Marine Biology

, Volume 146, Issue 5, pp 985–993 | Cite as

Thermotolerance and heat-shock protein expression in Northeastern Pacific Nucella species with different biogeographical ranges

Research Article

Abstract

We investigated physiological traits responsible for determining the tide-height and latitudinal distributions of Northeastern Pacific Nucella congeners. First, we determined the thermotolerances of two species of intertidal dogwhelks, N. ostrina and N. canaliculata, which co-occur on the Oregon coast. We found that N. ostrina, which are distributed higher on the shore, and thus experience higher habitat temperatures, than N. canaliculata, had correspondingly higher heat-coma temperatures. Second, we acclimated individuals of all five Northeastern Pacific Nucella congeners to a common temperature and determined their thermotolerances, measured as recovery from thermal exposure, after a 5-day, 3-week, and 7-week acclimation period. The south-latitude (N. emarginata) and mid-latitude (N. ostrina) high-intertidal species were more thermotolerant than the mid-latitude low-intertidal (N. canaliculata and N. lamellosa) and north-latitude high-intertidal (N. lima) species. The results of these two experiments suggest that temperature plays a role in determining the tide-height and latitudinal distributions of these Nucella species. Finally, we measured total and inducible levels of an evolutionarily conserved and ecologically relevant protein, the 70-kDa heat-shock protein (Hsp70), which has been found to confer thermotolerance in model laboratory organisms. The results showed that the level of total, not stress inducible, Hsp70 was a better predictor of thermotolerance and that there were species-specific differences in the relationship between Hsp70 expression and thermotolerance. We suggest that Hsp70 expression may be important in conferring thermotolerance in Nucella species in nature and that higher levels of molecular chaperones may underlie increased thermotolerance between conspecifics.

