Live where you thrive: joint evolution of habitat choice and local adaptation facilitates specialization and promotes diversity

American Naturalist

Volumn 174, Issue 4, 2009, Pages

  Ravigné, Virginie ^a,b   Dieckmann, Ulf ^c   Olivieri, Isabelle ^a  

^a UNIV MONTPELLIER   (France)

^b CIRAD   (France)

^c INTERNATIONAL INSTITUTE FOR APPLIED SYSTEMS ANALYSIS   (Austria)

Author keywords

Adaptive dynamics; Hard selection; Heterogeneous environment; Protected polymorphism; Soft selection; Trade off

Indexed keywords

COEXISTENCE; COVARIANCE ANALYSIS; DENSITY DEPENDENCE; DIVERSITY INDEX; EVOLUTIONARILY STABLE STRATEGY; HABITAT SELECTION; LIFE CYCLE; LOCAL ADAPTATION; QUALITATIVE ANALYSIS; SITE INVESTIGATION; SPECIALIZATION; TRADE-OFF; VARIANCE ANALYSIS;

ADAPTATION; ANIMAL; ARTICLE; BIOLOGICAL MODEL; DECISION MAKING; ECOSYSTEM; EVOLUTION; GENETIC POLYMORPHISM; LIFE CYCLE; POPULATION DENSITY;

ADAPTATION, BIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; CHOICE BEHAVIOR; ECOSYSTEM; LIFE CYCLE STAGES; MODELS, GENETIC; POLYMORPHISM, GENETIC; POPULATION DENSITY;

EID: 70349416592     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/605369     Document Type: Article

References (132)

