Temporal Structure in Cooperative Interactions: What Does the Timing of Exploitation Tell Us about Its Cost?

PLoS Biology

Volumn 14, Issue 2, 2016, Pages

  Barker, Jessica L ^a   Bronstein, Judith L ^a  

^a The University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EMPIRICAL RESEARCH; HUMAN; PREDICTION; SPECIES; SYMBIOSIS; ANIMAL; TIME FACTOR;

ANIMALS; SYMBIOSIS; TIME FACTORS;

EID: 84959550689     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002371     Document Type: Article

References (108)

1. Darwin C, On the Origin of Species. London: John Murray; 1859.
2. Boucher DH, The Biology of Mutualism: Ecology and Evolution. The Biology of Mutualism: Ecology and Evolution. Oxford: Oxford University Press; 1985.
3. Bergstrom CT, Bronstein JL, Bshary R, Connor RC, Daly M, Frank SA, Hammerstein P, et al. Interspecific mutualism: puzzles and predictions. In: Genetic and Cultural Evolution of Cooperation. Cambridge, MA: MIT Press; 2003. pp. 241–256.
4. Bronstein JL, Levin SA, Mutualism and symbiosis. In: Princeton Guide to Ecology. Princeton, NJ: Princeton University Press; 2009. pp. 233–238.
5. Bronstein JL, Bronstein JL, The study of mutualism. In: Mutualism. Oxford: Oxford University Press; 2015. pp. 3–19.
6. Bronstein JL, The exploitation of mutualisms. Ecol Lett. 2001;4: 277–287. doi: 10.1046/j.1461-0248.2001.00218.x
7. Yu DW, Parasites of mutualisms. Biol J Linn Soc. 2001;72: 529–546.
8. Bronstein JL, The costs of mutualism. Am Zool. 2001;41: 825–839. doi: 10.1093/icb/41.4.825
9. Douglas AE, Conflict, cheats and the persistence of symbioses. New Phytol. 2008;177: 849–858. doi: 10.1111/j.1469-8137.2007.02326.x18275492
10. Frederickson ME, Rethinking mutualism stability: cheaters and the evolution of sanctions. Q Rev Biol. 2013;88: 269–295. doi: 10.1086/67375724552098
11. Sachs JL, Bronstein JL, The exploitation of mutualisms. In: Mutualism. Oxford: Oxford University Press; 2015. pp. 93–106.
12. Jones EI, Afkhami ME, Akçay E, Bronstein JL, Bshary R, Frederickson ME, et al. Cheaters must prosper: reconciling theoretical and empirical perspectives on cheating in mutualism. Ecol Lett. 2015; doi: 10.1111/ele.12507
13. Ghoul M, Griffin AS, West SA, Toward an evolutionary definition of cheating. Evolution. 2013;68: 318–331. doi: 10.1111/evo.12266
14. West SA, Griffin AS, Gardner A, Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J Evol Biol. 2007;20: 415–432. doi: 10.1111/j.1420-9101.2006.01258.x17305808
15. Weyl EG, Frederickson ME, Yu DW, Pierce NE, Economic contract theory tests models of mutualism. Proc Natl Acad Sci U S A. 2010;107: 15712–15716. 20733067
16. Bshary R, Bronstein JL, A general scheme to predict partner control mechanisms in pairwise cooperative interactions between unrelated individuals. Ethology. 2011;117: 271–283. doi: 10.1111/j.1439-0310.2011.01882.x
17. Kiers ET, Rousseau RA, West SA, Denison RF, Host sanctions and the legume-rhizobium mutualism. Nature. 2003;425: 78–81. doi: 10.1038/nature0193112955144
18. Frederickson ME, Ravenscraft A, Miller GA, Arcila Hernández LM, Booth G, Pierce NE, The direct and ecological costs of an ant-plant symbiosis. Am Nat. 2012;179: 768–778. doi: 10.1086/66565422617264
19. O’Brien S, Brockhurst MA, Social evolution: slimy cheats pay a price. Curr Biol. 2015;25: R378–R381. doi: 10.1016/j.cub.2015.03.01825942554
20. Bronstein JL, Conditional outcomes in mutualistic interactions. Trends Ecol Evol. 1994;9: 214–217. doi: 10.1016/0169-5347(94)90246-121236825
21. Chamberlain SA, Bronstein JL, Rudgers JA, How context dependent are species interactions?Ecol Lett. 2014;17: 881–890. doi: 10.1111/ele.1227924735225
22. Hoeksema JD, Bruna EM, Bronstein JL, Context-dependent outcomes of mutualistic interactions. In: Mutualism. Oxford: Oxford University Press; 2015. pp. 181–202.
