The roles of tolerance in the evolution, maintenance and breakdown of mutualism

Naturwissenschaften

Volumn 96, Issue 10, 2009, Pages 1137-1145

  Edwards, David P ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

By product mutualism; Evolved dependence; Host sanction; Overcompensation; Resistance; Symbiosis

Indexed keywords

ANTAGONISM; FITNESS; HOST-PARASITE INTERACTION; LIFE HISTORY TRAIT; MUTUALISM; SOCIAL BEHAVIOR; TOLERANCE;

EVOLUTIONARY ADAPTATION; HOST CELL; HOST PARASITE INTERACTION; NONHUMAN; PARASITE; REVIEW; SYMBIOSIS;

ANIMALS; ANTS; EVOLUTION, MOLECULAR; FLOWERS; HOST-PARASITE INTERACTIONS; MODELS, BIOLOGICAL; MOTHS; PARASITES; PHEROMONES; PLANTS; POLLINATION; SIGNAL TRANSDUCTION; SYMBIOSIS; WASPS;

EID: 70349599017     PISSN: 00281042     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00114-009-0559-0     Document Type: Review

References (110)

1. DK Aanen RF Hoekstra 2007 The evolution of obligate mutualism: if you can't beat 'em, join 'em Trends Ecol Evol 22 506 509 17825952
2. AA Agrawal 2000 Overcompensation of plants in response to herbivory and the by-product benefits of mutualism Trends Plant Sci 5 309 313 10871904 1:STN:280:DC%2BD3cvgtlCgtQ%3D%3D
3. AA Agrawal R Karban 1997 Domatia mediate plant-arthropod mutualism Nature 387 562 563 1:CAS:528:DyaK2sXktFCisbk%3D
4. R Axelrod WD Hamilton 1981 The evolution of cooperation Science 211 1390 1396 7466396 1:STN:280:DyaL3M7is1emsg%3D%3D
5. F Backhed RE Ley JL Sonnenburg DA Peterson JI Gordon 2005 Host-bacterial mutualism in the human intestine Science 211 1390 1396
6. Bergström CT, Bronstein JL, Bshary R, Connor RC, Daly M, Frank SA, Gintis H, Keller L, Leimar O, Noë R, Queller DC (2003) Group report: interspecific mutualism. Puzzles and predictions. In: Hammerstein P (ed) Genetic and cultural evolution of cooperation. MIT Press, Massachusetts, pp 241-256
7. CJ Bilbrough JH Richards 1993 Growth of sagebrush and bitterbrush following simulated winter browsing-mechanisms of tolerance Ecology 74 481 492
8. M Boots 2008 Fight or learn to live with the consequences? Trends Ecol Evol 23 248 250 18374449
9. JL Bronstein 1994 Conditional outcomes in mutualistic interactions Trends Ecol Evol 9 214 217
10. JH Brown 1983 Interaction and coevolution-Thompson, Jn Science 220 1043 1043 17754548
11. R Bshary AS Grutter 2002 Asymmetric cheating opportunities and partner control in a cleaner fish mutualism Anim Behav 63 547 555
12. R Bshary AS Grutter 2002 Experimental evidence that partner choice is a driving force in the payoff distribution among cooperators or mutualists: the cleaner fish case Ecol Letts 5 130 136
13. R Bshary D Schaffer 2002 Choosy reef fish select cleaner fish that provide high-quality service Anim Behav 63 557 564
14. R Bshary R Bergmüller 2008 Distinguishing four fundamental approaches to the evolution of helping J Evol Biol 21 405 420 18179515 1:STN:280:DC%2BD1c7htFCmuw%3D%3D
15. JJ Bull WR Rice 1991 Distinguishing mechanisms for the evolution of cooperation J Theo Biol 149 63 74 1:STN:280:DyaK3MzltVOrug%3D%3D
16. JH Christy 1995 Mimicry, mate choice, and the sensory trap hypothesis Am Nat 146 171 181
17. K Clay 1991 Parasitic castration of plants by fungi Trends Ecol Evol 6 141 172