1. Abrams, P. A. 2006a. Adaptive change in the resource-exploitation traits of a generalist consumer: the evolution and coexistence of generalists and specialists. Evolution 60:427-439.
2. -2006b. The prerequisites for and likelihood of generalistspecialist coexistence. American Naturalist 167:329-342.
3. Abrams, P. A., Y. Harada, and H. Matsuda. 1993. On the relationship between quantitative genetics and ESS models. Evolution 47:982-985.
4. Anderson, S. S., K. D. McRea, W. G. Abrahamson, and L. M. Hartzel. 1989. Host genotype choice by the ball gallmaker Eurosta solidaginis (Diptera Tephritidae). Ecology 70:1048-1054.
5. Balkau, B. J., and M. W. Feldman. 1973. Selection for migration modification. Genetics 74:171-174.
6. Beltman, J. B., and P. Haccou. 2005. Speciation through the learning of habitat features. Theoretical Population Biology 67:189-202.
7. Beltman, J. B., and J. A. J. Metz. 2005. Speciation: more likely through a genetic or through a learned habitat preference? Proceedings of the Royal Society B: Biological Sciences 272:1455-1463.
8. Beltman, J. B., P. Haccou, and C. Ten Cate. 2004. Learning and colonization of new niches: a first step toward speciation. Evolution 58:35-46.
9. Bernays, E. A. 1998. The value of being a resource specialist: behavioral support for a neural hypothesis. American Naturalist 151: 451-464.
10. Brown, J. S. 1990. Habitat selection as an evolutionary game. Evolution 44:732-746.
11. -1998. Game theory and habitat selection. Pages 188-220 in A. L. Dugatkin and H. K. Reeve, eds. Game theory and animal behavior. Oxford University Press, Oxford.
12. Brown, J. S., and N. B. Pavlovic. 1992. Evolution in heterogeneous environments: effects of migration on habitat specialization. Evolutionary Ecology 6:360-382.
13. Bulmer, M. G. 1972. Multiple niche polymorphism. American Naturalist 106:254-257.
14. Castillo-Chavez, C., S. A. Levin, and F. Gould. 1988. Physiological and behavioral adaptation to varying environments: a mathematical model. Evolution 42:986-994. (Pubitemid 19325666)
15. Christiansen, F. B. 1974. Sufficient conditions for protected polymorphism in a subdivided population. American Naturalist 108: 157-166.
16. -1975. Hard and soft selection in a subdivided population. American Naturalist 109:11-16.
17. -1991. On the conditions for evolutionary stability for a continuously varying character. American Naturalist 138:37-50.
18. Czochor, R. J., and K. J. Leonard. 1982. Multiple-niche polymorphism in haploid microorganisms. American Naturalist 119:293-296.
19. Day, T. 2001. Population structure inhibits evolutionary diversification under competition for resources. Genetica 112-113:71-86. (Pubitemid 34119654)
20. Deakin, M. A. B. 1966. Sufficient conditions for genetic polymorphism. American Naturalist 100:690-692.
21. -1968. Genetic polymorphism in a subdivided population. Australian Journal of Biological Sciences 21:165-168.
22. -1972. Correction. Australian Journal of Biological Sciences 25:213.
23. de Mazancourt, C., and U. Dieckmann. 2004. Trade-off geometries and frequency-dependent selection. American Naturalist 164:765-778.
24. de MeeÛs, T. 2000. Adaptive diversity, specialisation, habitat preference and parasites. Pages 27-42 in R. Poulin, S. Morand, and A. Skorping, eds. Evolutionary biology of host-parasite relationships: theory meets reality. Developments in Animal and Veterinary Sciences. Elsevier, Amsterdam.
25. de Meeûs, T., and J. Goudet. 2000. Adaptive diversity in heterogeneous environments for populations regulated by a mixture of soft and hard selection. Evolutionary Ecology Research 2:981-995.
26. de Meeûs, T., Y. Michalakis, F. Renaud, and I. Olivieri. 1993. Polymorphism in heterogeneous environments, evolution of habitat selection and sympatric speciation. Evolutionary Ecology 7:175-198.
27. Dempster, E. R. 1955. Maintenance of genetic heterogeneity. Cold Spring Harbor Symposia on Quantitative Biology 20:25-32.
28. Dieckmann, U. 1994. Coevolutionary dynamics of stochastic replicator systems. MS thesis, University of Aachen, Germany. Available at http://www.iiasa.ac.at/∼dieckman/reprints/ThesisDieckmann1994.pdf.
29. -1997. Can adaptive dynamics invade? Trends in Ecology & Evolution 12:128-131.
