Fitness consequences of plants growing with siblings: Reconciling kin selection, niche partitioning and competitive ability

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1727, 2012, Pages 209-218

  File, Amanda L ^a   Murphy, Guillermo P ^a   Dudley, Susan A ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Fitness; Kin selection; Niche partitioning; Plant; Sibling competition

Indexed keywords

CONCEPTUAL FRAMEWORK; FITNESS; FUTURE PROSPECT; GROWTH RATE; KIN SELECTION; NICHE PARTITIONING; PLANT COMMUNITY; SIBLING; THEORETICAL STUDY;

EID: 82955169668     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.1995     Document Type: Article

References (104)

1. Casper, B. B. & Jackson, R. B. 1997 Plant competition underground. Ann. Rev. Ecol. Syst. 28, 545-570. doi:10.1146/annurev.ecolsys.28.1.545
2. Jones, H. G. 1992 Plant and microclimate: a quantitative approach to environmental plant physiology. Cambridge, UK: Cambridge University Press.
3. Novoplansky, A. 2009 Picking battles wisely: plant behaviour under competition. Plant Cell Environ. 32, 726-741. doi:10.1111/j.1365-3040.2009.01979.x
4. Bais, H. P., Weir, T. L., Perry, L. G., Gilroy, S. & Vivanco, J. M. 2006 The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 57, 233-266. doi:10.1146/ annurev.arplant.57.032905.105159
5. Grace, J. B. 1990 On the relationship between plant traits and competitive ability. In Perspectives on plant competition (eds J. B. Grace & D. Tilman), pp. 51-65. NY, USA: Academic Press.
6. Milbau, A., Reheul, D., De Cauwer, B. & Nijs, I. 2007 Factors determining plant-neighbour interactions on different spatial scales in young species-rich grassland communities. Ecol. Res. 22, 242-247. doi:10.1007/ s11284-006-0018-8
7. Wade, M. J. 1980 An experimental study of kin selection. Evolution 34, 844-855. doi:10.2307/2407991
8. Hamilton, W. D. 1964 The genetical evolution of social behavior, I & II. J. Theor. Biol. 7, 1-52. doi:10.1016/ 0022-5193(64)90038-4
9. Young, J. P. W. 1981 Sib competition can favour sex in two ways. J. Theor. Biol. 88, 755-756. doi:10.1016/ 0022-5193(81)90249-6
10. Willson, M. F., Hoppes, W. G., Goldman, D. A., Thomas, P. A., Katusic-Malmborg, P. L. & Bothwell, J. L. 1987 Sibling competition in plants: an experimental study. Am. Nat. 129, 304-311. doi:10.1086/284636
11. Tonsor, S. J. 1989 Relatedness and intraspecific competition in Plantago lanceolata. Am. Nat. 134, 897-906. doi:10.1086/285020
12. Donohue, K. 2003 The influence of neighbor relatedness on multilevel selection in the Great Lakes sea rocket. Am. Nat. 162, 77-92. doi:10.1086/375299
13. Karban, R. & Shiojiri, K. 2009 Self-recognition affects plant communication and defense. Ecol. Lett. 12, 502-506. doi:10.1111/j.1461-0248.2009.01313.x
14. Andalo, C., Goldringer, I. & Godelle, B. 2001 Inter- and intragenotypic competition under elevated carbon dioxide in Arabidopsis thaliana. Ecology 82, 157-164. doi:10. 1890/0012-9658(2001)082[0157:IAICUE]2.0.CO;2
15. Ronsheim, M. L. 1996 Evidence against a frequencydependent advantage for sexual reproduction in Allium vineale. Am. Nat. 147, 718-734. doi:10.1086/285876
16. Collins, A., Hart, E. M. & Molofsky, J. 2010 Differential response to frequency-dependent interactions: an experimental test using genotypes of an invasive grass. Oecologia 164, 959-969. doi:10.1007/s00442-010-1719-9
17. Boyden, S., Binkley, D. & Stape, J. L. 2008 Competition among Eucalyptus trees depends on genetic variation and resource supply. Ecology 89, 2850-2859. doi:10.1890/07-1733.1
18. Allard, R.W. & Adams, J. 1969 Population studies in predominantly self-pollinating species. XIII. Intergenotypic competition and population structure in barley and wheat. Am. Nat. 103, 621-645. doi:10.1086/282630
19. Ellstrand, N. C. & Antonovics, J. 1985 Experimental studies of the evolutionary significance of sexual reproduction. II. A test of the density-dependent selection hypothesis. Evolution 39, 657-666. doi:10.2307/ 2408660
