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8 - Climate warming results in phenotypic and evolutionary changes in spring events: a mini-review

from Section 2 - Adaptation, speciation and extinction

Published online by Cambridge University Press:  16 May 2011

By
A. Donnelly ,
A. Caffarra ,
E. Diskin ,
C. T. Kelleher ,
A. Pletsers ,
H. Proctor ,
R. Stirnemann ,
M. B. Jones ,
J. O'Halloran  and
B. F. O'Neill
...Show all authors
Edited by
Trevor R. Hodkinson ,
Michael B. Jones ,
Stephen Waldren  and
John A. N. Parnell
A. Donnelly
Affiliation:
Trinity College Dublin, Ireland
A. Caffarra
Affiliation:
Istituto Agrario San Michele all'Adige, Italy
E. Diskin
Affiliation:
Trinity College Dublin, Ireland
C. T. Kelleher
Affiliation:
National Botanic Gardens, Glasnevin, Dublin, Ireland
A. Pletsers
Affiliation:
Trinity College Dublin, Ireland
H. Proctor
Affiliation:
Trinity College Dublin, Ireland
R. Stirnemann
Affiliation:
Trinity College Dublin, Ireland
M. B. Jones
Affiliation:
Trinity College Dublin, Ireland
J. O'Halloran
Affiliation:
University College Cork, Ireland
B. F. O'Neill
Affiliation:
Trinity College Dublin, Ireland
J. Peñuelas
Affiliation:
Campus Universitat Autònoma de Barcelona, Spain
T. Sparks
Affiliation:
Technische Universität München, Germany and Institute of Zoology, Poznań University of Life Sciences, University of Cambridge, UK
Trevor R. Hodkinson
Affiliation:
Trinity College, Dublin
Michael B. Jones
Affiliation:
Trinity College, Dublin
Stephen Waldren
Affiliation:
Trinity College, Dublin
John A. N. Parnell
Affiliation:
Trinity College, Dublin
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Summary

Abstract

The impact of climate change, in particular increasing spring temperatures, on life-cycle events of plants and animals has gained scientific attention in recent years. Leafing of trees, appearance and abundance of insects, and migration of birds, across a range of species and countries, have been cited as phenotrends that are advancing in response to warmer spring temperatures. The ability of organisms to acclimate to variations in environmental conditions is known as phenotypic plasticity. Plasticity allows organisms to time developmental stages to coincide with optimum availability of environmental resources. There may, however, come a time when the limit of this plasticity is reached and the species needs to adapt genetically to survive. Here we discuss evidence of the impact of climate warming on plant, insect and bird phenology through examination of: (1) phenotypic plasticity in (a) bud burst in trees, (b) appearance of insects and (c) migration of birds; and (2) genetic adaptation in (a) gene expression during bud burst in trees, (b) the timing of occurrence of phenological events in insects and (c) arrival and breeding times of migratory birds. Finally, we summarise the potential consequences of future climatic changes for plant, insect and bird phenology.

Introduction

The recent resurgence of interest in phenology (the timing of recurring life-cycle events in plants and animals) has stemmed from research on the impact of climate change, in particular, global warming.

Type
Chapter
Information
Climate Change, Ecology and Systematics , pp. 176 - 200
Publisher: Cambridge University Press
Print publication year: 2011