30. Dieckmann, U., and M. Doebeli. 1999. On the origin of species by sympatric speciation. Nature 400:354-357.
31. -2004. Adaptive dynamics of speciation: sexual populations. Pages 76-111 in U. Dieckmann, J. A. J. Metz, M. Doebeli, and D. Tautz, eds. Adaptive speciation. Cambridge University Press, Cambridge.
32. Dieckmann, U., and R. Law. 1996. The dynamical theory of coevolution: a derivation from stochastic ecological processes. Journal of Mathematical Biology 34:579-612. (Pubitemid 126768843)
33. Dieckmann, U., P. Marrow, and R. Law. 1995. Evolutionary cycling in predator-prey interactions: population dynamics and the Red Queen. Journal of Theoretical Biology 176:91-102. (Pubitemid 26452961)
34. Dieckmann, U., J. A. J. Metz, M. Doebeli, and D. Tautz. 2004a. Introduction. Pages 1-16 in U. Dieckmann, J. A. J. Metz, M. Doebeli, and D. Tautz, eds. Adaptive speciation. Cambridge University Press, Cambridge.
35. Dieckmann, U., D. Tautz, M. Doebeli, and J. A. J. Metz. 2004b. Epilogue. Pages 380-394 in U. Dieckmann, J. A. J. Metz, M. Doebeli, and D. Tautz, eds. Adaptive speciation. Cambridge University Press, Cambridge.
36. Diehl, S. R., and G. L. Bush. 1989. The role of habitat preference in adaptation and speciation. Pages 345-365 in D. Otte and J. A. Endler, eds. Speciation and its consequences. Sinauer, Sunderland, MA.
37. Doebeli, M., and U. Dieckmann. 2000. Evolutionary branching and sympatric speciation caused by different types of ecological interactions. American Naturalist 156(suppl.):S77-S101. (Pubitemid 30738208)
38. Doyle, R. W. 1975. Settlement of planktonic larvae: a theory of habitat selection in varying environments. American Naturalist 109:113-126.
39. Edelaar, P., A. M, Siepielski, and J. Clobert. 2008. Matching habitat choice causes directed gene flow: a neglected dimension in evolution and ecology. Evolution 62:2462-2472.
40. Egas, M., U. Dieckmann, and M. W. Sabelis. 2004. Evolution restricts the coexistence of specialists and generalists: the role of trade-off structure. American Naturalist 163:518-531. (Pubitemid 38630545)
41. Eshel, I., and U. Motro. 1981. Kin selection and strong evolutionary stability of mutual help. Theoretical Population Biology 19:420-433.
42. Felsenstein, J. 1981. Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution 35:124-138.
43. Fretwell, S. D. 1972. Populations in a seasonal environment. Princeton University Press, Princeton, NJ.
44. Fretwell, S. D., and H. J. Lucas. 1970. On territorial behavior and other factors influencing habitat distribution in birds. Acta Biotheoretica 14:16-36.
45. Fry, J. D. 2003. Multilocus models of sympatric speciation: Bush versus Rice versus Felsenstein. Evolution 57:1735-1746.
46. Fryxell, J. M. 1997. Evolutionary dynamics of habitat use. Evolutionary Ecology 11:687-701.
47. Futuyma, D. J. 1997. Evolutionary biology. Sinauer, Sunderland, MA.
48. Futuyma, D. J., and G. Moreno. 1988. The evolution of ecological specialization. Annual Review of Ecology and Systematics 19:207-233.
49. Garcia-Dorado, A. 1986. The effect of niche preference on polymorphism protection in a heterogeneous environment. Evolution 40:936-945. (Pubitemid 18284968)
50. -1987. Polymorphism from environmental heterogeneity: some features of genetically induced niche preference. Theoretical Population Biology 32:66-75.
51. Geritz, S. A. H., and E. Kisdi. 2000. Adaptive dynamics in diploid, sexual populations and the evolution of reproductive isolation. Proceedings of the Royal Society B: Biological Sciences 267:1671-1678.
52. Geritz, S. A. H., J. A. J. Metz, E. Kisdi, and G. Meszéna. 1997. The dynamics of adaptation and evolutionary branching. Physical Review Letters 78:2024-2027.
53. Gliddon, C., and C. Strobeck. 1975. Necessary and sufficient conditions for multiple-niche polymorphism in haploids. American Naturalist 109:233-235.
54. Hedrick, P. W. 1990a. Genotypic-specific habitat selection: a new model and its application. Heredity 65:145-149.
55. --1990 Theoretical analysis of habitat selection and the maintenance of genetic variation. Pages 209-227 in J. S. F. Barker, W. T. Starmer, and R. Maclntyre, eds. Ecological and evolutionary genetics of Drosopkila. Plenum, New York.
