Phenotypic selection favors missing trait combinations in coexisting annual plants

American Naturalist

Volumn 182, Issue 2, 2013, Pages 191-207

  Kimball, Sarah ^a   Gremer, Jennifer R ^b   Huxman, Travis E ^a   Lawrence Venable, D ^b   Angert, Amy L ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of Arizona   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Phenotypic selection analysis; Relative growth rate; Sonoran Desert; Trade offs; Water use efficiency; Winter annual plants

Indexed keywords

WATER;

ANNUAL PLANT; ASSEMBLY RULE; BIODIVERSITY; GROWTH RATE; LIFE HISTORY TRAIT; NATURAL SELECTION; PHENOTYPIC PLASTICITY; PLANT COMMUNITY; TRADE-OFF;

ANGIOSPERM; ARTICLE; DESERT CLIMATE; ECOSYSTEM; GENETIC SELECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHENOTYPE; PHYSIOLOGY;

ANGIOSPERMS; DESERT CLIMATE; ECOSYSTEM; PHENOTYPE; SELECTION, GENETIC; WATER;

SONORAN DESERT;

EID: 84880091980     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/671058     Document Type: Article

References (91)

1. Abrams, P. A. 1990. Ecological vs. evolutionary consequences of competition. Oikos 57:147-151.
2. Ackerly, D. D., S. A. Dudley, S. E. Sultan, J. Schmitt, J. S. Coleman, C. R. Linder, D. R. Sandquist, et al. 2000. The evolution of plant ecophysiological traits: recent advances and future directions. BioScience 50:979-995.
3. Agrawal, A. A., J. K. Conner, and S. Rasmann. 2010. Tradeoffs and adaptive negative correlations in evolutionary ecology. Pages 243-268 in M. A. Bell, W. F. Eanes, D. J. Futuyma, and J. S. Levinton, eds. Evolution after Darwin: the first 150 years. Sinauer, Sunderland, MA.
4. Agrawal, A. A., A. C. Erwin, and S. C. Cook. 2008. Natural selection on and predicted responses of ecophysiological traits of swamp milkweed (Asclepias incarnata). Journal of Ecology 96:536-542.
5. Aicher, R. J., L. Larios, and K. N. Suding. 2011. Seed supply, recruitment, and assembly: quantifying relative seed and establishment limitation in a plant community context. American Naturalist 178:464-477.
6. Angert, A. L., J. L. Horst, T. E. Huxman, and D. L. Venable. 2010. Phenotypic plasticity and precipitation response in Sonoran Desert winter annuals. American Journal of Botany 97:405-411.
7. Angert, A. L., T. E. Huxman, G. A. Barron-Gafford, K. L. Gerst, and D. L. Venable. 2007. Linking growth strategies to long-term population dynamics in a guild of desert annuals. Journal of Ecology 95:321-331.
8. Angert, A. L., T. E. Huxman, P. Chesson, and D. L. Venable. 2009. Functional tradeoffs determine species coexistence via the storage effect. Proceedings of the National Academy of Sciences of the USA 106:11641-11645.
9. Antonovics, J., and P. H. van Tienderen. 1991. Ontoecogenophyloconstraints? the chaos of constraint terminology. Trends in Ecology and Evolution 6:166-168.
10. Arnold, S. J. 1992. Constraints on phenotypic evolution. American Naturalist 140(suppl.):S85-S107.
11. Arnold, S. J., and M. J. Wade. 1984. On the measurement of natural and sexual selection: applications. Evolution 38:720-734.
12. Arntz, A. M., and L. F. Delph. 2001. Pattern and process: evidence for the evolution of photosynthetic traits in natural populations. Oecologia (Berlin) 127:455-467.
13. Aspi, J., A. Jakalaniemi, J. Tuomi, and P. Siikamaki. 2003. Multilevel phenotypic selection on morphological characters in a metapopulation of Silene tatarica. Evolution 57:509-517.
14. Atkin, O. K., B. Botman, and H. Lambers. 1996. The causes of inherently slow growth in alpine plants: an analysis based on the underlying carbon economies of alpine and lowland Poa species. Functional Ecology 10:698-707.
15. Belyea, L. R., and J. Lancaster. 1999. Assembly rules within a contingent ecology. Oikos 86:402-416.
16. Bonsall, M. B., and M. Mangel. 2004. Life-history trade-offs and ecological dynamics in the evolution of longevity. Proceedings of the Royal Society B: Biological Sciences 271:1143-1150.
17. Campbell, D. R., N. M. Waser, and E. J. Meléndez-Ackerman. 1997. Analyzing pollinator-mediated selection in a plant hybrid zone: hummingbird visitation patterns on three spatial scales. American Naturalist 149:295-315.
18. Caruso, C. M., H. Maherali, and M. Sherrard. 2006. Plasticity of physiology in Lobelia: testing for adaptation and constraint. Evolution 60:980-990.