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References

Ahola, M. P., Laaksonen, T., Eeva, T. and Lehikoinen, E. (2007). Climate change can alter competitive relationships between resident and migratory birds. Journal of Animal Ecology, 76, 1045–1052.CrossRefGoogle ScholarPubMed
Aitken, S. N., Yeaman, S., Holliday, J. A., Wang, T. and Curtis-McLane, S. (2008). Adaptation, migration or extirpation: climate change outcomes for tree populations. Evolutionary Applications, 1, 95–111.CrossRefGoogle ScholarPubMed
Arora, R., Rowland, L. J. and Tanino, K. (2003). Induction and release of bud dormancy in woody perennials, a science comes of age. Hortscience, 38, 911–921.Google Scholar
Bale, J. S., Masters, G. J., Hodkinson, I. D. et al. (2002). Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology, 8, 1–16.CrossRefGoogle Scholar
Barrett, R. T. (2002). The phenology of spring bird migration to north Norway. Bird Study, 49, 270–277.CrossRefGoogle Scholar
Bearhop, S., Fiedler, W., Furness, R. W. et al. (2005). Assortative mating as a mechanism for rapid evolution of a migratory divide. Science, 310, 502–504.CrossRefGoogle ScholarPubMed
Böhlenius, H., Huang, T., Charbonnel-Campaa, L. et al. (2006). The conserved CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science, 312, 1040–1043.CrossRefGoogle Scholar
Both, C. (2007). Comment on ‘rapid advance of spring arrival dates in long-distance migratory birds’. Science, 315, 1959–1961.CrossRefGoogle Scholar
Both, C. and Te Marvelde, L. (2007). Climate change and timing of avian breeding and migration through Europe. Climate Research, 35, 93–105.CrossRefGoogle Scholar
Both, C. and Visser, M. (2001). Adjustment to climate change is constrained by arrival date in a long-distance migrant bird. Nature, 411, 296–298.CrossRefGoogle Scholar
Both, C., Bijlsma, R. G. and Visser, M. (2005). Climatic effects on timing of spring migration and breeding in a long-distance migrant, the pied flycatcher Ficedula hypoleuca. Journal of Avian Biology, 36, 368–373.CrossRefGoogle Scholar
Both, C., Bouwhuis, S., Lessells, C. M. and Visser, M. E. (2006). Climate change and population declines in a long-distance migratory bird. Nature, 441, 81–83.CrossRefGoogle Scholar
Bradshaw, A. D. (1965). Evolutionary significance of phenotypic plasticity in plants. Advances in Genetics, 13, 115–155.Google Scholar
Bradshaw, H. D. and Stettler, R. F. (1995). Molecular genetics of growth and development in Populus. IV. Mapping QTLs with large effects on growth, form, and phenology traits in a forest tree. Genetics, 139, 963–973.Google Scholar
Bradshaw, W. E. and Holzapfel, C. M. (2001). Genetic shift in photoperiodic response correlated with global warming. Proceedings of the National Academy of Sciences of the USA, 98, 14509–14511.CrossRefGoogle ScholarPubMed
Bradshaw, W. E. and Holzapfel, C. M. (2006). Evolutionary response to rapid climate change. Science, 312, 1477–1478.CrossRefGoogle ScholarPubMed
Brommer, J. E., Merilä, J., Sheldon, B. C. and Gustafsson, L. (2005). Natural selection and genetic variation for reproductive reaction norms in a wild bird population. Evolution, 59, 1362–1371.CrossRefGoogle Scholar
Charmantier, A., McCleery, R. H., Cole, L. R. et al. (2008). Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science, 322, 800–803.CrossRefGoogle Scholar
Chmielewski, F. M. and Rö tzer, T. (2001). Responses of tree phenology to climatic changes across Europe. Agricultural and Forest Meteorology, 108, 101–112.CrossRefGoogle Scholar
Cleland, E. E., Chuine, I., Menzel, A., Mooney, H. A. and Schwartz, M. D. (2007). Shifting plant phenology in response to global change. Trends in Ecology and Evolution, 22, 357–365.CrossRefGoogle ScholarPubMed
