Restricted access
Research articles
Research articlesRapid evolution of cold tolerance in stickleback
Published:04 August 2010https://doi.org/10.1098/rspb.2010.0923
Abstract
Climate change is predicted to lead to increased average temperatures and greater intensity and frequency of high and low temperature extremes, but the evolutionary consequences for biological communities are not well understood. Studies of adaptive evolution of temperature tolerance have typically involved correlative analyses of natural populations or artificial selection experiments in the laboratory. Field experiments are required to provide estimates of the timing and strength of natural selection, enhance understanding of the genetics of adaptation and yield insights into the mechanisms driving evolutionary change. Here, we report the experimental evolution of cold tolerance in natural populations of threespine stickleback fish (Gasterosteus aculeatus). We show that freshwater sticklebacks are able to tolerate lower minimum temperatures than marine sticklebacks and that this difference is heritable. We transplanted marine sticklebacks to freshwater ponds and measured the rate of evolution after three generations in this environment. Cold tolerance evolved at a rate of 0.63 haldanes to a value 2.5°C lower than that of the ancestral population, matching values found in wild freshwater populations. Our results suggest that cold tolerance is under strong selection and that marine sticklebacks carry sufficient genetic variation to adapt to changes in temperature over remarkably short time scales.
References
- 1
Crowley T. J.& North G. R. . 1988Abrupt climate change and extinction events in earth history. Science 240, 996–1002.doi:10.1126/science.240.4855.996 (doi:10.1126/science.240.4855.996). Crossref, PubMed, Google Scholar - 2
Deutsch C., Tewksbury J., Huey R., Sheldon K., Ghalambor C., Haak D.& Martin P. . 2008Impacts of climate warming on terrestrial ectotherms across latitude. Proc. Natl Acad. Sci. USA 105, 6668–6672.doi:10.1073/pnas.0709472105 (doi:10.1073/pnas.0709472105). Crossref, PubMed, Google Scholar - 3
Hoffmann A. A., Hallas R. J., Dean J. A.& Schiffer M. . 2003Low potential for climatic stress adaptation in a rainforest Drosophila species. Science 301, 100–102.doi:10.1126/science.1084296 (doi:10.1126/science.1084296). Crossref, PubMed, Google Scholar - 4
Huey R. B., Deutsch C. A., Tewksbury J. J., Vitt L. J.& Hertz P. E. . 2009Why tropical lizards are vulnerable to climate warming. Proc. R. Soc. B 276, 1939–1948.doi:10.1098/rspb.2008.1957 (doi:10.1098/rspb.2008.1957). Link, Google Scholar - 5
Malcolm J. R., Liu C., Neilson R. P.& Hansen L. . 2006Global warming and extinctions of endemic species from biodiversity hotspots. Conserv. Biol. 20, 538–548.doi:10.1111/j.1523-1739.2006.00364.x (doi:10.1111/j.1523-1739.2006.00364.x). Crossref, PubMed, Google Scholar - 6
Thomas C. D., 2004Extinction risk from climate change. Nature 427, 145–148.doi:10.1038/nature02121 (doi:10.1038/nature02121). Crossref, PubMed, ISI, Google Scholar - 7
Skelly D. K., Joseph L. N., Possingham H. P., Freidenburg L. K., Farrugia T. J., Kinnison M. T.& Hendry A. P. . 2007Evolutionary responses to climate change. Conserv. Biol. 21, 1353–1355.doi:10.1111/j.1523-1739.2007.00764.x (doi:10.1111/j.1523-1739.2007.00764.x). Crossref, PubMed, Google Scholar - 8
Bell G.& Collins S. . 2008Adaptation, extinction and global change. Evol. Appl. 1, 3–16.doi:10.1111/j.1752-4571.2007.00011.x (doi:10.1111/j.1752-4571.2007.00011.x). Crossref, PubMed, Google Scholar - 9
Bradshaw W. E.& Holzapfel C. M. . 2006Evolutionary response to rapid climate change. Science 312, 1477–1478.doi:10.1126/science.1127000 (doi:10.1126/science.1127000). Crossref, PubMed, Google Scholar - 10
Smith T. B.& Bernatchez L. . 2008Evolutionary change in human-altered environments. Mol. Ecol. 17, 1–8.doi:10.1111/j.1365-294X.2007.03607.x (doi:10.1111/j.1365-294X.2007.03607.x). Crossref, PubMed, Google Scholar - 11