18. K Clay C Schardl 2002 Evolutionary origins and ecological consequences of endophyte symbiosis with grasses Am Nat 160 S99 S127 18707456
19. RC Connor 1986 Pseudo-reciprocity-investing in mutualism Anim Behav 34 1562 1566
20. R Connor 2007 Invested, extracted and byproduct benefits: a modified scheme for the evolution of cooperation Behav Processes 76 109 113 17714885
21. DW Davidson D McKey 1993 The evolutionary ecology of symbiotic ant-plant relationships J Hym Res 2 13 83
22. C De Mazancourt M Loreau U Dieckmann 2005 Understanding mutualism when there is adaptation to the partner J Ecol 93 305 314
23. M Doebeli N Knowlton 1998 The evolution of interspecific mutualism Proc Nat Acad Sci U S A 95 8676 8680 1:CAS:528:DyaK1cXkvFals7k%3D
24. BB Edinger 1985 Conditional mutualism in three aphid-tending ants Bull Ecol Soc Am 66 168
25. DP Edwards R Arauco M Hassall WJ Sutherland K Chamberlain LJ Wadhams DW Yu 2007 Protection in an ant-plant mutualism: an adaptation or a sensory trap? Anim Behav 74 377 385
26. DP Edwards DW Yu 2007 The roles of sensory traps in the origin, maintenance, and breakdown of mutualism Behav Ecol Sociobiol 61 1321 1327
27. DP Edwards DW Yu 2008 Tolerating castration by hiding flowers in plain sight Behav Ecol Sociobiol 63 95 102
28. DP Edwards M Hassall WJ Sutherland DW Yu 2006 Selection for protection in an ant-plant mutualism: host sanctions, host modularity and the principal-agent game Proc R Soc Lond B 273 595 602
29. EG Espinosa J Fornoni 2006 Host tolerance does not impose selection on natural enemies New Phytologist 170 609 614 16626480
30. SH Faeth TJ Sullivan 2003 Mutualistic asexual endophytes in a native grass are usually parasitic Am Nat 161 310 325 12675375
31. PA Fay DC Hartnett AK Knapp 1996 Plant tolerance of gall-insect attack and gall-insect performance Ecology 77 521 534
32. K Fenn M Baxter 2004 Are filarial nematode Wolbachia obligate mutualist symbionts? Trends Ecol Evol 19 163 166 16701248
33. JB Ferdy B Godelle 2005 Diversification of transmission modes and the evolution of mutualism Am Nat 166 613 627 16224726
34. MK Fischer AW Shingleton 2001 Host plant and ants influence the honeydew sugar composition of aphids Funct Ecol 15 544 550
35. MK Fischer KH Hoffmann W Völkl 2001 Competition for mutualists in an ant-Homopteran interaction mediated by hierarchies of ant attendance Oikos 92 531 541
36. J Fornoni J Núñez-Farfán PL Valverde MD Rausher 2004 Evolution of mixed strategies of plant defense allocation against natural enemies Evolution 58 1685 1695 15446423
37. KR Foster T Wenseleers 2006 A general model for the evolution of mutualisms J Evol Biol 19 1283 1293 16780529 1:STN:280:DC%2BD28zmslCksg%3D%3D
38. WA Foster PK Rhoden 1998 Soldiers effectively defend aphid colonies against predators in the field Anim Behav 55 761 765 9514674
39. SA Frank 1996 Host-symbiont conflict over the mixing of symbiotic lineages Proc R Soc Lond B 263 339 344 1:STN:280:DyaK2s%2FnslKrug%3D%3D
40. SA Frank 2003 Perspective: repression of competition and the evolution of cooperation Evolution 57 693 705 12778541
41. J Ghazoul 2001 Can floral repellents pre-empt potential ant-plant conflicts? Ecol Letts 4 295 299
42. PA Gronemeyer BJ Dilger JL Bouzat KN Paige 1997 The effects of herbivory on paternal fitness in scarlet gilia: better moms also make better pops Am Nat 150 592 602 18811302 1:STN:280:DC%2BD1cnit1OrsQ%3D%3D