20. Schmitt, J. & Antonovics, J. 1986 Experimental studies of the evolutionary significance of sexual reproduction. IV. Effect of neighbor relatedness and aphid infestation on seedling performance. Evolution 40, 830-836. doi:10.2307/2408467
21. Kelley, S. E. 1989 Experimental studies of the evolutionary significance of sexual reproduction. V. A field-test of the sib competition lottery hypothesis. Evolution 43, 1054-1065. doi:10.2307/2409585
22. Escarre, J., Houssard, C. & Thompson, J. D. 1994 An experimental study of the role of seedling density and neighbor relatedness in the persistence of Rumex acetosella in an old-field succession. Can. J. Bot. 72, 1273-1281. doi:10.1139/b94-155
23. Cheplick, G. P. & Kane, K. H. 2004 Genetic relatedness and competition in Triplasis purpurea (Poaceae): resource partitioning or kin selection? Int. J. Plant Sci. 165, 623-630. doi:10.1086/386556
24. Milla, R., Forero, D. M., Escudero, A. & Iriondo, J. M. 2009 Growing with siblings: a common ground for cooperation or for fiercer competition among plants? Proc. R. Soc. B 276, 2531-2540. doi:10.1098/rspb. 2009.0369
25. Delesalle, V. R. A. & Mazer, S. J. 2002 The neighborhood matters: effects of neighbor number and sibling (or kin) competition on floral traits in Spergularia marina (Caryophyllaceae). Evolution 56, 2406-2413. doi:10.1111/j.0014-3820.2002.tb00166.x
26. Argyres, A. Z. & Schmitt, J. 1992 Neighborhood relatedness and competitive performance in Impatiens capensis (Balsaminaceae): a test of the resource partitioning hypothesis. Am. J. Bot. 79, 181-185. doi:10. 2307/2445106
27. Burt, A. & Bell, G. 1992 Tests of sib diversification theories of outcrossing in Impatiens capensis: effects of inbreeding and neighbor relatedness on production and infestation. J. Evol. Biol. 5, 575-588. doi:10. 1046/j.1420-9101.1992.5040575.x
28. Cheplick, G. P. & Salvadori, G. M. 1991 Intraclonal and interclonal competition in the cleistogamous grass Amphibromus scabrivalvis. Am. J. Bot. 78, 1494-1502. doi:10.2307/2444974
29. Karron, J. D. & Marshall, D. L. 1993 Effects of environmental variation on fitness of singly and multiply sired progenies of Raphanus sativus (Brassicaceae). Am. J. Bot. 80, 1407-1412. doi:10.2307/2445669
30. Masclaux, F., Hammond, R. L., Meunier, J., Gouhier-Darimont, C., Keller, L. & Reymond, P. 2010 Competitive ability not kinship affects growth of Arabidopsis thaliana accessions. New Phytol. 185, 322-331. doi:10.1111/j.1469-8137.2009.03057.x
31. McCall, C., Mitchell-Olds, T. & Waller, D. M. 1989 Fitness consequences of outcrossing in Impatiens capensis-tests of the frequency-dependent and sibcompetition models. Evolution 43, 1075-1084. doi:10. 2307/2409587
32. Monzeglio, U. & Stoll, P. 2007 Effects of spatial pattern and relatedness in an experimental plant community. Evol. Ecol. 22, 723-741. doi:10.1007/s10682-007-9197-1
33. Puustinen, S., Koskela, T. & Mutikainen, P. 2004 Relatedness affects competitive performance of a parasitic plant (Cuscuta europaea) in multiple infections. J. Evol. Biol. 17, 897-903. doi:10.1111/j.1420-9101.2004. 00728.x
34. Rautiainen, P., Koivula, K. & Hyvarinen, M. 2004 The effect of within-genet and between-genet competition on sexual reproduction and vegetative spread in Potentilla anserina ssp egedii. J. Ecol. 92, 505-511. doi:10. 1111/j.0022-0477.2004.00878.x
35. Schmitt, J. & Ehrhardt, D. W. 1987 A test of the sibcompetition hypothesis for outcrossing advantage in Impatiens capensis. Evolution 41, 579-590. doi:10. 2307/2409259
36. Willis, C. G., Brock, M. T. & Weinig, C. 2010 Genetic variation in tolerance of competition and neighbour suppression in Arabidopsis thaliana. J. Evol. Biol. 23, 1412-1424. doi:10.1111/j.1420-9101.2010.02003.x
37. Biernaskie, M. 2011 Evidence for competition and cooperation among climbing plants. Proc. R. Soc. B 278, 1989-1996. doi:10.1098/rspb.2010.1771