23. Irwin RE, Maloof JE, Variation in nectar robbing over time, space, and species. Oecologia. 2002;133: 525–533. doi: 10.1007/s00442-002-1060-z
24. Palmer TM, Doak DF, Stanton ML, Bronstein JL, Kiers ET, Young TP, et al. Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism. Proc Natl Acad Sci U S A. 2010;107: 17234–17239. doi: 10.1073/pnas.100687210720855614
25. Billick I, Tonkel K, The relative importance of spatial vs. temporal variability in generating a conditional mutualism. Ecology. 2003;84: 289–295.
26. Pen I, Taylor PD, Modelling information exchange in worker-queen conflict over sex allocation. Proc R Soc B. 2005;272: 2403–2408. doi: 10.1098/rspb.2005.323416243692
27. Zink AG, Reeve HK, Predicting the temporal dynamics of reproductive skew and group membership in communal breeders. Behav Ecol. 2005;16: 880–888. doi: 10.1093/beheco/ari062
28. Shen S-F, Reeve HK, Herrnkind W, The brave leader game and the timing of altruism among nonkin. Am Nat. 2010;176: 242–248. doi: 10.1086/653663
29. Taylor PD, Day T, Nagy D, Wild G, André J-B, Gardner A, The evolutionary consequences of plasticity in host–pathogen interactions. Theor Popul Biol. 2006;69: 323–331. 16469343
30. Blonder B, Wey TW, Dornhaus A, James R, Sih A, Temporal dynamics and network analysis. Methods Ecol Evol. 2012;3: 958–972. doi: 10.1111/j.2041-210X.2012.00236.x
31. Pinter-Wollman N, Hobson EA, Smith JE, Edelman AJ, Shizuka D, de Silva S, et al. The dynamics of animal social networks: analytical, conceptual, and theoretical advances. Behav Ecol. 2013;25: 242–255. doi: 10.1093/beheco/art047
32. Bronstein JL, Alarcón R, Geber M, The evolution of plant-insect mutualisms. New Phytol. 2006;172: 412–428. doi: 10.1111/j.1469-8137.2006.01864.x17083673
33. Smithson A, Gigord LDB, The evolution of empty flowers revisited. Am Nat. 2003;161: 537–552. doi: 10.1086/36834712776883
34. Irwin RE, Bronstein JL, Manson JS, Richardson L, Nectar robbing: ecological and evolutionary perspectives. Annu Rev Ecol Evol Syst. 2010;41: 271–292. doi: 10.1146/annurev.ecolsys.110308.120330
35. Dufaÿ M, Anstett M-C, Conflicts between plants and pollinators that reproduce within inflorescences: evolutionary variations on a theme. Oikos. 2003;100: 3–14. doi: 10.1034/j.1600-0706.2003.12053.x
36. Peter CI, Johnson SD, Mimic and magnets: the importance of color and ecological facilitation in floral deception. Ecology. 2008;89: 1583–1595. doi: 10.1890/07-1098.1
37. Johnson SD, Peter CI, Nilsson LA, Ågren J, Pollination success in a deceptive orchid is enhanced by co-occurring rewarding magnet plants. Ecology. 2003;84: 2919–2927.
38. Juillet N, Gonzalez MA, Page PA, Gigord LDB, Pollination of the European food-deceptive Traunsteinera globosa (Orchidaceae): the importance of nectar-producing neighbouring plants. Plant Syst Evol. 2007;265: 123–129. doi: 10.1007/s00606-006-0507-9
39. Internicola AI, Page PA, Bernasconi G, Gigord LDB, Competition for pollinator visitation between deceptive and rewarding artificial inflorescences: an experimental test of the effects of floral colour similarity and spatial mingling. Funct Ecol. 2007;21: 864–872. doi: 10.1111/j.1365-2435.2007.01303.x
40. Laverty TM, Plant interactions for pollinator visits: a test of the magnet species effect. Oecologia. 1992;89: 502–508. doi: 10.1007/BF00317156
41. da Paz JRL, Gimenes M, Pigozzo CM, Three diurnal patterns of anthesis in Ipomoea carnea subsp. fistulosa (Convolvulaceae): implications for temporal, behavioral and morphological characteristics of pollinators?Flora. 2013;208: 138–146.
