Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1743, 2012, Pages 3843-3852

  Anderson, Jill T ^a,b,d   Inouye, David W ^b,c   McKinney, Amy M ^b,c   Colautti, Robert I ^a   Mitchell Olds, Tom ^a  

^a DUKE UNIVERSITY   (United States)

^b ROCKY MOUNTAIN BIOLOGICAL LABORATORY   (United States)

^c Bldg 142   (United States)

^d UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Adaptive evolution; Boechera stricta; Flowering phenology; Natural selection; Response to selection; Rocky mountain biological laboratory

Indexed keywords

ADAPTATION; ANTHROPOGENIC EFFECT; CLIMATE CHANGE; DICOTYLEDON; FIELD SURVEY; FLOWERING; LIFE HISTORY TRAIT; NATURAL SELECTION; PHENOLOGY; PHENOTYPIC PLASTICITY; SNOWMELT;

ROCKY MOUNTAINS; UNITED STATES;

EID: 84864925044     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.1051     Document Type: Article

References (48)

1. Inouye, D. W. 2008 Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89, 353-362. (doi:10.1890/06-2128.1)
2. Thomson, J. D. 2010 Flowering phenology, fruiting success, and progressive deterioration of pollination in an early-flowering geophyte. Phil. Trans. R. Soc. B 365, 3187-3199. (doi:10.1098/rstb.2010.0115)
3. Pilson, D. 2000 Herbivory and natural selection on flowering phenology in wild sunflower, Helianthus annuus. Oecologia 122, 72-82. (doi:10.1007/PL00008838)
4. Anderson, J. T., Lee, C. R. & Mitchell-Olds, T. 2011 Life-history QTLs and natural selection on flowering time in Boechera stricta, a perennial relative of Arabidopsis. Evolution 65, 771-787. (doi:10.1111/j.1558-5646.2010.01175.x)
5. Mitchell-Olds, T. 1996 Genetic constraints on life-history evolution: quantitative-trait loci influencing growth and flowering in Arabidopsis thaliana. Evolution 50, 140-145. (doi:10.2307/2410788)
6. Franke, D., Ellis, A., Dharjwa, M., Freshwater, M., Fujikawa, M., Padron, A. & Weis, A. 2006 A steep cline in flowering time for Brassica rapa in Southern California: Population-level variation in the field and the greenhouse. Int. J. Plant Sci. 167, 83-92. (doi:10.1086/497648)
7. O'Neil, P. 1999 Natural selection on genetically correlated phenological characters in Lythrum salicaria L. (Lythraceae). Evolution 51, 267-274. (doi:10.2307/2410980)
8. Biere, A. & Antonovics, J. 1996 Sex-specific costs of resistance to the fungal pathogen Ustilago violacea (Microbotryum violaceum) in Silene alba. Evolution 50, 1098-1110. (doi:10.2307/2410650)
9. Munguía-Rosas, M., Ollerton, J., Parra-Tabla, V. & De-Nova, J. 2011 Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured. Ecol. Lett. 14, 511-521. (doi:10.1111/j.1461-0248.2011.01601.x)
10. Ehrlén, J. & Münzbergova ́, Z. 2009 Timing of flowering: Opposed selection on different fitness components and trait covariation. Am. Nat. 173, 819-830. (doi:10.1086/598492)
11. Franks, S. J., Sim, S. & Weis, A. E. 2007 Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proc. Natl Acad. Sci. USA 104, 1278-1282. (doi:10.1073/pnas.0608379104)
12. Parmesan, C. & Yohe, G. 2003 A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37-42. (doi:10.1038/nature01286)
13. 2. New Phytol. 176, 243-255. (doi:10.1111/j.1469-8137.2007.02196.x)
14. Beaubien, E. & Hamann, A. 2011 Spring flowering response to climate change between 1936 and 2006 in Alberta, Canada. Bioscience 61, 514-524. (doi:10.1525/bio.2011.61.7.6)