38. Dudley, S. A. & File, A. L. 2007 Kin recognition in an annual plant. Biol. Lett. 3, 435-438. doi:10.1098/rsbl. 2007.0232
39. Murphy, G. P. & Dudley, S. A. 2009 Kin recognition: competition and cooperation in Impatiens (Balsaminaceae). Am. J. Bot. 96, 1990-1996. doi:10.3732/ajb. 0900006
40. Bhatt, M. V., Khandelwal, A. & Dudley, S. A. 2010 Kin recognition, not competitive interactions, predicts root allocation in young Cakile edentula seedling pairs. New Phytol. 189, 1135-1142. doi:10.1111/j.1469-8137.2010.03458.x
41. Biedrzycki, M., Jilany, T., Dudley, S. & Bais, H. 2010 Root exudates mediate kin recognition in plants. Commun. Integr. Biol. 3, 1-8. doi:10.4161/cib.3.1.9694
42. de Kroon, H. 2007 Ecology: how do roots interact? Science 318, 1562-1563. doi:10.1126/science.1150726
43. Lankinen, A. 2008 Root competition influences pollen competitive ability in Viola tricolor: effects of presence of a competitor beyond resource availability? J. Ecol. 96, 756-765. doi:10.1111/j.1365-2745.2008.01387.x
44. Biedrzycki, M. L., Venkatachalam, L. & Bais, H. P. 2011 The role of ABC transporters in kin recognition in Arabidopsis thaliana. Plant Signall. Behav. 6, 1154-1161. doi:10.4161/psb.6.8.15907
45. Donohue, K. 2004 Density-dependent multilevel selection in the Great Lakes sea rocket. Ecology 85, 180-191. doi:10.1890/02-0767
46. Callaway, R. M. & Mahall, B. E. 2007 Plant ecology: family roots. Nature 448, 145-147. doi:10.1038/ 448145a
47. Lande, R. & Arnold, S. J. 1983 The measurement of selection on correlated characters. Evolution 37, 1210-1226. doi:10.2307/2408842
48. Bijma, P. & Wade, M. J. 2008 The joint effects of kin, multilevel selection and indirect genetic effects on response to genetic selection. J. Evol. Biol. 21, 1175-1188. doi:10. 1111/j.1420-9101.2008.01550.x
49. West Eberhard, M. 1975 The evolution of social behavior by kin selection. Q. Rev. Biol. 50, 1-33. doi:10. 1111/j.1469-185X.1975.tb00988.x
50. Cheplick, G. P. 1992 Sibling competition in plants. J. Ecol. 80, 567-575. doi:10.2307/2260699
51. Thorpe, A. S., Aschehoug, E. T., Atwater, D. Z. & Callaway, R. M. 2011 Interactions among plants and evolution. J. Ecol. 99, 729-740. doi:10.1111/j.1365- 2745.2011.01802.x
52. Kelly, J. K. 1996 Kin selection in the annual plant Impatiens capensis. Am. Nat. 147, 899-918. doi:10.1086/ 285885
53. Platt, T. G. & Bever, J. D. 2009 Kin competition and the evolution of cooperation. Trends Ecol. Evol. 24, 370-377. doi:10.1016/j.tree.2009.02.009
54. Van Dyken, J. D. 2010 The components of kin competition. Evolution 64, 2840-2854. doi:10.1111/ j.1558-5646.2010.01033.x
55. Gardner, A. & West, S. A. 2010 Greenbeards. Evolution 64, 25-38. doi:10.1111/j.1558-5646.2009. 00842.x
56. Chesson, P. L. & Ellner, S. 1989 Invasibility and stochastic boundedness in monotonic competition models. J. Math. Biol. 27, 117-138. doi:10.1007/ BF00276099
57. Waldman, B. 1988 The ecology of kin recognition. Annu. Rev. Ecol. Syst. 19, 543-571. doi:10.1146/ annurev.es.19.110188.002551
58. Pfennig, D.W., Reeve, H. K. & Sherman, P.W. 1993 Kin recognition and cannibalism in Spadefoot Toad tadpoles. Anim. Behav. 46, 87-94. doi:10.1006/anbe.1993.1164
59. Silvertown, J. 2004 Plant coexistence and the niche. Trends Ecol. Evol. 19, 605-611. doi:10.1016/j.tree. 2004.09.003
60. Price, T. 1987 Diet variation in a population of Darwin's finches. Ecology 68, 1015-1028. doi:10.2307/1938373
61. Parrish, J. A. D. & Bazzaz, F. A. 1976 Underground niche separation in successional plants. Ecology 57, 1281-1288. doi:10.2307/1935052
62. Stegen, J. C. & Swenson, N. G. 2009 Functional trait assembly through ecological and evolutionary time. Theoret. Ecol. 2, 239-250. doi:10.1007/s12080-009-0047-3
63. Diaz, S. & Cabido, M. 1997 Plant functional types and ecosystem function in relation to global change. J. Veg. Sci. 8, 463-474.