42. Kullenberg B, Studies in Ophrys pollination. Zool Bidr fran Uppsala. 1961;34: 1–340.
43. Brandenburg A, Bshary R, Variable responses of hawkmoths to nectar-depleted plants in two native Petunia axillaris (Solanaceae) populations. Arthropod Plant Interact. 2011;5: 141–148. doi: 10.1007/s11829-011-9122-y
44. Parra-Tabla V, Vargas CF, Phenology and phenotypic natural selection on the flowering time of a deceit-pollinated tropical orchid, Myrmecophila christinae. Ann Bot. 2004;94: 243–50. doi: 10.1093/aob/mch13415205176
45. Sabat AM, Ackerman JD, Fruit set in a deceptive orchid: the effect of flowering phenology, display size, and local floral abundance. Am J Bot. 1996;83: 1181–1186.
46. Lammi A, Kuitunen M, Deceptive pollination of Dactylorhiza incarnata: an experimental test of the magnet species hypothesis. Oecologia. 1995;101: 500–503. doi: 10.1007/BF00329430
47. Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G, Time after time: flowering phenology and biotic interactions. Trends Ecol Evol. 2007;22: 432–439. doi: 10.1016/j.tree.2007.05.00617573151
48. Kindlmann P, Jersáková J, Effect of floral display on reproductive success in terrestrial orchids. Folia Geobot. 2006;41: 47–60. doi: 10.1007/BF02805261
49. Pellissier L, Vittoz P, Internicola AI, Gigord LDB, Generalized food-deceptive orchid species flower earlier and occur at lower altitudes than rewarding ones. J Plant Ecol. 2010;3: 243–250. doi: 10.1093/jpe/rtq012
50. Internicola AI, Harder LD, Bumble-bee learning selects for both early and long flowering in food-deceptive plants. Proc R Soc B. 2012;279: 1538–1543. doi: 10.1098/rspb.2011.184922090384
51. Gaskett AC, Winnick CG, Herberstein ME, Orchid sexual deceit provokes ejaculation. Am Nat. 2008;171: E206–E212. doi: 10.1086/58753218433329
52. Kerdelhué C, Rasplus J-Y, Non-pollinating Afrotropical fig wasps affect the fig-pollinator mutualism in Ficus within the subgenus Sycomorus. Oikos. 1996;75: 3–14.
53. Bshary R, Bronstein JL, Game structures in mutualistic interactions: what can the evidence tell us about the kind of models we need?Adv Study Behav. 2004;34: 59–101.
54. Law R, Bronstein JL, Ferrière R, On mutualists and exploiters: plant-insect coevolution in pollinating seed-parasite systems. J Theor Biol. 2001;212: 373–389. 11829358
55. Raihani NJ, Bshary R, Resolving the iterated prisoner’s dilemma: theory and reality. J Evol Biol. 2011;24: 1628–1639. doi: 10.1111/j.1420-9101.2011.02307.x21599777
56. Axelrod R, Hamilton WD, The evolution of cooperation. Science (80-). 1981;211: 1390–1396.
57. Archetti M, Scheuring I, Hoffman M, Frederickson ME, Pierce NE, Yu DW, Economic game theory for mutualism and cooperation. Ecol Lett. 2011;14: 1300–1312. doi: 10.1111/j.1461-0248.2011.01697.x22011186
58. Foster KR, Diminishing returns in social evolution: the not-so-tragic commons. J Evol Biol. 2004;17: 1058–1072. doi: 10.1111/j.1420-9101.2004.00747.x15312078
59. Weesie J, Asymmetry and timing in the volunteer’s dilemma. J Conflict Resolut. 1993;37: 569–590.
60. Archetti M, The volunteer’s dilemma and the optimal size of a social group. J Theor Biol. 2009;261: 475–480. doi: 10.1016/j.jtbi.2009.08.01819703470
61. Blurton Jones NG, A selfish origin for human food sharing: tolerated theft. Ethol Sociobiol. 1984;5: 1–3.
62. Blurton Jones NG, Tolerated theft, suggestions about the ecology and evolution of sharing, hoarding and scrounging. Soc Sci Inf. 1987;26: 31–54. doi: 10.1177/053901887026001002
63. Winterhalder B, A marginal model of tolerated theft. Ethol Sociobiol. 1996;17: 37–53.
64. Winterhalder B, Social foraging and the behavioral ecology of intragroup resource transfers. Evol Anthropol. 1996;5: 46–57.