43. AS Grutter 2001 Parasite infection rather than tactile stimulation is the proximate cause of cleaning behaviour in reef fish Proc R Soc Lond B 268 1361 1365 1:STN:280:DC%2BD3Mznt12gsg%3D%3D
44. AS Grutter R Bshary 2003 Cleaner wrasse prefer client mucus: support for partner control mechanisms in cleaning interactions Proc R Soc Lond B 270 S242 S244
45. WD Hamilton 1964 The genetical evolution of social behaviour 1 J Theo Biol 7 1 16 1:STN:280:DyaF2s7jtVehsA%3D%3D
46. WD Hamilton 1964 The genetical evolution of social behaviour 2 J Theo Biol 7 17 52 1:STN:280:DyaF2s7jtVehsw%3D%3D
47. Inouye DW (1983) The ecology of nectar robbing. In: Bentley B, Elias T (eds) The biology of nectarines. Columbia University Press, New York, pp 153-173
48. DH Janzen 1980 When is it coevolution Evolution 34 611 612
49. J Jaremo J Tuomi P Nilsson T Lennartsson 1999 Plant adaptations to herbivory: mutualistic versus antagonistic coevolution Oikos 84 313 320
50. RA Johnstone R Bshary 2008 Mutualism, market effects and partner control J Evol Biol 21 879 888 18312320 1:STN:280:DC%2BD1c3kvVOksg%3D%3D
51. Keeler KH (1985) Cost:benefit models of mutualism. In: Boucher DH (ed) The biology of mutualism, ecology and evolution. Oxford University Press, England, pp 100-127
52. ET Kiers RA Rousseau SA West RF Denison 2003 Host sanctions and the legume-rhizobium mutualism Nature 425 78 81 12955144 1:CAS:528: DC%2BD3sXmvFans78%3D
53. T Koskela S Puustinen V Salonen P Mutikainen 2002 Resistance and tolerance in a host plant-holoparasitic plant interaction: genetic variation and costs Evolution 56 899 908 12093026
54. Leimar O, Connor RC (2003) By-product benefits, reciprocity and pseudoreciprocity in mutualism. In: Hammerstein P (ed) Genetic and cultural evolution of cooperation. MIT Press, Massachusetts, pp 203-222
55. R Leimu J Koricheva 2006 A meta-analysis of tradeoffs between plant tolerance and resistance to herbivores: combining the evidence from ecological and agricultural studies Oikos 112 1 9
56. T Lennartsson J Tuomi P Nilsson 1997 Evidence for an evolutionary history of overcompensation in the grassland biennial Gentianella campestris (Gentianaceae) Am Nat 149 1147 1155 18811268 1:STN:280:DC%2BD1cnit1Onuw%3D%3D
57. T Lennartsson P Nilsson J Tuomi 1998 Induction of overcompensation in the field gentian, Gentianella campestris Ecology 79 1061 1072
58. JE Maloof DW Inouye 2000 Are nectar robbers cheaters or mutualists? Ecology 81 2651 2661
59. R Mauricio MD Rausher DS Burdick 1997 Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78 1301 1311
60. AC McCall RE Irwin 2006 Florivory: the intersection of pollination and herbivory Ecol Letts 9 1351 1365
61. R Medel 2001 Assessment of correlational selection on tolerance and resistance traits in a host plant-parasitic plant interaction Evol Ecol 15 37 52
62. MR Miller A White M Boots 2006 The evolution of parasites in response to tolerance in their hosts: the good, the bad, and apparent commensalism Evolution 60 945 956 16817535
63. R Noë P Hammerstein 1994 Biological markets-supply-and-demand determine the effect of partner choice in cooperation, mutualism and mating Behav Ecol Sociobiol 35 1 11
64. J Núñez-Farfán J Fornoni PL Valverde 2007 The evolution or resistance and tolerance to herbivores Ann Rev Ecol Evol Syst 38 541 566