56. HilleRisLambers, R., and U. Dieckmann. 2003. Competition and predation in simple food webs: intermediately strong trade-offs maximize coexistence. Proceedings of the Royal Society B: Biological Sciences 270:2591-2598. (Pubitemid 38082947)
57. Hofbauer, J., and K. Sigmund. 1990. Adaptive dynamics and evolutionary stability. Applied Mathematics Letters 3:75-79.
58. Holsinger, K. E., and S. W. Pacala. 1990. Multiple-niche polymorphisms in plant populations. American Naturalist 135:301-309.
59. Holt, R. D. 1985. Density-independent mortality, non-linear competitive interactions, and species coexistence. Journal of Theoretical Biology 116:479-493.
60. Holt, R. D., and M. S. Gaines. 1992. Analysis of adaptation in heterogeneous landscapes-implications for the evolution of fundamental niches. Evolutionary Ecology 6:433-447.
61. Iwasa, Y., A. Pomiankowski, and S. Nee. 1991. The evolution of costly mate preferences. II. The "handicap" principle. Evolution 45:1431-1442.
62. Jaenike, J. 1990. Host specialization in phytophagous insects. Annual Review of Ecology and Systematics 21:243-273.
63. Jaenike, J., and R. D. Holt. 1991. Genetic variation for habitat preference: evidence and explanations. American Naturalist 137(suppl.): S67-S90.
64. Johnson, P. A., F. C. Hoppensteadt, J. J. Smith, and G. L. Bush. 1996. Conditions for sympatric speciation: a diploid model incorporating habitat fidelity and non-habitat assortative mating. Evolutionary Ecology 10:187-205. (Pubitemid 27003621)
65. Karlin, S. 1982. Classification of selection migration structures and conditions for a protected polymorphism. Evolutionary Biology 14:61-204.
66. Karlin, S., and R. B. Campbell. 1981. The existence of a protected polymorphism under conditions of soft as opposed to hard selection in a multideme population system. American Naturalist 117:262-275.
67. Karlin, S., and J. McGregor. 1972. Application of method of small parameters to multi-niche population genetic models. Theoretical Population Biology 3:186-209.
68. Kawecki, T. J. 1997. Sympatric speciation via habitat specialization driven by deleterious mutations. Evolution 51:1751-1763.
69. Kisdi, E. 2001. Long-term adaptive diversity in Levene-type models. Evolutionary Ecology Research 3:721-727. (Pubitemid 33631421)
70. -2002. Dispersal: risk spreading versus local adaptation. American Naturalist 159:579-596.
71. Kisdi, E., and S. A. H. Geritz. 1999. Adaptive dynamics in allele space: evolution of genetic polymorphism by small mutations in a heterogeneous environment. Evolution 53:993-1008. (Pubitemid 29416943)
72. Lande, R. 1976. Natural selection and random genetic drift in phenotypic evolution. Evolution 30:314-334.
73. Lawlor, L. R., and J. Maynard Smith. 1976. The coevolution and stability of competing species. American Naturalist 110:79-99.
74. Leimar, O. 2005. The evolution of phenotypic polymorphism: randomized strategies versus evolutionary branching. American Naturalist 165:669-681. (Pubitemid 40748344)
75. -2009. Multidimensional convergence stability. Evolutionary Ecology Research 11:191-208.
76. Levene, H. 1953. Genetic equilibrium when more than one niche is available. American Naturalist 87:331-333.
77. Levins, R. 1962. Theory of fitness in a heterogeneous environment. I. The fitness set and adaptive function. American Naturalist 96: 361-373.
78. -1963. Theory of fitness in a heterogeneous environment. II. Developmental flexibility and niche selection. American Naturalist 97:75-90.
79. -1968. Evolution in changing environments. Princeton University Press, Princeton, NJ.
80. Levins, R., and R. MacArthur. 1966. Maintenance of genetic polymorphism in a spatially heterogeneous environment: variations on a theme by Howard Levene. American Naturalist 100:585-589.
81. MacArthur, R., and R. Levins. 1964. Competition, habitat selection and character displacement in a patchy environment. Proceedings of the National Academy of Sciences of the USA 51:1207-1210.
82. -1967. Limiting similarity convergence and divergence of coexisting species. American Naturalist 101:377-385.
83. MacArthur, R., and E. R. Pianka. 1966. On optimal use of a patchy environment. American Naturalist 100:603-609.