15. Parmesan, C. 2006 Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Systematics 37, 637-669. (doi:10.1146/annurev.ecolsys.37.091305.110100)
16. Angert, A., Crozier, L., Leslie, R., Gilman, S., Tewksbury, J. & Chunco, A. 2011 Do species' traits predict recent shifts at expanding range edges? Ecol. Lett. 15, 677-689. (doi:10.1111/j.1461-0248.2011.01620.x)
17. Gienapp, P., Teplitsky, C., Alho, J., Mills, J. & Merila, J. 2008 Climate change and evolution: disentangling environmental and genetic responses. Mol. Ecol. 17, 167-178. (doi:10.1111/j.1365-294X.2007.03413.x)
18. Réale, D., McAdam, A. G., Boutin, S. & Berteaux, D. 2003 Genetic and plastic responses of a northern mammal to climate change. Proc. R. Soc. Lond. B 270, 591-596. (doi:10.1098/rspb.2002.2224)
19. Teplitsky, C., Mills, J., Alho, J., Yarrall, J. & Merila, J. 2008 Disentangling environmental and genetic responses in a wild bird population. Proc. Natl Acad. Sci. USA 105, 13492-13496. (doi:10.1073/pnas.0800999105)
20. Hoffmann, A. & Sgro, C. 2011 Climate change and evolutionary adaptation. Nature 470, 479-485. (doi:10.1038/nature09670)
21. Bradshaw, W. E. & Holzapfel, C. 2001 Genetic shift in photoperiodic response correlated with global warming. Proc. Natl Acad. Sci. USA 98, 14509-14511. (doi:10.1073/pnas.241391498)
22. Etterson, J. R. & Shaw, R. G. 2001 Constraint to adaptive evolution in response to global warming. Science 294, 151-154. (doi:10.1126/science.1063656)
23. Lande, R. & Shannon, S. 1996 The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50, 434-437. (doi:10.2307/2410812)
24. Song, B. H., Clauss, M., Pepper, A. & Mitchell-Olds, T. 2006 Geographic patterns of microsatellite variation in Boechera stricta, a close relative of Arabidopsis. Mol. Ecol. 15, 357-369. (doi:10.1111/j.1365-294X.2005.02817.x)
25. IPCC. 2007 Climate change 2007: The physical science basis. Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. New York, NY: Cambridge University Press.
26. Lenoir, J., Gégout, J., Marquet, P., de Ruffray, P. & Brisse, H. 2008 A significant upward shift in plant species optimum evolution during the 20th century. Science 320, 1768-1771. (doi:10.1126/science.1156831)
27. Knowles, N., Dettinger, M.D. & Cayan, D. R. 2006 Trends in snowfall versus rainfall in the Western United States. J. Clim. 19, 4545-4559. (doi:10.1175/JCLI3850.1)
28. Lambert, A. M., Miller-Rushing, A. J. & Inouye, D. W. 2010 Changes in snowmelt date and summer precipitation affect the flowering phenology of Erythronium grandiflorum (glacier lily; Liliaceae). Am. J. Bot. 97, 1431-1437. (doi:10.3732/ajb.1000095)
29. Sheffield, J. & Wood, E. 2008 Projected changes in drought occurrence under future global warming from multi-model, multi-scenario, IPCC AR4 simulations. Clim. Dynam. 31, 79-105. (doi:10.1007/s00382-007-0340-z)
30. Miller-Rushing, A. J., Inouye, D. W. & Primack, R. B. 2008 How well do first flowering dates measure plant responses to climate change? The effects of population size and sample frequency. J. Ecol. 96, 1289-1296. (doi:10.1111/j.1365-2745.2008.01436.x)
31. Hendry, A. P. & Kinnison, M. T. 1999 The pace of modern life: Measuring rates of contemporary microevolution. Evolution 53, 1637-1653. (doi:10.2307/2640428)