65. Patel A, Anstett M-C, Hossaert-McKey M, Kjellberg F, Pollinators entering female dioecious figs: why commit suicide?J Evol Biol. 1995;8: 301–313. doi: 10.1046/j.1420-9101.1995.8030301.x
66. Bradbury JW, Vehrencamp SL, Principles of Animal Communication. 2nd ed. Sunderland, MA: Sinauer Associates; 2011.
67. Reeve HK, The evolution of conspecific acceptance thresholds. Am Nat. 1989;133: 407–435.
68. Green DM, Swets JA, Signal detection theory and psychophysics. New York: Wiley; 1966.
69. Davies NB, Brooke MDL, Kacelnik A, Recognition errors and probability of parasitism determine whether reed warblers should accept or reject mimetic cuckoo eggs. Proc R Soc. 1996;263: 925–931.
70. Yamamura N, Higashi M, Behera N, Yuichiro Wakano J, Evolution of mutualism through spatial effects. J Theor Biol. 2004;226: 421–428. 14759648
71. Doebeli M, Knowlton N, The evolution of interspecific mutualisms. Proc Natl Acad Sci U S A. 1998;95: 8676–8680. doi: 10.1073/pnas.95.15.86769671737
72. Hamilton WD, Eisenberg JF, Dillon WS, Selection of selfish and altruistic behaviour in some extreme models. In: Man and Beast: Comparative Social Behavior. Washington, D. C.: Smithsonian Institution Press; 1971. pp. 59–91.
73. Raine NE, Gammans N, Macfadyen IJ, Scrivner GK, Stone GN, Guards and thieves: antagonistic interactions between two ant species coexisting on the same ant-plant. Ecol Entomol. 2004;29: 345–352. doi: 10.1111/j.0307-6946.2004.00608.x
74. Fayle TM, Edwards DP, Turner EC, Dumbrell AJ, Eggleton P, Foster WA, Public goods, public services and by-product mutualism in an ant-fern symbiosis. Oikos. 2012;121: 1279–1286. doi: 10.1111/j.1600-0706.2011.20062.x
75. Fitzpatrick G, Lanan MC, Bronstein JL, Thermal tolerance affects mutualist attendance in an ant-plant protection mutualism. Oecologia. 2014;176: 129–138. doi: 10.1007/s00442-014-3005-825012597
76. Morris WF, Wilson WG, Bronstein JL, Ness JH, Environmental forcing and the competitive dynamics of a guild of cactus-tending ant mutualists. Ecology. 2005;86: 3190–3199. doi: 10.1890/05-0465
77. Roux O, Céréghino R, Solano PJ, Dejean A, Moreau CS, Caterpillars and fungal pathogens: two co-occurring parasites of an ant-plant mutualism. PLoS ONE. 2011;6: e20538. doi: 10.1371/journal.pone.0020538
78. Yu DW, Pierce NE, A castration parasite of an ant-plant mutualism. Proc R Soc B. 1998;265: 375–382. doi: 10.1098/rspb.1998.0305
79. Fedriani JM, Delibes M, Pulp feeders alter plant interactions with subsequent animal associates. J Ecol. 2013;101: 1581–1588. doi: 10.1111/1365-2745.12146
80. Vander Wall SB, Jenkins SH, Reciprocal pilferage and the evolution of food-hoarding behavior. Behav Ecol. 2003;14: 656–667. doi: 10.1093/beheco/arg064
81. Ness JH, Morris WF, Bronstein JL, Integrating quality and quantity of mutualistic service to contrast ant species protecting Ferocactus wislizeni. Ecology. 2006;87: 912–921. 16676535
82. Morris WF, Vázquez DP, Chacoff NP, Benefit and cost curves for typical pollination mutualisms. Ecology. 2010;91: 1276–1285. doi: 10.1890/08-2278.120503861
83. Irwin RE, Adler LS, Brody AK, The dual role of floral traits: pollinator attraction and plant defense. Ecology. 2004;85: 1503–1511. doi: 10.1890/03-0390
84. Oliver TH, Leather SR, Cook JM, Tolerance traits and the stability of mutualism. Oikos. 2009;118: 346–352. doi: 10.1111/j.1600-0706.2008.17045.x
85. Edwards DP, The roles of tolerance in the evolution, maintenance and breakdown of mutualism. Naturwissenschaften. 2009;96: 1137–45. doi: 10.1007/s00114-009-0559-019484212
86. Kelly D, The evolutionary ecology of mast seeding. Trends Ecol Evol. 1994;9: 465–470. doi: 10.1016/0169-5347(94)90310-721236924
87. Koenig WD, Mumme RL, Carmen WJ, Stanback MT, Acorn production by oaks in central coastal California: variation within and among years. Ecology. 1994;75: 99.