19. Chesson, P. 2000. Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31:343-366.
20. Coleman, J. S., K. D. M. McConnaughay, and D. D. Ackerly. 1994. Interpreting phenotypic variation in plants. Trends in Ecology and Evolution 9:187-191.
21. Culley, T. M., A. K. Dunbar-Wallis, A. K. Sakai, S. G. Weller, M. Mishio, D. R. Campbell, and M. Herzenach. 2006. Genetic variation of ecophysiological traits in two gynodioecious species of Schiedea (Caryophyllaceae). New Phytologist 169:589-601.
22. Donovan, L. A., F. Ludwig, D. M. Rosenthal, L. H. Rieseberg, and S. A. Dudley. 2009. Phenotypic selection on leaf ecophysiological traits in Helianthus. New Phytologist 183:868-879.
23. Dudley, L. S., A. A. Hove, and S. J. Mazer. 2012. Physiological performance and mating system in Clarkia (Onagraceae): does phenotypic selection predict divergence between sister species? American Journal of Botany 99:488-507.
24. Dudley, S. A. 1996. Differing selection on plant physiological traits in response to environmental water availability: a test of adaptive hypotheses. Evolution 50:92-102.
25. Edwards, C. E., B. E. Ewers, C. R. McClung, P. Lou, and C. Weinig. 2012. Quantitative variation in water-use efficiency across water regimes and its relationship with circadian, vegetative, reproductive, and leaf gas-exchange traits. Molecular Plant 5:653-668.
26. Evans, J. R. 1989. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia (Berlin) 78:9-19.
27. Farquhar, G. D., J. R. Ehleringer, and K. T. Hubick. 1989. Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40:503-537.
28. Farris, M. A., and M. J. Lechowicz. 1990. Functional interactions among traits that determine reproductive success in a native annual plant. Ecology 71:548-557.
29. Fox, C.W., M. S. Thakar, and T. A. Mousseau. 1997. Egg size plasticity in a seed beetle: an adaptive maternal effect. American Naturalist 149:149-163.
30. Futuyma, D. J., and G. Moreno. 1988. The evolution of ecological specialization. Annual Review of Ecology and Systematics 19:207-233.
31. Geber, M. A., and T. E. Dawson. 1990. Genetic variation in and covariation between leaf gas exchange, morphology, and development in Polygonum arenastrum, an annual plant. Oecologia (Berlin) 85:153-158.
32. Geber, M. A., and T. E. Dawson. 1997. Genetic variation in stomatal and biochemical limitations to photosynthesis in the annual plant, Polygonum arenastrum. Oecologia (Berlin) 109:535-546.
33. Geber, M. A., and L. R. Griffen. 2003. Inheritance and natural selection on functional traits. International Journal of Plant Sciences 164(suppl.):S21-S42.
34. Gilbert, B., S. J. Wright, H. C. Muller-Landau, K. Kitajima, and A. Hernandez. 2006. Life history trade-offs in tropical trees and lianas. Ecology 87:1281-1288.
35. Gleeson, S. K., and D. Tilman. 1990. Allocation and the transient dynamics of succession on poor soils. Ecology 71:1144-1155.
36. Golluscio, R. A., and M. Oesterheld. 2007. Water use efficiency of twenty-five co-existing Patagonian species growing under different soil water availability. Oecologia (Berlin) 154:207-217.
37. Goyal, R. K. 2004. Sensitivity of evapotranspiration to global warming: a case study of arid zone of Rajasthan (India). Agricultural Water Management 69:1-11.
38. Gremer, J. R., S. Kimball, A. L. Angert, D. L. Venable, and T. E. Huxman. 2012. Variation in photosynthetic response to temperature in a guild of winter annual plants. Ecology 93:2693-2704.
39. Gremer, J. R., S. Kimball, K. Keck, T. E. Huxman, A. L. Angert, and D. L. Venable. Forthcoming. Water-use efficiency and relative growth rate mediate competitive interactions in Sonoran Desert winter annual plants. American Journal of Botany.
40. Grime, J. P. 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological theory. American Naturalist 111:1169-1194.
41. Grime, J. P., and R. Hunt. 1975. Relative growth rate: its range and adaptive significance in a local flora. Journal of Ecology 63:393-422.
42. Gronroos, M., and J. Heino. 2012. Species richness at the guild level: effects of species pool and local environmental conditions on stream macroinvertebrate communities. Journal of Animal Ecology 81:679-691.
43. Hamerlynck, E. P., T. E. Huxman, J. R. McAuliffe, and S. D. Smith. 2004. Carbon isotope discrimination and foliar nutrient status of Larrea tridentata (creosote bush) in contrasting Mojave Desert soils. Oecologia (Berlin) 138:210-215.