Coleman, G. D. and Chen, K. Y. (2008). Regulation of FLC-like genes and bud dormancy in poplar. Plant and Animal Genome Conference XVI, San Diego, CA. www.intl-pag.org/16/abstracts/PAG16_W10_80.html.
Collier, R. H., Finch, S., Phelps, K. and Thompson, A. R. (1991). Possible impact of global warming on cabbage root fly (Delia radicum) activity in the UK. Annals of Applied Biology, 118, 261–271.CrossRefGoogle Scholar
Cotton, P. A. (2003). Avian migration phenology and global climate change. Proceedings of the National Academy of Sciences of the USA, 100, 12219–12222.CrossRefGoogle ScholarPubMed
Crabbe, J. (1994). Dormancy. Encyclopedia of Agricultural Sciences. Volume I. New York, NY: Academic Press.Google Scholar
Davis, M. B. and Shaw, R. G. (2001). Range shifts and adaptive responses to Quaternary climate change. Science, 292, 673–679.CrossRefGoogle ScholarPubMed
Donnelly, A., Salamin, N. and Jones, M. B. (2006). Changes in tree phenology: an indicator of spring warming in Ireland?Biology and Environment: Proceedings of the Royal Irish Academy, 106, 47–55.Google Scholar
Donnelly, A., Cooney, T., Jennings, E., Buscardo, E. and Jones, M. B. (2009). Response of birds to climatic variability; evidence from the western fringe of Europe. International Journal of Biometeorology, 53, 211–220.CrossRefGoogle ScholarPubMed
Edwards, M. and Richardson, A. J. (2004). Impact of climate change on marine pelagic phenology and trophic mismatch. Nature, 430, 881–884.CrossRefGoogle ScholarPubMed
Forkner, R. E., Marquis, R. J., Lill, J. T. and Le Corff, J. (2008). Timing is everything? Phenological synchrony and population variability in leaf-chewing herbivores of Quercus. Ecological Entomology, 33, 276–285.CrossRefGoogle Scholar
García-Gil, M. R., Mikkonen, M. and Savolainen, O. (2003). Nucleotide diversity at two phytochrome loci along a latitudinal cline in Pinus sylvestris. Molecular Ecology, 12, 1195–1206.CrossRefGoogle Scholar
Gilchrist, G. W. (1995). Specialists and generalists in changing environments. I. Fitness landscapes of thermal sensitivity. American Naturalist, 146, 252–270.CrossRefGoogle Scholar
Gordo, O. and Sanz, J. J. (2006). Temporal trends in phenology of the honey bee Apis mellifera (L.) and the small white Pieris rapae (L.) in the Iberian Peninsula (1952–2004). Ecological Entomology, 31, 261–268.CrossRefGoogle Scholar
Hall, D., Luquez, V., Garcia, V. M. et al. (2007). Adaptive population differentiation in phenology across a latitudinal gradient in European aspen (Populus tremula, L.): a comparison of neutral markers, candidate genes and phenotypic traits. Evolution, 61, 2849–2860.CrossRefGoogle ScholarPubMed
Harrington, R., Woiwod, I. and Sparks, T. (1999). Climate change and trophic interactions. Trends in Ecology and Evolution, 14, 146–150.CrossRefGoogle ScholarPubMed
Hartl, D. L. and Jones, E. W. (2009). Genetics: Analysis of Genes and Genomes, 7th edn. Boston, MA: Jones and Bartlett.Google Scholar
Hegland, S. J., Nielsen, A., Lázaro, A., Bjerknes, A. and Totland, , Ø. (2008). How does climate warming affect plant–pollinator interactions?Ecology Letters, 12, 184–195.CrossRefGoogle ScholarPubMed
Herre, E. A., Knowlton, N., Mueller, U. G. and Rehner, S. A. (1999). The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends in Ecology and Evolution, 14, 49–53.CrossRefGoogle ScholarPubMed
Horvath, D. P., Anderson, J. V., Chao, W. S. and Foley, M. F. (2003). Knowing when to grow: signals regulating bud dormancy. Trends in Plant Science, 8, 534–540.CrossRefGoogle ScholarPubMed
Huntley, B. (2007). Evolutionary response to climate change?Heredity, 98, 247–248.CrossRefGoogle Scholar
Hüppop, O. and Hüppop, K. (2003). North Atlantic Oscillation and timing of spring migration in birds. Proceedings of the Royal Society of London B, 270, 233–240.CrossRefGoogle ScholarPubMed
