The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’

Journal of Experimental Biology - Tập 213 Số 6 - Trang 912-920 - 2010
George N. Somero1
1Hopkins Marine Station, Department of Biology, Stanford University, Pacific Grove, CA 93950, USA

Tóm tắt

SUMMARY

Physiological studies can help predict effects of climate change through determining which species currently live closest to their upper thermal tolerance limits, which physiological systems set these limits, and how species differ in acclimatization capacities for modifying their thermal tolerances. Reductionist studies at the molecular level can contribute to this analysis by revealing how much change in sequence is needed to adapt proteins to warmer temperatures — thus providing insights into potential rates of adaptive evolution — and determining how the contents of genomes — protein-coding genes and gene regulatory mechanisms — influence capacities for adapting to acute and long-term increases in temperature. Studies of congeneric invertebrates from thermally stressful rocky intertidal habitats have shown that warm-adapted congeners are most susceptible to local extinctions because their acute upper thermal limits (LT50 values) lie near current thermal maxima and their abilities to increase thermal tolerance through acclimation are limited. Collapse of cardiac function may underlie acute and longer-term thermal limits. Local extinctions from heat death may be offset by in-migration of genetically warm-adapted conspecifics from mid-latitude ‘hot spots’, where midday low tides in summer select for heat tolerance. A single amino acid replacement is sufficient to adapt a protein to a new thermal range. More challenging to adaptive evolution are lesions in genomes of stenotherms like Antarctic marine ectotherms, which have lost protein-coding genes and gene regulatory mechanisms needed for coping with rising temperature. These extreme stenotherms, along with warm-adapted eurytherms living near their thermal limits, may be the major ‘losers’ from climate change.

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Tài liệu tham khảo

Barry, 1995, Climate-related, long-term faunal changes in a California rocky intertidal community, Science, 267, 672, 10.1126/science.267.5198.672

Beere, 2004, ‘The stress of dying’: the role of heat shock proteins in the regulation of apoptosis, J. Cell Sci., 117, 2641, 10.1242/jcs.01284

Braby, 2006, Following the heart: temperature and salinity effects on heart rate in native and invasive species of blue mussels (genus Mytilus), J. Exp. Biol., 209, 2554, 10.1242/jeb.02259

Buckley, 2009, cDNA microarray analysis reveals the capacity of the cold-adapted Antarctic fish Trematomus bernacchii to alter gene expression in response to heat stress, Polar Biol., 32, 403, 10.1007/s00300-008-0533-x

Buckley, 2006, The cellular response to heat stress in the goby Gillichthys mirabilis: a cDNA microarray and protein-level analysis, J. Exp. Biol., 209, 2660, 10.1242/jeb.02292

Clark, 2009, HSP70 heat shock proteins and environmental stress in Antarctic marine organisms: a mini-review, Mar. Genom., 2, 11, 10.1016/j.margen.2009.03.003

Clark, 2009, Lack of an HSP70 heat shock response in two Antarctic marine invertebrates, Polar Biol., 31, 1059, 10.1007/s00300-008-0447-7

Cocca, 1997, Do the hemoglobinless icefishes have globin genes?, Comp. Biochem. Physiol. A, 118, 1027, 10.1016/S0300-9629(97)00010-8

Creagh, 2000, Heat shock proteins — modulators of apoptosis in tumour cells, Leukemia, 14, 1161, 10.1038/sj.leu.2401841

Crummett, 2007, Genetic evidence for the cryptic species pair Lottia digitalis and Lottia austrodigitalis and microhabitat partitioning in sympatry, Mar. Biol., 152, 1, 10.1007/s00227-007-0621-4

Deutsch, 2008, Impacts of climate warming on terrestrial ectotherms across latitude, Proc. Natl. Acad. Sci. USA, 105, 6668, 10.1073/pnas.0709472105

Dong, 2009, Temperature adaptation of cytosolic malate dehydrogenases of limpets (genus Lottia): differences in stability and function due to minor changes in sequence correlate with biogeographic and vertical distributions, J. Exp. Biol., 212, 169, 10.1242/jeb.024505

Eastman, 1993, Antarctic Fish Biology: Evolution in a Unique Environment

Fangue, 2006, Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus, J. Exp. Biol., 209, 2859, 10.1242/jeb.02260

Fields, 2004, Decreases in activation energy and substrate affinity in cold-adapted A4-lactate dehydrogenases: evidence from the Antarctic notothenioid fish Chaenocephalus aceratus, Mol. Biol. Evol., 21, 2246, 10.1093/molbev/msh237