88. Vander Wall SB, Masting in animal-dispersed pines facilitates seed dispersal. Ecology. 2002;83: 3508–3516. doi: 10.1890/0012-9658(2002)083[3508:MIADPF]2.0.CO;2
89. Irwin RE, Realized tolerance to nectar robbing: compensation to floral enemies in Ipomopsis aggregata. Ann Bot. 2009;103: 1425–1433. doi: 10.1093/aob/mcp05619304813
90. Tewksbury JJ, Nabhan GP, Seed dispersal: directed deterrence by capsaicin in chilies. Nature. 2001;412: 403–404. doi: 10.1038/3508665311473305
91. Heil M, Rattke J, Boland W, Postsecretory hydrolysis of nectar sucrose and specialization in ant/plant mutualism. Science. 2005;308: 560–563. doi: 10.1126/science.1107536
92. Labouche A-M, Bernasconi G, Cost limitation through constrained oviposition site in a plant-pollinator/seed predator mutualism. Funct Ecol. 2013;27: 509–521. doi: 10.1111/1365-2435.12062
93. Brouat C, Garcia N, Andary C, McKey D, Plant lock and ant key: pairwise coevolution of an exclusion filter in an ant-plant mutualism. Proc R Soc B. 2001;268: 2131–2141. doi: 10.1098/rspb.2001.176311600077
94. Carpenter FL, Competition between hummingbirds and insects for nectar. Am Zool. 1979;19: 1105–1114. doi: 10.1093/icb/19.4.1105
95. Izzo TJ, Vasconcelos HL, Cheating the cheater: domatia loss minimizes the effects of ant castration in an Amazonian ant-plant. Oecologia. 2002;133: 200–205. doi: 10.1007/s00442-002-1027-0
96. Pyke GH, What does it cost a plant to produce floral nectar? Nature. 1991;350: 58–59.
97. Pyke GH, Optimal nectar production in a hummingbird pollinated plant. Theor Popul Biol. 1981;20: 326–343.
98. Gingins S, Werminghausen J, Johnstone RA, Grutter AS, Bshary R, Power and temptation cause shifts between exploitation and cooperation in a cleaner wrasse mutualism. Proc R Soc B. 2013;280. doi: 10.1098/rspb.2013.0553
99. Sherratt TN, The evolution of Müllerian mimicry. Naturwissenschaften. 2008;95: 681–695. doi: 10.1007/s00114-008-0403-y18542902
100. Jones IM, Koptur S, Dynamic extrafloral nectar production: the timing of leaf damage affects the defensive response in Senna mexicana var. chapmanii (Fabaceae). Am J Bot. 2015;102: 58–66. doi: 10.3732/ajb.140038125587148
101. McNickle GG, Dybzinski R, Game theory and plant ecology. Ecol Lett. 2013;16: 545–555. doi: 10.1111/ele.1207123316756
102. Sick C, Carter AJ, Marshall HH, Knapp LA, Dabelsteen T, Cowlishaw G, Evidence for varying social strategies across the day in chacma baboons. Biol Lett. 2014;10: 3–6. doi: 10.1098/rsbl.2014.0249
103. de Roode JC, Helinski MEH, Anwar MA, Read AF, Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. Am Nat. 2005;166: 531–542. 16224719
104. Frank SA, Models of parasite virulence. Q Rev Biol. 1996;71: 37–78. 8919665
105. Frank SA, Microbial evolution: regulatory design prevents cancer-like overgrowths. Curr Biol. 2013;23: R343–346. doi: 10.1016/j.cub.2013.03.04623660352
106. Frank SA, Perspective: repression of competition and the evolution of cooperation. Evolution. 2003;57: 693–705.
107. Alexander RD, The Biology of Moral Systems. New York: Aldine de Gruyter; 1987.
108. Ratnieks FLW, Wenseleers T, Altruism in insect societies and beyond: voluntary or enforced?Trends Ecol Evol. 2008;23: 45–52. doi: 10.1016/j.tree.2007.09.01318082910