65. TH Oliver SR Leather JM Cook 2009 Tolerance traits and the stability of mutualism Oikos 118 346 352 10.1111/j.1600-0706.2008.17045.x
66. KN Paige 1999 Regrowth following ungulate herbivory in Ipomopsis aggregata: geographic evidence for overcompensation Oecologia 118 316 323
67. KN Paige TG Whitham 1987 Flexible life-history traits-shifts by scarlet gilia in response to pollinator abundance Ecology 68 1691 1695
68. BA Pannebakker B Loppin CPH Elemans L Humblot F Vavre 2007 Parasitic inhibition of cell death facilitates symbiosis Proc Nat Acad Sci U S A 104 213 215 1:CAS:528:DC%2BD2sXjs1WltQ%3D%3D
69. O Pellmyr CJ Huth 1994 Evolutionary stability of mutualism between yuccas and yucca moths Nature 372 257 260 1:CAS:528:DyaK2MXit1OqsLo%3D
70. L Råberg D Sim AF Read 2007 Disentangling genetic variation for resistance and tolerance to infectious diseases in animals Science 318 812 814 17975068
71. L Råberg AL Graham AF Read 2009 Decomposing health: tolerance and resistance to parasites in animals Phil Trans R Soc Lond B 364 37 49
72. NE Raine P Willmer GN Stone 2002 Spatial structuring and floral avoidance behavior prevent ant-pollinator conflict in a Mexican ant-acacia Ecology 83 3086 3096
73. RS Redman DD Dunigan RJ Rodriguez 2001 Fungal symbiosis from mutualism to parasitism: who controls the outcome, host or invader? New Phytologist 151 705 716
74. O Restif JC Koella 2003 Shared control of epidemiological traits in a coevolutionary model of host-parasite interactions Am Nat 161 827 836 12858269
75. O Restif JC Koella 2004 Concurrent evolution of resistance and tolerance to pathogens Am Nat 164 E90 E102 15459887
76. SC Richardson 2004 Are nectar-robbers mutualists or antagonists? Oecologia 139 246 254 14767755
77. SC Richardson 2004 Benefits and costs of floral visitors to Chilopsis linearis: pollen deposition and stigma closure Oikos 107 363 375
78. JP Rosenthal PM Kotanen 1994 Terrestrial plant tolerance to herbivory Trends Ecol Evol 9 145 148
79. BA Roy JW Kirchner 2000 Evolutionary dynamics of pathogen resistance and tolerance Evolution 54 51 63 10937183 1:CAS:528:DC%2BD3cXis1egtLk%3D
80. JL Sachs EL Simms 2006 Pathways to mutualism breakdown Trends Ecol Evol 21 585 592 16828927
81. JL Sachs UG Mueller TP Wilcox JJ Bull 2004 The evolution of cooperation Quart Rev Biol 79 135 160 15232949
82. K Saikkonen P Wali M Helander SH Faeth 2004 Evolution of endophyte-plant symbioses Trends Plant Sci 9 275 280 15165558 1:CAS:528:DC%2BD2cXksVemtbY%3D
83. JM Shapiro JF Addicott 2003 Regulation of moth-yucca mutualisms: mortality of eggs in oviposition-induced 'damage zones' Ecol Letts 6 440 447
84. AW Shingleton WA Foster 2000 Ant tending influences soldier production in a social aphid Proc R Soc Lond B 267 1863 1868 1:STN:280:DC%2BD3M3jt1Knsg%3D%3D
85. AM Siepielski CW Benkman 2007 Extreme environmental variation sharpens selection that drives the evolution of a mutualism Proc R Soc Lond B 274 1799 1805
86. EL Simms J Triplett 1994 Costs and benefits of plant-responses to disease-resistance and tolerance Evolution 48 1973 1985
87. A Smithson LD Gigord 2003 The evolution of empty flowers revisited Am Nat 161 537 552 12776883
88. JR Stinchcombe 2002 Can tolerance traits impose selection on herbivores? Evol Ecol 16 595 602