Fields, 1998, Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A4 orthologs of Antarctic notothenioid fishes, Proc. Natl. Acad. Sci. USA, 95, 11476, 10.1073/pnas.95.19.11476

Fields, 2006, Temperature sensitivities of cytosolic malate dehydrogenases from native and invasive species of marine mussels (genus Mytilus): sequence-function linkages and correlations with biogeographic distribution, J. Exp. Biol., 209, 656, 10.1242/jeb.02036

Gilman, 2006, Variation in the sensitivity of organismal body temperature to climate change over local and geographic scales, Proc. Natl. Acad. Sci. USA, 103, 9560, 10.1073/pnas.0510992103

Harrison, 2002, Studying genomes through the aeons: protein families, pseudogenes and proteome evolution, J. Mol. Biol., 318, 1155, 10.1016/S0022-2836(02)00109-2

Helmuth, 2009, From cells to coastlines: how can we use physiology to forecast the impacts of climate change?, J. Exp. Biol., 212, 753, 10.1242/jeb.023861

Helmuth, 2002, Climate change and latitudinal patterns of intertidal thermal stress, Science, 298, 1015, 10.1126/science.1076814

Helmuth, 2006, Mosaic patterns of thermal stress in the rocky intertidal zone: implications for climate change, Ecol. Monogr., 76, 461, 10.1890/0012-9615(2006)076[0461:MPOTSI]2.0.CO;2

Hochachka, 2002, Biochemical adaptation: mechanism and process in physiological evolution, 10.1093/oso/9780195117028.001.0001

Hoffmann, 2008, Detecting genetic responses to environmental change, Nature Rev. Genet., 9, 421, 10.1038/nrg2339

Hoffmann, 2003, Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches, J. Therm. Biol., 28, 175, 10.1016/S0306-4565(02)00057-8

Hofmann, 2000, Heat shock protein expression is absent in the Antarctic fish Trematomus bernacchii (Family Nototheniidae), J. Exp. Biol., 203, 2331, 10.1242/jeb.203.15.2331

Holland, 1997, Evolution of lactate dehydrogenase-A homologs of barracuda fishes (Genus Sphyraena) from different thermal environments: differences in kinetic properties and thermal stability are due to amino acid substitutions outside the active site, Biochemistry, 36, 3207, 10.1021/bi962664k

Hull, 1999, Heat stability and activity levels of aspartate aminotransferase and alanine aminotransferase in British Littorinidae, J. Exp. Mar. Biol. Ecol., 237, 255, 10.1016/S0022-0981(99)00006-4

Johns, 2004, Evolutionary convergence in adaptation of proteins to temperature: A4-lactate dehydrogenases of Pacific damselfishes (Chromis spp.), Mol. Biol. Evol., 21, 314, 10.1093/molbev/msh021

Kuo, 2009, Geographic variation in the upper thermal limits of an intertidal snail: implications for climate envelope models, Mar. Ecol. Prog. Ser., 388, 137, 10.3354/meps08102

Meredith, 2005, Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century, Geophys. Letts., 32, L19604

Montgomery, 2000, Disaptation and recovery in the evolution of Antarctic fishes, Trends Ecol. Evol., 15, 267, 10.1016/S0169-5347(00)01896-6

Murphy, 2005, Transient response of the Hadley Centre coupled ocean-atmosphere model to increasing carbon dioxide, J. Climate, 8, 496, 10.1175/1520-0442(1995)008<0496:TROTHC>2.0.CO;2

Panova, 2004, Microscale variation in Aat (aspartate aminotransferase) is supported by activity differences between upper and lower shore allozymes of Littorina saxitalis, Mar. Biol., 144, 1157, 10.1007/s00227-003-1274-6

Peck, 2004, Extreme sensitivity of biological function to temperature in Antarctic marine species, Func. Ecol., 18, 625, 10.1111/j.0269-8463.2004.00903.x

Peck, 2009, Lack of acclimation in Ophionotus victoriae: brittle stars are not fish, Polar Biol., 32, 399, 10.1007/s00300-008-0532-y

Podrabsky, 2004, Changes in gene expression associated with acclimation to constant and fluctuating daily temperatures in an annual killfish Austrofundulus limnaeus, J. Exp. Biol., 207, 2237, 10.1242/jeb.01016

Podrabsky, 2006, Inducible heat tolerance in Antarctic notothenioid fishes, Polar Biol., 30, 39, 10.1007/s00300-006-0157-y