Balanya J., Oller J. M., Huey R. B., Gilchrist G. W.& Serra L. . 2006Global genetic change tracks global climate warming in Drosophila subobscura. Science 313, 1773–1775.doi:10.1126/science.1131002 (doi:10.1126/science.1131002). Crossref, PubMed, Google Scholar - 12
Bearhop S., Fiedler W., Furness R. W., Votier S. C., Waldron S., Newton J., Bowen G. J., Berthold P.& Farnsworth K. . 2005Assortative mating as a mechanism for rapid evolution of a migratory divide. Science 310, 502–504.doi:10.1126/science.1115661 (doi:10.1126/science.1115661). Crossref, PubMed, ISI, Google Scholar - 13
Berthold P., Helbig A. J., Mohr G.& Querner U. . 1992Rapid microevolution of migratory behavior in a wild bird species. Nature 360, 668–670.doi:10.1038/360668a0 (doi:10.1038/360668a0). Crossref, Google Scholar - 14
Bradshaw W.& Holzapfel C. . 2001Genetic shift in photoperiodic response correlated with global warming. Proc. Natl Acad. Sci. USA 98, 14 509–14 511.doi:10.1073/pnas.241391498 (doi:10.1073/pnas.241391498). Crossref, Google Scholar - 15
Jonzen N., 2006Rapid advance of spring arrival dates in long-distance migratory birds. Science 312, 1959–1961.doi:10.1126/science.1126119 (doi:10.1126/science.1126119). Crossref, PubMed, Google Scholar - 16
Kausrud K. L., 2008Linking climate change to lemming cycles. Nature 456, 93–97.doi:10.1038/nature07442 (doi:10.1038/nature07442). Crossref, PubMed, Google Scholar - 17
Nussey D. H., Postma E., Gienapp P.& Visser M. E. . 2005Selection on heritable phenotypic plasticity in a wild bird population. Science 310, 304–306.doi:10.1126/science.1117004 (doi:10.1126/science.1117004). Crossref, PubMed, ISI, Google Scholar - 18
Reale D., Berteaux D., McAdam A. G.& Boutin S. . 2003Lifetime selection on heritable life-history traits in a natural population of red squirrels. Evolution 57, 2416–2423. Crossref, PubMed, Google Scholar - 19
Umina P. A., Weeks A. R., Kearney M. R., McKechnie S. W.& Hoffmann A. A. . 2005A rapid shift in a classic clinal pattern in Drosophila reflecting climate change. Science 308, 691–693.doi:10.1126/science.1109523 (doi:10.1126/science.1109523). Crossref, PubMed, Google Scholar - 20
Partridge L., Prowse N.& Pignatelli P. . 1999Another set of responses and correlated responses to selection on age at reproduction in Drosophila melanogaster. Proc. R. Soc. Lond. B 266, 255–261.doi:10.1098/rspb.1999.0630 (doi:10.1098/rspb.1999.0630). Link, Google Scholar - 21
Beitinger T. L., Bennett W. A.& McCauley R. W. . 2000Temperature tolerances of North American freshwater fishes exposed to dynamic changes in temperature. Environ. Biol. Fish. 58, 237–275.doi:10.1023/A:1007676325825 (doi:10.1023/A:1007676325825). Crossref, Google Scholar - 22
Fangue N. A., Hofmeister M.& Schulte P. M. . 2006Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus. J. Exp. Biol. 209, 2859–2872.doi:10.1242/jeb.02260 (doi:10.1242/jeb.02260). Crossref, PubMed, Google Scholar - 23
Schluter D. . 1994Experimental evidence that competition promotes divergence in adaptive radiation. Science 266, 798–801.doi:10.1126/science.266.5186.798 (doi:10.1126/science.266.5186.798). Crossref, PubMed, Google Scholar - 24
Schluter D. . 2003Frequency dependent natural selection during character displacement in sticklebacks. Evolution 57, 1142–1150. Crossref, PubMed, Google Scholar - 25
Day T., Pritchard J.& Schluter D. . 1994A comparison of two sticklebacks. Evolution 48, 1723–1734.doi:10.2307/2410260 (doi:10.2307/2410260). Crossref, PubMed, Google Scholar - 26
Barrett R. D. H., Rogers S. M.& Schluter D. . 2008Natural selection on a major armor gene in threespine stickleback. Science 322, 255–257.doi:10.1126/science.1159978 (doi:10.1126/science.1159978). Crossref, PubMed, Google Scholar - 27
Colosimo P. F., 2005Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307, 1928–1933.doi:10.1126/science.1107239 (doi:10.1126/science.1107239). Crossref, PubMed, Google Scholar - 28