Hsu, C. Y., Liu, Y., Luthe, D. S. and Yuceer, C. (2006). Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. Plant and Cell Physiology, 49, 291–300.Google Scholar
Ingvarsson, P. K., García, M. V., Hall, D., Luquez, V. and Jansson, S. (2006). Clinal variation inphyB2, a candidate gene for day-length-induced growth cessation and bud set, across a latitudinal gradient in European aspen (Populus tremula). Genetics, 172, 1845–1853.Google ScholarPubMed
,Intergovernmental Panel on Climate Change (IPCC) (2007). Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, ed. Parry, M., Canziani, O., Palutikof, J., Linden, P. and Hanson, C.. Cambridge: Cambridge University Press.Google Scholar
Jansson, S. and Douglas, C. J. (2007). Populus: a model system for plant biology. Annual Review of Plant Biology, 58, 435–458.CrossRefGoogle ScholarPubMed
Jonzén, N., Lindén, A., Ergon, T. et al. (2006). Rapid advance of spring arrival dates in long-distance migratory birds. Science, 312, 1959–1961.CrossRefGoogle ScholarPubMed
Jump, A. S. and Peñuelas, J. (2005). Running to stand still: adaptation and the response of plants to rapid climate change. Ecology Letters, 8, 1010–1020.CrossRefGoogle Scholar
Jump, A. S., Hunt, J. M., Martinez-Izquierdo, J. A. and Peñuelas, J. (2006). Natural selection and climate change: temperature-linked spatial and temporal trends in gene frequency in Fagus sylvatica. Molecular Ecology, 15, 3469–3480.CrossRefGoogle ScholarPubMed
Jump, A. S., Peñuelas, J., Rico, L. et al. (2008). Simulated climate change provokes rapid genetic change in the Mediterranean shrub Fumana thymifolia. Global Change Biology, 14, 637–643.CrossRefGoogle Scholar
Kellermann, V. M., Heerwaarden, B., Hoffmann, A. A. and Sgrò, C. M. (2006). Very low additive genetic variance and evolutionary potential in multiple populations of two rainforest Drosophila species. Evolution, 60, 1104–1108.CrossRefGoogle ScholarPubMed
Kruuk, L. E. B. (2004). Estimating genetic parameters in natural populations using the ‘animal model’. Philosophical Transactions of the Royal Society of London B, 359, 873–890.CrossRefGoogle Scholar
Lang, G. A., Early, J. D., Martin, G. C. and Darnell, R. L. (1987). Endodormancy, paradormancy, and ecodormancy – physiological terminology and classification for dormancy research. Hortscience, 22, 371–377.Google Scholar
Law, R. D. and Suttle, J. C. (2003). Transient decreases in methylation at 5'-cCGG-3'sequences in potato (Solanum tuberosum) meristem DNA during progression of tubers through dormancy precede the resumption of sprout growth. Plant Molecular Biology, 51, 437–447.CrossRefGoogle ScholarPubMed
Lechowics, M. J. (1984). Why do temperate deciduous trees leaf out at different times? Adaptation and ecology of forest communities. American Naturalist, 124, 821–842.CrossRefGoogle Scholar
Lehikoinen, E., Sparks, T. H. and Zalakevicius, M. (2004). Arrival and departure dates. In Birds and Climate Change. Advances in Ecological Research, Vol. 35, ed. Møller, A. P., Fiedler, W. and Berthold, P.. London, UK: Academic Press, pp. 1–31.Google Scholar
Levitan, M. and Etges, W. J. (2005). Climate change and recent genetic flux in populations of Drosophila robusta. BMC Evolutionary Biology, 5, 4.CrossRefGoogle ScholarPubMed
Lyon, B. E., Chaine, A. S. and Winkler, D. W. (2008). A matter of timing. Science, 321, 1051–1052.CrossRefGoogle ScholarPubMed
Memmott, J., Craze, P. G., Waser, N. M. and Price, M. V. (2007). Global warming and the disruption of plant–pollinator interactions. Ecology Letters, 10, 710–717.CrossRefGoogle ScholarPubMed
Menzel, A. and Fabian, P. (1999). Growing season extended in Europe. Nature, 397, 659.CrossRefGoogle Scholar