44. Heisler, I. L., and J. Damuth. 1987. A method for analyzing selection in hierarchically structured populations. American Naturalist 130: 582-602.
45. Heschel, M. S., K. Donohue, N. Hausmann, and J. Schmitt. 2002. Population differentiation and natural selection for water-use efficiency in Impatiens capensis (Balsaminaceae). International Journal of Plant Sciences 163:907-912.
46. Heschel, M. S., and C. Riginos. 2005. Mechanisms of selection for drought stress tolerance and avoidance in Impatiens capensis (Balsaminaceae). American Journal of Botany 92:37-44.
47. Hunt, R., D. R. Causton, B. Shipley, and A. P. Askew. 2002. A modern tool for classical plant growth analysis. Annals of Botany 90:485-488.
48. Huxman, T. E., G. Barron-Gafford, K. L. Gerst, A. L. Angert, A. P. Tyler, and D. L. Venable. 2008. Photosynthetic resource-use efficiency and demographic variability in desert winter annual plants. Ecology 89:1554-1563.
49. Ignace, D. D., and T. E. Huxman. 2009. Limitations to photosynthetic function across season in Larrea tridentata (creosotebush) growing on contrasting soil surfaces in the Sonoran Desert. Journal of Arid Environments 73:626-633.
50. Jia, P., T. Bayaerta, X. Q. Li, and G. Z. Du. 2011. Relationships between flowering phenology and functional traits in eastern Tibet alpine meadow. Arctic, Antarctic, and Alpine Research 43:585-592.
51. Keddy, P. A. 1992. Assembly and response rules: two goals for predictive community ecology. Journal of Vegetation Science 3:157-164.
52. Kimball, S., A. L. Angert, T. E. Huxman, and D. L. Venable. 2011. Differences in the timing of germination and reproduction relate to growth physiology and population dynamics of Sonoran Desert winter annuals. American Journal of Botany 98:1773-1781.
53. Kimball, S., J. R. Gremer, A. L. Angert, T. E. Huxman, and D. L. Venable. 2012. Fitness and physiology in a variable environment. Oecologia (Berlin) 169:319-329.
54. Kimball, S., J. R. Gremer, T. E. Huxman, D. L. Venable, and A. L. Angert. 2013. Data from: Phenotypic selection favors missing trait combinations in coexisting annual plants. American Naturalist, Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.c8c58.
55. Kingsolver, J. G., H. E. Hoekstra, J. M. Hoekstra, D. Berrigan, S. N. Vignieri, C. E. Hill, A. Hoang, P. Gibert, and P. Beerli. 2001. The strength of phenotypic selection in natural populations. American Naturalist 157:245-261.
56. Kingsolver, J. G., and D. W. Schemske. 1991. Path analysis of selection. Trends in Ecology and Evolution 6:276-280.
57. Kneitel, J. M., and J. M. Chase. 2004. Trade-offs in community ecology: linking spatial scales and species coexistence. Ecology Letters 7:69-80.
58. Lande, R., and S. J. Arnold. 1983. The measurement of selection on correlated characters. Evolution 37:1210-1226.
59. Molina-Montenegro, M. A., E. E. Cleland, S. M. Watts, and B. R. Broitman. 2012. Can a breakdown in competition-colonization tradeoffs help explain the success of exotic species in the California flora? Oikos 121:389-395.
60. Munguía-Rosas, M. A., J. Ollerton, V. Parra-Tabla, and J. A. De-Nova. 2011. Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured. Ecology Letters 14:511-521.
61. Nagel, O. W., H. Konings, and H. Lambers. 2001. Growth rate and biomass partitioning of wildtype and low-gibberellin tomato (Solanum lycopersicum) plants growing at a high and low nitrogen supply. Physiologia Plantarum 111:33-39.
62. Palmer, M. A., R. F. Ambrose, and N. L. Poff. 1997. Ecological theory and community restoration ecology. Restoration Ecology 5:291-300.
63. Pianka, E. R. 1980. Guild structure in desert lizards. Oikos 35:194-201.
64. Raddatz, R. L., and C. F. Shaykewich. 1998. Impact of warmsummers on the actual evapotranspiration from spring wheat grown on the eastern Canadian prairies. Canadian Journal of Soil Science 78: 171-179.
65. Rausher, M. D. 1992. The measurement of selection on quantitative traits: biases due to environmental covariances between traits and fitness. Evolution 46:616-626.
66. Reich, P. B., C. Buschena, M. G. Tjoelker, K. Wrage, J. Knops, D. Tilman, and J. L. Machado. 2003a. Variation in growth rate and ecophysiology among 34 grassland and savanna species under contrasting N supply: a test of functional group differences. New Phytologist 157:617-631.