Hendry A. P.& Kinnison M. T. . 1999Perspective: the pace of modern life: measuring rates of contemporary microevolution. Evolution 53, 1637–1653.doi:10.2307/2640428 (doi:10.2307/2640428). Crossref, PubMed, Google Scholar - 29
Easterling D. R., Meehl G. A., Parmesan C., Changnon S. A., Karl T. R.& Mearns L. O. . 2000Climate extremes: observations, modeling, and impacts. Science 289, 2068–2074.doi:10.1126/science.289.5487.2068 (doi:10.1126/science.289.5487.2068). Crossref, PubMed, ISI, Google Scholar - 30
Gienapp P., Teplitsky C., Alho J. S., Mills J. A.& Merila J. . 2008Climate change and evolution: disentangling environmental and genetic responses. Mol. Ecol. 17, 167–178.doi:10.1111/j.1365-294X.2007.03413.x (doi:10.1111/j.1365-294X.2007.03413.x). Crossref, PubMed, Google Scholar - 31
Lenton T. M., Held H., Kriegler E., Hall J. W., Lucht W., Rahmstorf S.& Schellnhuber H. J. . 2008Tipping elements in the Earth's climate system. Proc. Natl Acad. Sci. USA 105, 1786–1793.doi:10.1073/pnas.0705414105 (doi:10.1073/pnas.0705414105). Crossref, PubMed, ISI, Google Scholar - 32
Loarie S. R., Duffy P. B., Hamilton H., Asner G. P., Field C. B.& Ackerly D. D. . 2009The velocity of climate change. Nature 462, 1052–1055.doi:10.1038/nature08649 (doi:10.1038/nature08649). Crossref, PubMed, Google Scholar - 33
Meehl G. A.& Tebaldi C. . 2004More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305, 994–997.doi:10.1126/science.1098704 (doi:10.1126/science.1098704). Crossref, PubMed, ISI, Google Scholar - 34United Nations Environmental Programme. 2009Climate Change Science Compendium. See http://www.unep.org/compendium2009/. Google Scholar
- 35
Schar C., Vidale P., Luthi D., Frei C., Haberli C., Liniger M.& Appenzeller C. . 2004The role of increasing temperature variability in European summer heatwaves. Nature 427, 332–336.doi:10.1038/nature02300 (doi:10.1038/nature02300). Crossref, PubMed, Google Scholar - 36
Darimont C., Carlson S., Kinnison M., Paquet P., Reimchen T.& Wilmers C. . 2009Human predators outpace other agents of trait change in the wild. Proc. Natl Acad. Sci. USA 106, 952.doi:10.1073/pnas.0809235106 (doi:10.1073/pnas.0809235106). Crossref, PubMed, Google Scholar - 37
Kinnison M., Unwin M.& Quinn T. . 2008Eco-evolutionary versus habitat contributions to invasion in salmon: experimental evaluation in the wild. Mol. Ecol. 17, 405–414.doi:10.1111/j.1365-294X.2007.03495.x (doi:10.1111/j.1365-294X.2007.03495.x). Crossref, PubMed, Google Scholar - 38
Yoshida T., Jones L., Ellner S., Fussmann G.& Hairston N. . 2003Rapid evolution drives ecological dynamics in a predator–prey system. Nature 424, 303–306.doi:10.1038/nature01767 (doi:10.1038/nature01767). Crossref, PubMed, Google Scholar - 39Environment Canada. 2010Vancouver Airport Weather Station. Climate ID 1108447. National Climate Data and Information Archive. Google Scholar
- 40
Bell M. A., Aguirre W. E.& Buck N. J. . 2004Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution 58, 814–824. Crossref, PubMed, ISI, Google Scholar - 41
Klepaker T. . 1993Morphological changes in a marine population of threespined stickleback, Gasterosteus aculeatus, recently isolated in fresh water. Can. J. Zool. 71, 1251–1258.doi:10.1139/z93-171 (doi:10.1139/z93-171). Crossref, Google Scholar - 42
Kristjansson B. K. . 2005Rapid morphological changes in threespine stickleback, Gasterosteus aculeatus, in freshwater. Environ. Biol. Fish. 74, 357–363.doi:10.1007/s10641-005-1487-2 (doi:10.1007/s10641-005-1487-2). Crossref, Google Scholar - 43
Kristjansson B. K., Skulason S.& Noakes D. L. G. . 2002Rapid divergence in a recently isolated population of threespine stickleback (Gasterosteus aculeatus L.). Evol. Ecol. Res. 4, 659–672. Google Scholar - 44
Ramanathan V.& Feng Y. . 2008On avoiding dangerous anthropogenic interference with the climate system: formidable challenges ahead. Proc. Natl Acad. Sci. USA 105, 14 245–14 250.doi:10.1073/pnas.0803838105 (doi:10.1073/pnas.0803838105). Crossref, Google Scholar