Pörtner, 2002, Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals, Comp. Biochem. Physiol. A, 132, 739, 10.1016/S1095-6433(02)00045-4

Pörtner, 2008, Ecology: physiology and climate change, Science, 322, 690, 10.1126/science.1163156

Pörtner, 2007, Climate change affects marine fishes through the oxygen limitation of thermal tolerance, Science, 315, 95, 10.1126/science.1135471

Pörtner, 2006, Thermal limits and adaptation in marine Antarctic ectotherms: an integrative view, Phil. Trans. R. Soc. B., 362, 2233, 10.1098/rstb.2006.1947

Pratt, 1997, The role of the hsp90-based chaperone system in signal transduction by nuclear receptors and receptors signalling via MAP kinase, Annu. Rev. Pharmacol. Toxicol., 37, 297, 10.1146/annurev.pharmtox.37.1.297

Rudd, 1954, Vertebrates without erythrocytes and blood pigment, Nature, 173, 848, 10.1038/173848a0

Savolainen, 2007, Gene flow and local adaptation in trees, Annu. Rev. Ecol. Evol. Syst., 38, 595, 10.1146/annurev.ecolsys.38.091206.095646

Schmidt, 2001, Adaptive maintenance of genetic polymorphism in an intertidal barnacle: habitat- and life-stage-specific survivorship of mpi genotypes, Evolution, 55, 1336, 10.1111/j.0014-3820.2001.tb00656.x

Sidell, 2006, When bad things happen to a good fish: the loss of hemoglobin and myoglobin expression in Antarctic icefishes, J. Exp. Biol., 209, 1791, 10.1242/jeb.02091

Sidell, 1997, Variable expression of myoglobin among the hemoglobinless Antarctic icefishes, Proc. Natl. Acad. Sci. USA, 94, 3420, 10.1073/pnas.94.7.3420

Somero, 2002, Thermal physiology and vertical zonation of intertidal animals: optima, limits and cost of living, Integr. Comp. Biol., 42, 780, 10.1093/icb/42.4.780

Somero, 2004, Temperature adaptation of proteins: searching for basic “strategies”, Comp. Biochem. Physiol., 139, 321, 10.1016/j.cbpc.2004.05.003

Somero, 2005, Linking biogeography to physiology: evolutionary and acclimatory adjustments of thermal limits, Front. Zool., 2, 1, 10.1186/1742-9994-2-1

Somero, 1967, Temperature tolerance of some Antarctic fishes, Science, 156, 257, 10.1126/science.156.3772.257

Stachowicz, 2002, Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions, Proc. Natl. Acad. Sci. USA, 99, 15497, 10.1073/pnas.242437499

Stenseng, 2005, Evolutionary and acclimation-induced variation in the thermal limits of heart function in congeneric marine snails (genus Tegula): implications for vertical zonation, Biol. Bull., 208, 138, 10.2307/3593122

Stillman, 2002, Causes and consequences of thermal tolerance limits in rocky intertidal porcelain crabs, genus Petrolisthes, Integ. Comp. Biol., 42, 790, 10.1093/icb/42.4.790

Stillman, 2003, Acclimation capacity underlies susceptibility to climate change, Science, 301, 65, 10.1126/science.1083073

Stillman, 1996, Adaptation to temperature stress and aerial exposure in congeneric species of intertidal porcelain crabs (genus Petrolisthes): correlation of physiology, biochemistry and morphology with vertical distribution, J. Exp. Biol., 199, 1845, 10.1242/jeb.199.8.1845

Stillman, 2000, A comparative analysis of the upper thermal tolerance limits of eastern Pacific porcelain crabs, Genus Petrolisthes: influences of latitude, vertical zonation, acclimation and phylogeny, Physiol. Biochem. Zool., 73, 200, 10.1086/316738

Storch, 2009, Thermal tolerance of crustacean larvae (zoea I) in two different populations of the kelp crab Taliepus dentatus (Milne-Edwards), J. Exp. Biol., 212, 1371, 10.1242/jeb.030205

Tewksbury, 2008, Putting the heat on tropical animals, Science, 320, 1296, 10.1126/science.1159328

Tomanek, 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, 10.1242/jeb.202.21.2925

Watt, 2000, Molecular-functional studies of adaptive genetic variation in prokaryotes and eukaryotes, Annu. Rev. Genet., 34, 593, 10.1146/annurev.genet.34.1.593

Wolcott, 1973, Physiological ecology and intertidal zonation in limpets (Acmaea): a critical look at “limiting factors”, Biol. Bull., 145, 389, 10.2307/1540048