Contemporary evolution of plant reproductive strategies under global change is revealed by stored seeds

Journal of Evolutionary Biology

Volumn 28, Issue 4, 2015, Pages 766-778

  Thomann, M ^a,b   Imbert, E ^b   Engstrand, R C ^a   Cheptou, P O ^a  

^a UNIV MONTPELLIER   (France)

^b INSTITUT DES SCIENCES DE L EVOLUTION   (France)

Author keywords

Adaptation; Climate change; Mating system; Phenology; Pollinator decline; Resurrection study

Indexed keywords

ADAPTATION; DICOTYLEDON; EVOLUTIONARY BIOLOGY; GENE FLOW; GLOBAL CHANGE; LIFE HISTORY TRAIT; PHENOLOGY; REPRODUCTIVE STRATEGY; SEED;

CENTAUREA CYANUS; MAGNOLIOPHYTA;

ADAPTATION; CENTAUREA; CLIMATE CHANGE; EVOLUTION; FLOWER; FRANCE; GENE FLOW; GENETIC DRIFT; GENETIC SELECTION; GENETICS; GERMINATION; PHYSIOLOGY; PLANT SEED; POLLINATION;

ADAPTATION, PHYSIOLOGICAL; BIOLOGICAL EVOLUTION; CENTAUREA; CLIMATE CHANGE; FLOWERS; FRANCE; GENE FLOW; GENETIC DRIFT; GERMINATION; POLLINATION; SEEDS; SELECTION, GENETIC;

EID: 84928092522     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12603     Document Type: Article

References (83)