Menzel, A., Sparks, T. H., Estrella, N. et al. (2006). European phenological response to climate change matches the warming pattern. Global Change Biology, 12, 1–8.CrossRefGoogle Scholar
Møller, A. P., Rubolini, D. and Lehikoinen, E. (2008). Populations of migratory bird species that did not show a phenological response to climate change are declining. Proceedings of the National Academy of Sciences of the USA, 105, 16195–16200.CrossRefGoogle Scholar
Neale, D. B. and Savolainen, O. (2004). Association genetics of complex traits in conifers. Trends in Plant Science, 9, 325–330.CrossRefGoogle ScholarPubMed
Nussey, D. H., Postma, E., Gienapp, P. and Visser, M. E. (2005). Selection on heritable phenotypic plasticity in a wild bird population. Science, 310, 304–306.CrossRefGoogle Scholar
Ogaya, R. and Peñuelas, J. (2007). Tree growth, mortality, and above-ground biomass accumulation in a holm oak forest under a five-year experimental field drought. Plant Ecology, 189, 291–299.CrossRefGoogle Scholar
Olsen, J. E., Junttila, O., Nilsen, J. et al. (1997). Ectopic expression of oat phytochrome A in hybrid aspen changes critical daylength for growth and prevents cold acclimatization. The Plant Journal, 12, 1339–1350.CrossRefGoogle Scholar
Parmesan, C. (2006). Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics, 37, 637–669.CrossRefGoogle Scholar
Pearson, R. G. and Dawson, T. P. (2003). Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful?Global Ecology and Biogeography, 12, 361–371.CrossRefGoogle Scholar
Pellmyr, O. and Leebens-Mack, J. (1999). Forty million years of mutualism: evidence for Eocene origin of the yucca–yucca moth association. Proceedings of the National Academy of Sciences of the USA, 96, 9178–9183.CrossRefGoogle ScholarPubMed
Peñuelas, J. and Filella, I. (2001). Responses to a warming world. Science, 294, 793–795.CrossRefGoogle ScholarPubMed
Pulido, F. (2007). Phenotypic changes in spring arrival: evolution, phenotypic plasticity, effects of weather and condition. Climate Research, 35, 5–23.CrossRefGoogle Scholar
Pulido, F., Berthold, P., Mohr, G. and Querner, U. (2001). Heritability of the timing of autumn migration in a natural bird population. Proceedings of the Royal Society of London B, 268, 953–959.CrossRefGoogle Scholar
Rathcke, B. and Lacey, E. P. (1985). Phenological patterns of terrestrial plants. AnnualReview of Ecology and Systematics, 16, 179–214.Google Scholar
Reed, T. E., Wanless, S., Harris, M. P. et al. (2006). Responding to environmental change: plastic responses vary little in a synchronous breeder. Proceedings of the Royal Society of London B, 273, 2713–2719.CrossRefGoogle Scholar
Reed, T. E., Kruuk, L. E., Wanless, S. et al. (2008). Reproductive senescence in a long-lived seabird: rates of decline in late-life performance are associated with varying costs of early reproduction. American Naturalist, 171, 89–101.CrossRefGoogle Scholar
Rodriguez-Falcon, M., Bou, J. and Prat, S. (2006). Seasonal control of tuberization in potato: conserved elements with the flowering response. Annual Review of Plant Biology, 57, 151–180.CrossRefGoogle ScholarPubMed
Rodriguez-Trelles, F. and Rodriguez, M. A. (1998). Rapid micro-evolution and loss of chromosomal diversity in Drosophila in response to climate warming. Evolutionary Ecology, 12, 829–838.CrossRefGoogle Scholar
Rohde, A. and Bhalerao, R. P. (2007). Plant dormancy in the perennial context. Trends in Plant Science, 12, 217–223.CrossRefGoogle ScholarPubMed
Roy, D. B. and Sparks, T. H. (2000). Phenology of British butterflies and climate change. Global Change Biology, 6, 407–416.CrossRefGoogle Scholar
Ruttink, T., Arend, M., Morreel, K. et al. (2007). A molecular timetable for apical bud formation and dormancy induction in poplar. The Plant Cell, 19, 2370–2390.CrossRefGoogle ScholarPubMed
