–1101PubMedGoogle Scholar
  59. Krebs R A and Holbrook S H 2001 Reduced enzyme activity following Hsp70 overexpression in Drosophila melanogaster; Biochem. Genet. 39 73–82PubMedGoogle Scholar
  60. Lindquist S 1986 The heat-shock response; Annu. Rev. Biochem. 55 1151–1191PubMedGoogle Scholar
  61. Loeschcke V, Krebs R A, Dahlgaard J and Michalak P 1997 High-temperature stress and the evolution of thermal resistance in Drosophila; (ed.) Bijlsma R L, in Experientia Supplementum (Basel); Environmental stress, adaptation and evolution, (Basel) pp 175–190Google Scholar
  62. Maughan D W, Henkin J A and Vigoreaux J O 2005 Concentrations of glycolytic enzymes and other cytosolic proteins in the diffusible fraction of a vertebrate muscle proteome; Mol. Cell. Proteomics 4 1541–1549PubMedGoogle Scholar
  63. McMillan D M, Fearnley S L, Rank N E and Dahlhoff E P 2005 Natural temperature variation affects larval survival, development and Hsp70 expression in a leaf beetle; Funct. Ecol. 19 844–852Google Scholar
  64. Mitton J B 1997 Selection in natural populations (New York: Oxford University Press)Google Scholar
  65. Neargarder G, Dahlhoff E P and Rank N E 2003 Variation in thermal tolerance is linked to phosphoglucose isomerase genotype in a montane leaf beetle; Funct. Ecol. 17 213–221Google Scholar
  66. Nielsen M G and Watt W B 1998 Behavioural fitness component effects of the alba polymorphism of Colias (Lepidoptera, Pieridae): resource and time budget analysis; Funct. Ecol. 12 149–158Google Scholar
  67. Parmesan C and Yohe G 2003 A globally coherent fingerprint of climate change impacts across natural systems; Nature (London) 421 37–42Google Scholar
  68. Parsell D A and Lindquist S 1993 The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins; Annu. Rev. Genet. 27 437–496PubMedGoogle Scholar
  69. Patton Z J and Krebs R A 2001 The effect of thermal stress on the mating behavior of three Drosophila species; Physiol. Biochem. Zool. 74 783–788PubMedGoogle Scholar
  70. Price T D 2006 Phenotypic plasticity, sexual selection and the evolution of colour patterns; J. Exp. Biol. 209 2368–2376PubMedGoogle Scholar
  71. Rank N E, Bruce D A, McMillan D M, Barclay C and Dahlhoff E P 2007 Phosphoglucose isomerase genotype affects running speed and heat shock protein expression after exposure to extreme temperatures in a montane willow beetle; J. Exp. Biol. 210 750–764PubMedGoogle Scholar
  72. Rank N E 1992a A hierarchical analysis of genetic differentiation in a montane leaf beetle (Chrysomela aeneicollis); Evolution 46 1097–1111Google Scholar
  73. Rank N E 1992b Host plant preference based on salicylate chemistry in a willow leaf beetle (Chrysomela aeneicollis); Oecologia (Berlin) 90 95–101Google Scholar
  74. Rank N E 1994 Host plant effects on larval survival in a salicin-using leaf beetle Chrysomela aeneicollis (Coleoptera: Chrysomelidae); Oecologia (Berlin) 97 342–353Google Scholar
  75. Rank N E and Dahlhoff E P 2002 Allele frequency shifts in response to climate change and physiological consequences of allozyme variation in a montane insect; Evolution 56 2278–2289PubMedGoogle Scholar
  76. Riddoch B J 1993 The adaptive significance of electrophoretic mobility in phosphoglucose isomerase (PGI); Biol. J. Linn. Soc. 50 1–17Google Scholar
  77. Roberts D A, Hofmann G E and Somero G N 1997 Heat-shock protein expression in Mytilus californianus: Acclimatization (seasonal and tidal-height comparisons) and acclimation effects; Biol. Bull. 192 309–320Google Scholar
  78. Roberts S P and Feder M E 1999 Natural hyperthermia and expression of the heat shock protein Hsp70 affect developmental abnormalities in Drosophila melanogaster, Oecologia 121 323–329Google Scholar
  79. Roberts S P, Marden J H and Feder M E 2003 Dropping like flies: Environmentally induced impairment and protection of locomotor performance in adult Drosophila melanogaster; Physiol. Biochem. Zool. 76 615–621PubMedGoogle Scholar
  80. Robertson R M 2004 Thermal stress and neural function: adaptive mechanisms in insect model systems; J. Thermal Biol. 29 351–358Google Scholar
  81. Rutherford S L 2003 Between genotype and phenotype: Protein chaperones and evolvability; Nat. Rev. Genet. 4 263–274PubMedGoogle Scholar
  82. Rutherford S L and Lindquist S 1998 Hsp90 as a capacitor for morphological evolution; Nature (London) 396 336–342Google Scholar