67. Reich, P. B., D. S. Ellsworth, and M. B. Walters. 1998. Leaf structure (specific leaf area) modulates photosynthesis-nitrogen relations: evidence from within and across species and functional groups. Functional Ecology 12:948-958.
68. Reich, P. B., B. D. Kloeppel, D. S. Ellsworth, and M. B. Walters. 1995. Different photosynthesis-nitrogen relations in deciduous hardwood and evergreen coniferous tree species. Oecologia (Berlin) 104:24-30.
69. Reich, P. B., M. B. Walters, and D. S. Ellsworth. 1992. Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecological Monographs 62:365-392.
70. Reich, P. B., I. J. Wright, J. Cavender-Bares, J. M. Craine, J. Oleksyn, M. Westoby, and M. B. Walters. 2003b. The evolution of plant functional variation: traits, spectra, and strategies. International Journal of Plant Sciences 164(suppl.):S143-S164.
71. Ritz, M. S., and G. Kohler. 2010. Natural and sexual selection on male behaviour and morphology, and female choice in a wild field cricket population: spatial, temporal and analytical components. Evolutionary Ecology 24:985-1001.
72. Saldana, A., C. H. Lusk, W. L. Gonzales, and E. Gianoli. 2007. Natural selection on ecophysiological traits of a fern species in a temperate rainforest. Evolutionary Ecology 21:651-662.
73. Scheiner, S. M., R. J. Mitchell, and H. S. Callahan. 2000. Using path analysis to measure natural selection. Journal of Evolutionary Biology 13:423-433.
74. Schemske, D. W., and C. C. Horvitz. 1988. Plant animal interactions and fruit production in a Neotropical herb: a path analysis. Ecology 69:1128-1137.
75. Schluter, D. 1988. Estimating the form of natural selection on a quantitative trait. Evolution 42:849-861.
76. Schluter, D. 1996. Adaptive radiation along genetic lines of least resistance. Evolution 50:1766-1774.
77. Schluter, D. 2000. Ecological character displacement in adaptive radiation. American Naturalist 156(suppl.):S4-S16.
78. Shipley, B., D. Vile, and E. Garnier. 2006. From plant traits to plant communities: a statistical mechanistic approach to biodiversity. Science 314:812-814.
79. Sonnier, G., M. L. Navas, A. Fayolle, and B. Shipley. 2012.Quantifying trait selection driving community assembly: a test in herbaceous plant communities under contrasted land use regimes. Oikos 121: 1103-1111.
80. Stinchcombe, J. R., A. F. Agrawal, P. A. Hohenlohe, S. J. Arnold, and M. W. Blows. 2008. Estimating nonlinear selection gradients using quadratic regression coefficients: double or nothing? Evolution 62: 2435-2440.
81. Stinchcombe, J. R., M. T. Rutter, D. S. Burdick, P. Tiffin, M. D. Rausher, and R. Mauricio. 2002. Testing for environmentally induced bias in phenotypic estimates of natural selection: theory and practice. American Naturalist 160:511-523.
82. Suding, K. N., D. E. Goldberg, and K. M. Hartman. 2003. Relationships among species traits: separating levels of response and identifying linkages to abundance. Ecology 84:1-16.
83. Tilman, D. 1982. Resource competition and community structure. Princeton University Press, Princeton, NJ.
84. Tilman, D. 1990. Constraints and tradeoffs: toward a predictive theory of competition and succession. Oikos 58:3-15.
85. Tilman, D. 1994. Competition and biodiversity in spatially structured habitats. Ecology 75:2-16.
86. Tilman, D.1999. The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80:1455-1474.
87. Tilman, D., and D. Wedin. 1991. Plant traits and resource reduction for five grasses growing on a nitrogen gradient. Ecology 72:685-700.
88. Turnbull, L. A., M. Rees, and M. J. Crawley. 1999. Seed mass and the competition/colonization trade-off: a sowing experiment. Journal of Ecology 87:899-912.
89. Venable, D. L., and S. Kimball. Forthcoming. Population and community dynamics in variable environments: the desert annual system. In Environmental fluctuation, temporal dynamics and ecological process. Cambridge University Press, Cambridge.
90. Via, S. 1993. Adaptive phenotypic plasticity: target or by-product of selection in a variable environment. American Naturalist 142:352-365.
91. Wright, I. J., P. B. Reich, M. Westoby, D. D. Ackerly, Z. Baruch, F. Bongers, J. Cavender-Bares, et al. 2004. The worldwide leaf economics spectrum. Nature 428:821-827.