Saino, N. and Ambrosini, R. (2008). Climatic connectivity between Africa and Europe may serve as a basis for phenotypic adjustment of migration schedules of trans-Saharan migratory birds. Global Change Biology, 14, 250–263.CrossRefGoogle Scholar
Savolainen, O. and Pyhäjärvi, T. (2007). Genomic diversity in forest trees. Current Opinion in Plant Biology, 10, 162–167.CrossRefGoogle ScholarPubMed
Savolainen, O., Pyhäjärvi, T. and Knürr, T. (2007). Gene flow and local adaptation in trees. Annual Review of Ecology, Evolution, and Systematics, 38, 595–619.CrossRefGoogle Scholar
Sparks, T. H. and Tryjanowski, P. (2007). Patterns of spring arrival dates differ in two hirundines. Climate Research, 35, 159–164.CrossRefGoogle Scholar
Sparks, T. H., Bairlein, F., Bojarinova, J. G. et al. (2005). Examining the total arrival distribution of migratory birds. Global Change Biology, 11, 22–30.CrossRefGoogle Scholar
Stefanescu, C., Peñuelas, J. and Filella, I. (2003). Effects of climatic change on the phenology of butterflies in the northwest Mediterranean Basin. Global Change Biology, 9, 1494–1506.CrossRefGoogle Scholar
Stenseth, N. C. and Mysterud, A. (2002). Climate, changing phenology, and other life history traits: non-linearity and match-mismatch to the environment. Proceedings of the National Academy of Sciences of the USA, 99, 13379–13381.CrossRefGoogle Scholar
Stenseth, N. C., Mysterud, A., Ottersen, G. et al. (2002). Ecological effects of climate fluctuations. Science, 23, 1292–1296.CrossRefGoogle Scholar
Sung, S. and Amasino, R. M. (2005). Remembering winter: toward a molecular understanding of vernalization. Annual Review of Plant Biology, 56, 491–508.CrossRefGoogle Scholar
Tauber, M. J. and Tauber, C. A. (1976). Insect seasonality: diapause maintenance, termination, and postdiapause development. Annual Review of Entomology, 21, 81–107.CrossRefGoogle Scholar
Umina, P. A., Weeks, A. R., Kearney, M. R., McKechnie, S. W. and Hoffmann, A. A. (2008). A rapid shift in classical clinal pattern in Drosophila reflecting climate change. Science, 308, 691–693.CrossRefGoogle Scholar
Vähätalo, A. V., Rainio, K., Lehikoinen, A. and Lehikoinen, E. (2004). Spring arrival of birds depends on the North Atlantic Oscillation. Journal of Avian Biology, 35, 210–216.CrossRefGoogle Scholar
Asch, M. and Visser, M. E. (2007). Phenology of forest caterpillars and their host trees: the importance of synchrony. Annual Review of Entomology, 52, 37–55.CrossRefGoogle Scholar
Asch, M., Tienderen, P. H., Holleman, L. J. M. and Visser, M. E. (2007). Predicting adaptation of phenology in response to climate change, an insect herbivore example. Global Change Biology, 13, 1596–1604.CrossRefGoogle Scholar
Visser, M. E., Noordwijk, A. J., Tinbergen, J. M. and Lessells, C. M. (1998). Warmer springs lead to mistimed reproduction in great tits (Parus major). Proceedings of the Royal Society of London B, 265, 1867–1870.CrossRefGoogle Scholar
Walther, G. R., Post, E., Convey, P. et al. (2002). Ecological responses to recent climate change. Nature, 416, 389–395.CrossRefGoogle ScholarPubMed
Wingfield, J. C., Hahn, T. P., Levin, R. and Honey, P. (1992). Environmental predictability and control of gonadal cycles in birds. Journal of Experimental Zoology, 261, 214–231.CrossRefGoogle Scholar
Yakovlev, I. A., Fossdal, C. G., Johnsen, O., Junttila, O. and Skrøppa, T. (2006). Analysis of gene expression during bud burst initiation in Norway spruce via ESTs from subtracted cDNA libraries. Tree Genetics and Genomes, 2, 1614–2950.CrossRefGoogle Scholar
Yanovsky, M. J. and Kay, S. A. (2002). Molecular basis of seasonal time measurement in Arabidopsis. Nature, 419, 308–312.CrossRefGoogle ScholarPubMed

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