64. Song, Y., Drossel, B. & Scheu, S. 2011 Tangled Bank dismissed too early. Oikos 120, 1601-1607. doi:10. 1111/j.1600-0706.2011.19698.x
65. Antonovics, J. & Ellstrand, N. C. 1984 Experimental studies of the evolutionary significance of sexual reproduction. I. A test of the frequency-dependent selection hypothesis. Evolution 38, 103-115. doi:10. 2307/2408550
66. Svanback, R. & Bolnick, D. I. 2007 Intraspecific competition drives increased resource use diversity within a natural population. Proc. R. Soc. B 274, 839-844. doi:10.1098/rspb.2006.0198
67. Cavender-Bares, J., Kitajima, K. & Bazzaz, F. A. 2004 Multiple trait associations in relation to habitat differentiation among 17 Floridian oak species. Ecol. Monogr. 74, 635-662. doi:10.1890/03-4007
68. Cavender-Bares, J., Ackerly, D. D., Baum, D. A. & Bazzaz, F. A. 2004 Phylogenetic overdispersion in Floridian oak communities. Am. Nat. 163, 823-843. doi:10.1086/386375
69. Hughes, A. R., Inouye, B. D., Johnson, M. T. J., Underwood, N. & Vellend, M. 2008 Ecological consequences of genetic diversity. Ecol. Lett. 11, 609-623. doi:10.1111/j.1461-0248.2008.01179.x
70. Pfennig, D. W. 2009 Disruptive selection in natural populations: the roles of ecological specialization and resource competition. Am. Nat. 174, 268-281. doi:10.1086/600090
71. Kerkhoff, A. J. 2004 Expectation, explanation and masting. Evol. Ecol. Res. 6, 1003-1020.
72. Xiao, Z., Gao, X., Steele, M. A. & Zhang, Z. 2009 Frequency-dependent selection by tree squirrels: adaptive escape of non-dormant white oaks. Behav. Ecol. 21, 169-175. doi:10.1093/beheco/arp169
73. Chaboudez, P. B. 1995 Frequency-dependent selection in a wild plant-pathogen system. Oecologia 102, 490-493. doi:10.1007/BF00341361
74. Bever, J. D. et al. 2010 Rooting theories of plant community ecology in microbial interactions. Trends Ecol. Evol. 25, 468-478. doi:10.1016/j.tree.2010. 05.004
75. Reynolds, H. L., Packer, A., Bever, J. D. & Clay, K. 2003 Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84, 2281-2291. doi:10.1890/02- 0298
76. Ronsheim, M. L. & Anderson, S. E. 2001 Populationlevel specificity in the plant-mycorrhizae association alters intraspecific interactions among neighboring plants. Oecologia 128, 77-84. doi:10.1007/s00442 0000625
77. Bever, J. D., Westover, K. M. & Antonovics, J. 1997 Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J. Ecol. 85, 561-573. doi:10.2307/2960528
78. Via, S. & Lande, R. 1985 Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39, 505-522. doi:10.2307/2408649
79. Taper, M. & Case, T. 1985 Quantitative genetic models for the coevolution of character displacement. Ecology 66, 355-371. doi:10.2307/1940385
80. Scheiner, S. M. 1993 Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst. 24, 35-68. doi:10.1146/annurev.es.24.110193.000343
81. Krakauer, A. H. 2005 Kin selection and cooperative courtship in wild turkeys. Nature 434, 69-72. doi:10. 1038/nature03325
82. Heisler, I. L. & Damuth, J. 1987 A method for analyzing selection in hierarchically structured populations. Am. Nat. 130, 582-602. doi:10.1086/284732
83. Goodnight, C. J. 2005 Multilevel selection: the evolution of cooperation in non-kin groups. Popul. Ecol. 47, 3-12. doi:10.1007/s10144-005-0207-2
84. Abrams, P. A., Rueffler, C. & Kim, G. 2008 Determinants of the strength of disruptive and/or divergent selection arising from resource competition. Evolution 62, 1571-1586. doi:10.1111/j.1558-5646.2008.00385.x
85. Pfennig, D. W. & Pfennig, K. S. 2010 Character displacement and the origins of diversity. Am. Nat. 176, S26-S44. doi:10.1086/657056