89. KA Stowe RJ Marquis CG Hochwender EL Simms 2000 The evolutionary ecology of tolerance to consumer damage Ann Rev Ecol Syst 31 565 595
90. SY Strauss AA Agrawal 1999 The ecology and evolution of plant tolerance to herbivory Trends Ecol Evol 14 179 185 10322530
91. B Stradler AFG Dixon 2005 Ecology and evolution of aphid-ant interactions Ann Rev Ecol Syst 36 345 372
92. S Takeda K Kinomura H Sakurai 1982 Effects of ant-attendance on the honeydew excretion and larviposition of the cowpea aphid Appl Entomol Zool 17 133 135
93. Thompson JN (1982) Interaction and coevolution. Wiley, New York
94. JN Thompson BM Cunningham 2002 Geographic structure and dynamics of coevolutionary selection Nature 417 735 738 12066183 1:CAS:528: DC%2BD38XksVGju70%3D
95. P Tiffin 2000 Are tolerance, avoidance, and antibiosis evolutionarily and ecologically equivalent responses of plants to herbivores? Am Nat 155 128 138 10657182
96. S Wambua TW Mwangi M Kortok SM Uyoga AW Macharia JK Mwacharo DJ Weatherall RW Snow K Marsh TN Williams 2006 The effect of alpha(+)-thalassaemia on the incidence of malaria and other diseases in children living on the coast of Kenya Plos Med 3 643 651
97. MJ Way 1963 Mutualism between ants and honeydew-producing Homoptera Ann Rev Entomol 8 307 344
98. SA West AS Griffin A Gardner 2007 Evolutionary explanations for cooperation Current Biol 17 R661 R672 1:CAS:528:DC%2BD2sXpt1KntrY%3D
99. SA West ET Kiers I Pen RF Denison 2002 Sanctions and mutualism stability: when should less beneficial mutualists be tolerated? J Evol Biol 15 830 837
100. SA West ET Kiers EL Simms RF Denison 2002 Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proc R Soc Lond B 269 685 694
101. MJ Wise JJ Cummins 2006 Strategies of Solanum carolinense for regulating maternal investment in response to foliar and floral herbivory J Ecol 94 629 636
102. MEJ Woolhouse JP Webster E Domingo B Charlesworth BR Levin 2002 Biological and biomedical implications of the co-evolution of pathogens and their hosts Nat Genet 32 569 577 12457190 1:CAS:528:DC%2BD38XptVShu7Y%3D
103. I Yao S Akimoto 2001 Ant attendance changes the sugar composition of the honeydew of the drepanosiphid aphid Tuberculatus quercicola Oecologia 128 36 43
104. I Yao S Akimoto 2002 Flexibility in the composition and concentration of amino acids in honeydew of the drepanosiphid aphid Tuberculatus quercicola Ecol Entomol 27 745 752
105. I Yao H Shibao S Akimoto 2000 Costs and benefits of ant attendance to the drepanosiphid aphid Tuberculatus quercicola Oikos 89 3 10
106. DW Yu 2001 Parasites of mutualisms Biol J Linn Soc 72 529 546
107. DW Yu HB Wilson NE Pierce 2001 An empirical model of species coexistence in a spatially structured environment Ecology 82 1761 1771
108. DW Yu NE Pierce 1998 A castration parasite of an ant-plant mutualism Proc R Soc Lond B 265 375 382
109. DW Yu J Ridley E Jousselin EA Herre SG Compton JM Cook JC Moore GD Weiblen 2004 Oviposition strategies, host coercion and the stable exploitation of figs by wasps Proc R Soc Lond B 271 1185 1195
110. DW Yu HB Wilson ME Frederickson W Palomino R De la Colina DP Edwards AA Balareso 2004 Experimental demonstration of species coexistence enabled by dispersal limitation J Anim Ecol 73 1102 1114