References

  1. Bertness MD, Schneider DE (1976) Temperature relations of Puget Sound Thaids in reference to their intertidal distribution. Veliger 19:47–58Google Scholar
  2. Bertness MD, Leonard GH, Levine JM, Bruno JF (1999) Climate-driven interactions among rocky intertidal organisms caught between a rock and a hot place. Oecologia 120:446–450CrossRefGoogle Scholar
  3. Brown JH (1984) On the relationship between abundance and distribution of species. Am Nat 124:255–279CrossRefGoogle Scholar
  4. Buckley BA, Owen M-E, Hofmann GE (2001) Adjusting the thermostat: the threshold induction temperature for the heat-shock response in intertidal mussels (genus Mytilus) changes as a function of thermal history. J Exp Biol 204:3571–3579Google Scholar
  5. Collins TM, Frazer K, Palmer AR, Vermeij GJ, Brown WM (1996) Evolutionary history of northern hemisphere Nucella (Gastropoda, Muricidae): molecular, morphological, ecological, and paleontological evidence. Evolution 50:2287–2304Google Scholar
  6. Dahlhoff EP, Buckley BA, Menge BA (2001) Physiology of the rocky intertidal predator Nucella ostrina along an environmental stress gradient. Ecology 82:2816–2829Google Scholar
  7. Dietz TJ, Somero GN (1992) The threshold induction temperature of the 90-kDa heat shock protein is subject to acclimatization in eurythermal goby fishes (genus Gillichthys). Proc Natl Acad Sci USA 89:3389–3393Google Scholar
  8. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282CrossRefPubMedGoogle Scholar
  9. Feder ME, Cartaño NV, Milos L, Krebs RA, Lindquist SL (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 199:1837–1844Google Scholar
  10. Fink AL (1999) Chaperone-mediated protein folding. Physiol Rev 79:425–449PubMedGoogle Scholar
  11. Halpin PM, Sorte CJ, Hofmann GE, Menge BA (2002) Patterns of variation in levels of Hsp70 in natural rocky shore populations from microscales to mesoscales. Integr Comp Biol 42:815–824Google Scholar
  12. Hartl FU, Hayer-Hartl, M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858CrossRefPubMedGoogle Scholar
  13. Helmuth BST, Hofmann GE (2001) Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol Bull 201:374–384Google Scholar
  14. Helmuth B, Harley CDG, Halpin PM, O’Donnell M, Hofmann GE, Blanchette CA (2002) Climate change and latitudinal patterns of intertidal thermal stress. Science 298:1015–1017CrossRefPubMedGoogle Scholar
  15. Hoffmann AA, Blows MW (1994) Species borders: ecological and evolutionary perspectives. Trends Ecol Evol 9:223–227CrossRefGoogle Scholar
  16. Hofmann GE (1999) Ecologically relevant variation in induction and function of heat shock proteins in marine organisms. Am Zool 39:889–900Google Scholar
  17. Hofmann GE, Somero GN (1995) Evidence for protein damage at environmental temperatures: seasonal changes in levels of ubiquitin conjugates and HSP70 in the intertidal mussel Mytilus trossulus. J Exp Biol 198:1509–1518Google Scholar
  18. Hofmann GE, Somero GN (1996a) Protein ubiquitination and stress protein synthesis in Mytilus trossulus occurs during recovery from tidal emersion. Mol Mar Biol Biotech 5:175–184Google Scholar
  19. Hofmann GE, Somero GN (1996b) Interspecific variation in thermal denaturation of proteins in the congeneric mussels Mytilus trossulus and M. galloprovincialis: evidence from the heat-shock response and protein ubiquitination. Mar Biol 126:65–75CrossRefGoogle Scholar
  20. Huey RB (1991) Physiological consequences of habitat selection. Am Nat 137:S91-S115CrossRefGoogle Scholar
  21. Landry J, Bernier D, Chretien P, Nicole LM, Tanguay RM, Marceau N (1982) Synthesis and degradation of heat shock proteins during development and decay of thermotolerance. Cancer Res 42:2457–2461Google Scholar
  22. Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151–1191CrossRefPubMedGoogle Scholar
  23. Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757CrossRefGoogle Scholar
  24. Newell RC (1979) Biology of intertidal animals. Marine Ecological Surveys, Faversham, UKGoogle Scholar
  25. Palmer AR (1980) A comparative and experimental study of feeding and growth in thaidid gastropods. PhD dissertation, University of Washington, Seattle, Wash.Google Scholar
  26. Palmer AR, Gayron SD, Woodruff DS (1990) Reproductive, morphological, and genetic evidence for two cryptic species of Northeastern Pacific Nucella. Veliger 33:325–338Google Scholar
  27. Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–439CrossRefGoogle Scholar
  28. Roberts DA, Hofmann GE, Somero GN (1997) Heat-shock protein expression in Mytilus californianus: acclimatization (seasonal and tidal-height comparisons) and acclimation effects. Biol Bull 192:309–320Google Scholar
  29. Sagarin RD, Gaines SD (2002) The ‘abundant centre’ distribution: to what extent is it a biogeographical rule? Ecol Lett 5:137–147CrossRefGoogle Scholar
  30. Sanders BM (1993) Stress proteins in aquatic organisms: an environmental perspective. Crit Rev Toxicol 23:49–75PubMedGoogle Scholar
  31. Sanford E (1999) Regulation of keystone predation by small changes in ocean temperature. Science 283:2095–2097CrossRefPubMedGoogle Scholar
  32. Sanford E (2002) The feeding, growth, and energetics of two rocky intertidal predators (Pisaster ochraceus and Nucella canaliculata) under water temperatures simulating episodic upwelling. J Exp Mar Biol Ecol 273:199–218CrossRefGoogle Scholar
  33. Sokolova IM, Pörtner H-O (2003) Metabolic plasticity and critical temperatures for aerobic scope in a eurythermal marine invertebrate (Littorina saxatilis, Gastropoda: Littorinidae) from different latitudes. J Exp Biol 206:195–207CrossRefPubMedGoogle Scholar
  34. Somero GN (1995) Proteins and temperature. Annu Rev Physiol 57:43–68CrossRefGoogle Scholar
  35. Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integr Comp Biol 42:780–789Google Scholar
  36. Sorte CJB (2003) The ecophysiological underpinnings of biogeographic patterns: temperature effects on the distributions of Nucella congeners. MA thesis, University of California, Santa Barbara, Calif.Google Scholar
  37. Sorte CJB, Hofmann GE (2004) Changes in latitudes, changes in aptitudes: Nucella canaliculata (Mollusca: Gastropoda) is more stressed at its range edge. Mar Ecol Progr Ser 274:263–268Google Scholar
  38. Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301:65CrossRefGoogle Scholar
  39. 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 202:2925–2936Google Scholar
  40. Tomanek L, Somero GN (2000) Time course and magnitude of synthesis of heat-shock proteins in congeneric marine snails (genus Tegula) from different tidal heights. Physiol Biochem Zool 73:249–256CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of Ecology, Evolution and Marine Biology and the Marine Science InstituteUniversity of CaliforniaSanta BarbaraUSA

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