86. Ackermann, M. & Doebeli, M. 2004 Evolution of niche width and adaptive diversification. Evolution 58, 2599-2612. doi:10.1554/04-244
87. Rueffler, C., Van Dooren, T., Leimar, O. & Abrams, P. 2006 Disruptive selection and then what? Trends Ecol. Evol. 21, 238-245. doi:10.1016/j.tree.2006.03.003
88. Boege, K. 2010 Induced responses to competition and herbivory: natural selection on multi-trait phenotypic plasticity. Ecology 91, 2628-2637. doi:10.1890/09- 0543.1
89. Stevens, L., Goodnight, C. J. & Kalisz, S. 1995 Multilevel selection in natural populations of Impatiens capensis. Am. Nat. 145, 513-526. doi:10.1086/285753
90. Weinig, C., Johnston, J. A., Willis, C. G. & Maloof, J. N. 2007 Antagonistic multilevel selection on size and architecture in variable density settings. Evolution 61, 58-67. doi:10.1111/j.1558-5646.2007.00005.x
91. Aspi, J., Jakalaniemi, A., Tuomi, J. & Siikamaki, P. 2003 Multilevel phenotypic selection on morphological characters in a metapopulation of Silene tatarica. Evolution 57, 509-517. doi:10.1554/0014-3820(2003)057 [0509:MPSOMC]2.0.CO;2
92. Goodnight, C. J. 1985 The influence of environmental variation on group and individual selection in a cress. Evolution 39, 545-558. doi:10.2307/2408652
93. Dayan, T. & Simberloff, D. 2005 Ecological and community-wide character displacement: the next generation. Ecol. Lett. 8, 875-894. doi:10.1111/j. 1461-0248.2005.00791.x
94. Nobel, P. S. & Linton, M. L. 1997 Frequencies, microclimate and root properties for three codominate perennials in the northwestern Sonoran desert on North- versus South-facing slopes. Ann. Bot. 80, 731-739. doi:10. 1006/anbo.1997.0508
95. von Felten, S., Hector, A., Buchmann, N., Niklaus, P., Schmid, B. & Scherer-Lorenzen, M. 2009 Belowground nitrogen partitioning in experimental grassland communities of varying species richness. Ecology 90, 1389-1399. doi:10.1890/08-0802.1
96. Michaels, H. J. & Bazzaz, F. A. 1989 Individual and population responses of sexual and apomictic plants to environmental gradients. Am. Nat. 134, 190-207. doi:10.1086/284975
97. Schmitt, J., Dudley, S. A. & Pigliucci, M. 1999 Manipulative approaches to testing adaptive plasticity: phytochrome-mediated shade-avoidance responses in plants. Am. Nat. 154, S43-S54. doi:10.1086/303282
98. Cahill, J. F. 1999 Fertilization effects on interactions between above-ground and below-ground competition in an old field. Ecology 80, 466-480. doi:10.1890/ 0012-9658(1999)080[0466:FEOIBA]2.0.CO;2
99. Wilson, S. D. & Tilman, D. 1995 Competitive responses of eight old-field plant species in four environments. Ecology 76, 1169-1180. doi:10.2307/1940924
100. Cipollini, D. F. & Schultz, J. C. 1999 Exploring cost constraints on stem elongation using phenotypic manipulation. Am. Nat. 153, 236-242. doi:10.1086/ 303164
101. Maliakal, S. K., McDonnell, K., Dudley, S. A. & Schmitt, J. 1999 Effects of red to far-red ratio and plant density on biomass allocation and gas exchange in Impatiens capensis. Int. J. Plant Sci. 160, 723-733. doi:10.1086/314157
102. Gersani, M., Brown, J. S., O'Brien, E. E., Maina, G. M. & Abramsky, Z. 2001 Tragedy of the commons as a result of root competition. J. Ecol. 89, 660-669. doi:10.1046/j. 0022-0477.2001.00609.x
103. Axelrod, R., Hammond, R. A. & Grafen, A. 2004 Altruism via kin-selection strategies that rely on arbitrary tags with which they coevolve. Evolution 58, 1833-1838. doi:10.1111/j.0014-3820.2004.tb00465.x
104. Nowak, M. A. 2006 Five rules for the evolution of cooperation. Science 314, 1560-1563. doi:10.1126/ science.1133755