  83. Sagarin R D, Barry J P, Gilman S E and Baxter C H 1999 Climate-related change in an intertidal community over short and long time scales; Ecol. Monogr. 69 465–490CrossRefGoogle Scholar
  84. Sagarin R D and Somero G N 2006 Complex patterns of expression of heat-shock protein 70 across the southern biogeographical ranges of the intertidal mussel Mytilus californianus and snail Nucella ostrina; J. Biogeogr. 33 622–630Google Scholar
  85. Smiley J T and Rank N E 1986 Predator protection versus rapid growth in a montane leaf beetle; Oecologia 70 106–112Google Scholar
  86. Somero G N 1995 Proteins and temperature; Annu. Rev. Physiol. 57 43–68PubMedGoogle Scholar
  87. Sorensen J G, Kristensen T N and Loeschcke V 2003 The evolutionary and ecological role of heat shock proteins; Ecol. Lett. 6 1025–1037Google Scholar
  88. Sorensen J G and Loeschcke V 2004 Effects of relative emergence time on heat stress resistance traits, longevity and hsp70 expression level in Drosophila melanogaster; J. Thermal Biol. 29 195–203Google Scholar
  89. Sorte C J B and Hofmann G E 2004 Changes in latitudes, changes in aptitudes: Nucella canaliculata (Mollusca: Gastropoda) is more stressed at its range edge; Mar. Ecol. Prog. Series 274 263–268Google Scholar
  90. Sorte C J B and Hofmann G E 2005 Thermotolerance and heatshock protein expression in Northeastern Pacific Nucella species with different biogeographical ranges; Mar. Biol. 146 985–993Google Scholar
  91. Tomanek L 2002 The heat-shock response: Its variation, regulation and ecological importance in intertidal gastropods (genus Tegula); Integr. Comp. Biol. 42 797–807Google Scholar
  92. Tomanek L 2005 Two-dimensional gel analysis of the heat-shock response in marine snails (genus Tegula): interspecific variation in protein expression and acclimation ability; J. Exp. Biol. 208 3133–3143PubMedGoogle Scholar
  93. Tomanek L and Somero G N 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
  94. Tomanek L and Somero G N 2002 Interspecific-and acclimation-induced variation in levels of heat-shock proteins 70 (hsp70) and 90 (hsp90) and heat-shock transcription factor-1 (HSF1) in congeneric marine snails (genus Tegula): implications for regulation of hsp gene expression; J. Exp. Biol. 205 677–685PubMedGoogle Scholar
  95. Walther G R, Post E, Convey P, Menzel A, Parmesan C, Beebee T J C, Fromentin J M, Hoegh-Guldberg O and Bairlein F 2002 Ecological responses to recent climate change; Nature (London) 416 389–395Google Scholar
  96. Watanabe J M 1984 The Influence of Recruitment, Competition, and Benthic Predation on Spatial Distributions of 3 Species of Kelp Forest Gastropods (Trochidae, Tegula); Ecology 65 920–936Google Scholar
  97. Watt W B 1977 Adaptation at specific loci. I. Natural selection on phosphoglucose isomerase of Colias butterflies: biochemical and population aspects; Genetics 87 177–194PubMedGoogle Scholar
  98. Watt W B 1983 Adaptation at specific loci. II. Demographic and biochemical elements in the maintenance of the Colias pgi polymorphism; Genetics 103 691–724PubMedGoogle Scholar
  99. Wheat C W, Watt W B, Pollock D D and Schulte P M 2006 From DNA to fitness differences: Sequences and structures of adaptive variants of Colias phosphoglucose isomerase (PGI); Mol. Biol. Evol. 23 499–512PubMedGoogle Scholar
  100. Willmer P, Stone G and Johnston I 2004 Environmental physiology of animals (Oxford: Blackwell Science)Google Scholar
  101. Yanagawa T, Funasaka T, Tsutsumi S, Watanabe H and Raz A 2004 Novel roles of the autocrine motility factor/phosphoglucose isomerase in tumor malignancy; Endocrine-Related Cancer 11 749–759PubMedGoogle Scholar
  102. Yiangou M, Tsapogas P, Nikolaidis N and Scouras Z G 1997 Heat shock gene expression during recovery after transient cold shock in Drosophila auraria (Diptera: Drosophilidae); Cytobios 92 91–98PubMedGoogle Scholar
  103. Yocum G D 2001 Differential expression of two HSP70 transcripts in response to cold shock, thermoperiod, and adult diapause in the Colorado potato beetle; J. Insect Physiol. 47 1139–1145PubMedGoogle Scholar

Copyright information

© Indian Academy of Sciences 2007

Authors and Affiliations

  1. 1.Department of BiologySanta Clara UniversitySanta ClaraUSA
  2. 2.Department of BiologySonoma State UniversityRohnert ParkUSA
  3. 3.White Mountain Research StationUniversity of CaliforniaBishopUSA

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