1. Anderson, S.H., Kelly, D., Ladley, J.J., Molloy, S. & Terry, J. 2011. Cascading effects of bird functional extinction reduce pollination and plant density. Science 331: 1068-1071.
2. Anderson, J.T., Inouye, D.W., McKinney, A.M., Colautti, R.I. & Mitchell-Olds, T. 2012. Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proc. R. Soc. Lond. B Biol. Sci. 279: 3843-3852.
3. Ashman, T.L. & Majetic, C.J. 2006. Genetic constraints on floral evolution: a review and evaluation of patterns. Heredity 96: 343-352.
4. Ashman, T.L. & Morgan, M.T. 2004. Explaining phenotypic selection on plant attractive characters: male function, gender balance or ecological context? Proc. R. Soc. Lond. B Biol. Sci. 271: 553-559.
5. Barrett, R.D.H. & Hendry, A.P. 2012. Evolutionary rescue under environmental change? In: Behavioural Responses to a Changing World: Mechanisms and Consequences. (U. Candolin & B.B.M. Wong, eds), pp. 216-233. Oxford University Press, Oxford, UK.
6. Bellanger, S. (2011) Etude de la biologie d'une messicole en régression: le bleuet (Centaurea cyanus L.). In: Inra Agrosup Dijon. pp. Université de Bourgogne.
7. Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemuller, R., Edwards, M., Peeters, T. et al. 2006. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313: 351-354.
8. Bischoff, A. & Muller-Scharer, H. 2010. Testing population differentiation in plant species - how important are environmental maternal effects. Oikos 119: 445-454.
9. Bodbyl Roels, S.A. & Kelly, J.K. 2011. Rapid evolution caused by pollinator loss in Mimulus guttatus. Evolution 65: 2541-2552.
10. Brookfield, J.F.Y. 1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Mol. Ecol. 5: 453-455.
11. Brys, R. & Jacquemyn, H. 2012. Effects of human-mediated pollinator impoverishment on floral traits and mating patterns in a short-lived herb: an experimental approach. Funct. Ecol. 26: 189-197.
12. Bustos-Segura, C., Fornoni, J. & Nunez-Farfan, J. 2014. Evolutionary changes in plant tolerance against herbivory through a resurrection experiment. J. Evol. Biol. 27: 488-496.
13. Calinger, K.M., Queenborough, S. & Curtis, P.S. 2013. Herbarium specimens reveal the footprint of climate change on flowering trends across north-central North America. Ecol. Lett. 16: 1037-1044.
14. Celedon-Neghme, C., Gonzales, W.L. & Gianoli, E. 2007. Cost and benefits of attractive floral traits in the annual species Madia sativa (Asteraceae). Evol. Ecol. 21: 247-257.
15. Chapuis, M.P. & Estoup, A. 2007. Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24: 621-631.
16. Charmantier, A., McCleery, R.H., Cole, L.R., Perrins, C., Kruuk, L.E.B. & Sheldon, B.C. 2008. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320: 800-803.
17. Cheptou, P.O. & Avendano, L.G. 2006. Pollination processes and the Allee effect in highly fragmented populations: consequences for the mating system in urban environments. New Phyt. 172: 774-783.
18. Cheptou, P.O., Carrue, O., Rouifed, S. & Cantarel, A. 2008. Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta. Proc. Natl. Acad. Sci. USA 105: 3796-3799.
19. Cleland, E.E., Chuine, I., Menzel, A., Mooney, H.A. & Schwartz, M.D. 2007. Shifting plant phenology in response to global change. Trends Ecol. Evol. 22: 357-365.
20. Conner, J.K. 2001. How strong is natural selection? Trends Ecol. Evol. 16: 215-217.
21. Darimont, C.T., Carlson, S.M., Kinnison, M.T., Paquet, P.C., Reimchen, T.E. & Wilmers, C.C. 2009. Human predators outpace other agents of trait change in the wild. Proc. Natl. Acad. Sci. USA 106: 952-954.
22. Darwin, C. 1859. On the Origin of Species by Means of Natural Selection. John Murray, London.
23. De Jong, T.J. 2012. Pollination crisis, plant sex systems, and predicting evolutionary trends in attractiveness. In: Evolution of Plant-Pollinator Relationships, (S. Patiny, ed.), pp. 28-43 University Press of Cambridge, Cambridge.
24. Doyle, J.J. & Doyle, J.L. 1987. A rapid DNA isolation procedure from small quantities of fresh leaf tissues. Phytochem. Bull. 19: 11-15.
25. Eckert, C.G., Kalisz, S., Geber, M.A., Sargent, R., Elle, E., Cheptou, P.O. et al. 2010. Plant mating systems in a changing world. Trends Ecol. Evol. 25: 35-43.
26. ST - How wrong have we been? Mol. Ecol. 20: 4830-4839.
27. Endler, J.A. 1986. Natural Selection in the Wild. Princeton University Press, Princeton, NJ.