32. Schranz, M. E., Windsor, A. J., Song, B. H., Lawton-Rauh, A. & Mitchell-Olds, T. 2007 Comparative genetic mapping in Boechera stricta, a close relative of Arabidopsis. Plant Physiol. 144, 286-298. (doi:10.1104/pp.107.096685)
33. Anderson, J. T., Lee, C. R., Rushworth, C., Colautti, R. & Mitchell-Olds, T. 2012 Genetic tradeoffs and conditional neutrality contribute to local adaptation. Mol. Ecol. (doi:10.1111/j.1365-294X.2012.05522.x)
34. Mitchell-Olds, T. & Shaw, R. G. 1987 Regression analysis of natural selection: statistical inference and biological interpretation. Evolution 41, 1149-1161. (doi:10.2307/2409084)
35. Stinchcombe, J. R., Agrawal, A. F., Hohenlohe, P. A., Arnold, S. J. & Blows, M. W. 2008 Estimating nonlinear selection gradients using quadratic regression coefficients: double or nothing? Evolution 62, 2435-2440. (doi:10.1111/j.1558-646.2008.00449.x)
36. Morrissey, M. B., Kruuk, L. E. B. & Wilson, A. J. 2010 The danger of applying the breeder's equation in observational studies of natural populations. J. Evol. Biol. 23, 2277-2288. (doi:10.1111/j.1420-9101.2010.02084.x)
37. Stinchcombe, J. R. & Rausher, M. D. 2001 Diffuse selection on resistance to deer herbivory in the Ivyleaf Morning Glory, Ipomoea hederacea. Am. Nat. 158, 376-388. (doi:10.1086/321990)
38. Long, J. S. & Ervin, L. H. 2000 Using heteroscedasticity consistent standard errors in the linear regression model. Am. Statist. 54, 217-224.
39. Jonzén, N. et al. 2006 Rapid advance of spring arrival dates in long-distance migratory birds. Science 312, 1959-1961. (doi:10.1126/science.1126119)
40. Walther, G., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T., Fromentin, J., Hoegh-Guldberg, O. & Bairlein, F. 2002 Ecological responses to recent climate change. Nature 416, 389-395. (doi:10.1038/416389a)
41. Miller-Rushing, A. J. & Inouye, D. W. 2009 Variation in the impact of climate change on flowering phenology and abundance: an examination of two pairs of closely related wildflower species. Am. J. Bot. 96, 1821-1829. (doi:10.3732/ajb.0800411)
42. Inouye, D. W., Saavedra, F. & Lee-Yang, W. 2003 Environmental influences on the phenology and abundance of flowering by Androsace septentrionalis (Primulaceae). Am. J. Bot. 90, 905-910. (doi:10.3732/ajb.90.6.905)
43. Fitter, A. H. & Fitter, R. S. R. 2002 Rapid changes in flowering time in British plants. Science 296, 1689-1691. (doi:10.1126/science.1071617)
44. Nussey, D. H., Postma, E., Gienapp, P. & Visser, M. E. 2005 Selection on heritable phenotypic plasticity in a wild bird population. Science 310, 304-306. (doi:10.1126/science.1117004)
45. Geber, M. & Griffen, L. R. 2003 Inheritance and natural selection on functional traits. Int. J. Plant Sci. 164, S21-S42. (doi:10.1086/368233)
46. Hansen, J., Sato, M., Ruedy, R., Lo, K., Lea, D. & Medina-Elizade, M. 2006 Global temperature change. Proc. Natl Acad. Sci. USA 103, 14288-14293. (doi:10.1073/pnas.0606291103)
47. Forrest, J. & Miller-Rushing, A. J. 2010 Toward a synthetic understanding of the role of phenology in ecology and evolution. Phil. Trans. R. Soc. B 365, 3101-3112. (doi:10.1098/rstb.2010.0145)
48. Wilczek, A. M., Burghardt, L. T., Cobb, A. R., Cooper, M. D., Welch, S. M. & Schmitt, J. 2010 Genetic and physiological bases for phenological response to current and predicted climates. Phil. Trans. R. Soc. B 365, 3129-3147. (doi:10.1098/rstb.2010.0128)