28. Falconer, D.S. 1981. Introduction to Quantitative Genetics. Longman Inc., New York.
29. Franks, S.J. & Hoffmann, A.A. 2012. Genetics of climate change adaptation. Ann. Rev. Genet. 46: 185-208.
30. 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.
31. Franks, S.J., Avise, J.C., Bradshaw, W.E., Conner, J.K., Etterson, J.R., Mazer, S.J. et al. 2008. The Resurrection initiative: storing ancestral genotypes to capture evolution in action. Bioscience 58: 870-873.
32. Gienapp, P., Teplitsky, C., Alho, J.S., Mills, J.A. & Merilä, J. 2008. Climate change and evolution: disentangling environmental and genetic responses. Mol. Ecol. 17: 167-178.
33. Gingerich, P.D. 2009. Rates of evolution. Annu. Rev. Ecol. Evol. Syst. 40: 657-675.
34. Gomez, J.M., Abdelaziz, M., Lorite, J., Munoz-Pajares, A.J. & Perfectti, F. 2010. Changes in pollinator fauna cause spatial variation in pollen limitation. J. Ecol. 98: 1243-1252.
35. Gonsamo, A., Chen, J.M. & Wu, C.Y. 2013. Citizen Science: linking the recent rapid advances of plant flowering in Canada with climate variability. Sci. Rep. 3: 1-5.
36. Haig, D. & Westoby, M. 1988. On limits to seed production. Am. Nat. 131: 757-759.
37. Hansen, M.M., Olivieri, I., Waller, D.M., Nielsen, E.E. & Ge, M.W.G. 2012. Monitoring adaptive genetic responses to environmental change. Mol. Ecol. 21: 1311-1329.
38. Harder, L.D. & Johnson, S.D. 2009. Darwin's beautiful contrivances: evolutionary and functional evidence for floral adaptation. New Phyt. 183: 530-545.
39. Hegland, S.J., Nielsen, A., Lazaro, A., Bjerknes, A.L. & Totland, O. 2009. How does climate warming affect plant-pollinator interactions? Ecol. Lett. 12: 184-195.
40. Heidsieck, H. & Allier, F. 2012. Propositions pour une prise en compte des insects pollinisateurs dans les politiques agricoles nationales et européennes. Cahier technique ITSAP - Institut de l'abeille. See http://www.itsap.asso.fr/downloads/publications/cahier_technique_verdissement_bd.pdf.
41. Hendry, A.P. 2002. QST> = ≠< FST? Trends Ecol. Evol. 17: 502.
42. Hendry, A.P., Farrugia, T.J. & Kinnison, M.T. 2008. Human influences on rates of phenotypic change in wild animal populations. Mol. Ecol. 17: 20-29.
43. Hoekstra, H.E., Hoekstra, J.M., Berrigan, D., Vignieri, S.N., Hoang, A., Hill, C.E. et al. 2001. Strength and tempo of directional selection in the wild. Proc. Natl. Acad. Sci. USA 98: 9157-9160.
44. Holzmann, C. 2012. Hivernage et pertes de colonies chez les apiculteurs professionnels français. Cahier technique ITSAP - Institut de l'abeille. See http://www.itsap.asso.fr/downloads/publications/ cahier_technique_enquete_pertes_bd.pdf.
45. Houle, D. 1992. Comparing evolvability and variability of quantitative traits. Genetics 130: 195-204.
46. Kingsolver, J.G., Hoekstra, H.E., Hoekstra, J.M., Berrigan, D., Vignieri, S.N., Hill, C.E. et al. 2001. The strength of phenotypic selection in natural populations. Am. Nat. 157: 245-261.
47. Koskinen, M.T., Haugen, T.O. & Primmer, C.R. 2002. Contemporary fisherian life-history evolution in small salmonid populations. Nature 419: 826-830.
48. Lafuma, L. & Maurice, S. 2007. Increase in mate availability without loss of self-incompatibility in the invasive species Senecio inaequidens (Asteraceae). Oikos 116: 201-208.
49. Le Corre, V., Bellanger, S., Guillemin, J.-P. & Darmency, H. 2014. Genetic diversity of the declining arable plant Centaurea cyanus: population fragmentation within an agricultural landscape is not associated with enhanced spatial genetic structure. Weed Res. 54: 436-444.
50. Lloyd, D.G. 1979. Some reproductive factors affecting the selection of self-fertilization in plants. Am. Nat. 113: 67-79.
51. Lloyd, D.G. 1992. Self-fertilization and cross-fertilization in plants. 2. The selection of self-fertilization. Int. J. Plant Sci. 153: 370-380.
52. Medel, R., Botto-Mahan, C. & Kalin-Arroyo, M. 2003. Pollinator-mediated selection on the nectar guide phenotype in the Andean monkey flower, Mimulus luteus. Ecology 84: 1721-1732.
53. Menzel, A., Sparks, T.H., Estrella, N., Koch, E., Aasa, A., Ahas, R. et al. 2006. European phenological response to climate change matches the warming pattern. Glob. Change Biol. 12: 1969-1976.
54. Merilä, J. & Hendry, A.P. 2014. Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol. Appl. 7: 1-14.
55. Merilä, J. & Sheldon, B.C. 1999. Genetic architecture of fitness and nonfitness traits: empirical patterns and development of ideas. Heredity 83: 103-109.
56. Mojica, J.P. & Kelly, J.K. 2010. Viability selection prior to trait expression is an essential component of natural selection. Proc. R. Soc. Lond. B Biol. Sci. 277: 2945-2950.
57. Ohashi, K. & Yahara, T. 1998. Effects of variation in flower number on pollinator visits in Cirsium purpuratum (Asteraceae). Am. J. Bot. 85: 219-224.
58. Parmesan, C. & Yohe, G. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37-42.
59. Pauw, A. & Hawkins, J.A. 2011. Reconstruction of historical pollination rates reveals linked declines of pollinators and plants. Oikos 120: 344-349.
60. Peakall, R. & Smouse, P.E. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6: 288-295.
61. Pinheiro, J., Bates, D., Debroy, S., Sarkar, D.and the R Development Core Team. 2012. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-103.
62. Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O. & Kunin, W.E. 2010. Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25: 345-353.
63. R Development Core Team (2012) R: A language and environment for statistical. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, Available at: http://www.R-project.org/.
64. Rasmont, P. & Mersch, P. 1988. First estimation of faunistic drift by bumblebees of Belgium (Hymenoptera, Apidae). Ann. Soc. R. Zool. Belg. 118: 141-147.
65. Rasmont, P., Pauly, A., Terzo, M., Patiny, S., Michez, D., Iserbyt, S. et al. 2005. The Survey of Wild Bees (Hymenoptera, Apoidea) in Belgium and France. FAO, Rome.
66. Renoult, J.P., Thomann, M., Schaefer, H.M. & Cheptou, P.O. 2013. Selection on quantitative colour variation in Centaurea cyanus: the role of the pollinator's visual system. J. Evol. Biol. 26: 2415-2427.
67. Reznick, D.N. & Ghalambor, C.K. 2001. The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112: 183-198.
68. Rhone, B., Vitalis, R., Goldringer, I. & Bonnin, I. 2010. Evolution of flowering time in experimental wheat populations: a comprehensive approach to detect genetic signatures of natural selection. Evolution 64: 2110-2125.
69. Roach, D.A. & Wulff, R.D. 1987. Maternal effects in plants. Annu. Rev. Ecol. Evol. Syst. 18: 209-235.
70. Root, T.L., Price, J.T., Hall, K.R., Schneider, S.H., Rosenzweig, C. & Pounds, J.A. 2003. Fingerprints of global warming on wild animals and plants. Nature 421: 57-60.
71. Schemske, D.W. & Lande, R. 1985. The evolution of self-fertilization and inbreeding depression in plants. 2 Empirical observations. Evolution 39: 41-52.
72. Spitze, K. 1993. Population structure in Daphnia obtusa - quantitative genetic and allozymic variation. Genetics 135: 367-374.
73. Steffan-Dewenter, I. & Tscharntke, T. 1999. Effects of habitat isolation on pollinator communities and seed set. Oecologia 121: 432-440.
74. Sultan, S.E., Horgan-Kobelski, T., Nichols, L.M., Riggs, C.E. & Waples, R.K. 2013. A resurrection study reveals rapid adaptive evolution within populations of an invasive plant. Evol. Appl. 6: 266-278.
75. Thomann, M., Imbert, E., Devaux, C. & Cheptou, P.O. 2013. Flowering plants under global pollinator decline. Trends Plant Sci. 18: 353-359.
76. Thompson, J., Charpentier, A., Bouguet, G., Charmasson, F., Roset, S., Buatois, B. et al. 2013. Evolution of a genetic polymorphism with climate change in a Mediterranean landscape. Proc. Natl. Acad. Sci. USA 110: 2893-2897.
77. Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M. & Shipley, P. 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4: 535-538.
78. Venables, W.N. & Ripley, B.D. 2002. Modern Applied Statistics with S, 4th edn. Springer, New York. ISBN 0-387-95457-0.
79. Vigouroux, Y., Mariac, C., De Mita, S., Pham, J.L., Gerard, B., Kapran, I. et al. 2011. Selection for earlier flowering crop associated with climatic variations in the Sahel. PLoS One 6: e19563.
80. Wang, J.L. & Whitlock, M.C. 2003. Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163: 429-446.
81. Weigensberg, I. & Roff, D.A. 1996. Natural heritabilities: Can they be reliably estimated in the laboratory? Evolution 50: 2149-2157.
82. Whitlock, M.C. 2008. Evolutionary inference from Q(ST). Mol. Ecol. 17: 1885-1896.
83. Young, H.J. & Stanton, M.L. 1990. Influences of floral variation on pollen removal and seed production in wild radish. Ecology 71: 536-547.