84. Mayhew, P. J. 1997. Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79:417-428. (Pubitemid 27268895)
85. Maynard Smith, J. 1966. Sympatric speciation. American Naturalist 100:637-650.
86. -1989. Evolutionary genetics. Oxford University Press, Oxford.
87. Maynard Smith, J., and R. Hoekstra. 1980. Polymorphism in a varied environment: how robust are the models? Genetical Research 35: 45-47.
88. Maynard Smith, J., and G. R. Price. 1973. The logic of animal conflict. Nature 246:15-18.
89. McPeek, M. A., and R. D. Holt. 1992. The evolution of dispersal in spatially and temporally varying environments. American Naturalist 140:1010-1027.
90. Meszéna, G., I. Czibula, and S. A. H. Geritz. 1997. Adaptive dynamics in a 2-patch environment: a toy model for allopatric and parapatric speciation. Journal of Biological Systems 5:265-284. (Pubitemid 127532717)
91. Meszéna, G., E. Kisdi, U. Dieckmann, S. A. H. Geritz, and J. A. J. Metz. 2001. Evolutionary optimisation models and matrix games in the unified perspective of adaptive dynamics. Selection 2:193-210.
92. Metz, J. A. J., R. M. Nisbet, and S. A. H. Geritz. 1992. How should we define "fitness" for general ecological scenarios? Trends in Ecology & Evolution 7:198-202.
93. Metz, J. A. J., S. A. H. Geritz, G. Meszéna, F. J. A. Jacobs, and J. S. van Heerwaarden. 1996. Adaptive dynamics: a geometrical study of the consequences of nearly faithful reproduction. Pages 183- 231 in S. J. van Strien and S. M. Verduyn-Lunel, eds. Stochastic and spatial structures of dynamical systems. North Holland, Amsterdam.
94. Morris, D. W. 1988. Habitat-dependent population regulation and community structure. Evolutionary Ecology 2:253-269. (Pubitemid 19323487)
95. -1992. Scales and costs of habitat selection in heterogeneous landscapes. Evolutionary Ecology 6:412-432.
96. -1999. Has the ghost of competition passed? Evolutionary Ecology Research 1:3-20.
97. - 2003. Toward an ecological synthesis: a case for habitat selection. Oecologia (Berlin) 136:1-13.
98. Muko, S., and Y. Iwasa. 2000. Species coexistence by permanent spatial heterogeneity in a lottery model. Theoretical Population Biology 57:273-284. (Pubitemid 30369060)
99. Myers, J. H., J. Monro, and M. Neil. 1981. Egg clumping, host plant selection and population regulation in Cactoblastis cactorum (Lepidoptera). Oecologia (Berlin) 51:7-13.
100. Nurmi, T., and K. Parvinen. 2008. On the evolution of specialization with a mechanistic underpinning in structured metapopulations. Theoretical Population Biology 73:222-243.
101. Phillips, S. W., J. S. Bale, and G. M. Tatchell. 2000. Overwintering adaptations in the lettuce root aphid Pemphigus bursarius (L.). Journal of Insect Physiology 46:353-363.
102. Prout, T. 1968. Sufficient conditions for multiple niche polymorphism. American Naturalist 102:493-496.
103. Rausher, M. D. 1984. The evolution of habitat preference in subdivided populations. Evolution 38:596-608.
104. --------. 1993. The evolution of habitat preference: avoidance and adaptation. Pages 259-283 in K. C. Kim and B. A. McPheron, eds. Evolution of insect pests: the pattern of variations. Evolutionary Biology. Wiley, New York.
105. Rausher, M. D., and R. Englander. 1987. The evolution of habitat preference. II. Evolutionary genetic stability under soft selection. Theoretical Population Biology 31:116-139.
106. Ravigné, V., I. Olivieri, and U. Dieckmann. 2004. Implications of habitat choice for protected polymorphisms. Evolutionary Ecology Research 6:125-145. (Pubitemid 38184808)
107. Robinson, B. W., and D. S. Wilson. 1998. Optimal foraging, specialization and a solution to Liem's paradox. American Naturalist 151: 223-235.
108. Rohde, K. 1979. A critical evaluation of intrinsic and extrinsic factors responsible for niche restriction in parasites. American Naturalist 114:648-671.
109. Ronce, O. 2007. How does it feel to be like a rolling stone? ten questions about dispersal evolution. Annual Review of Ecology, Evolution, and Systematics 38:231-253.
110. Ronce, O., and M. Kirkpatrick. 2001. When sources become sinks: migrational meltdown in heterogeneous habitats. Evolution 55: 1520-1531. (Pubitemid 32908214)
111. Ronce, O., I. Olivieri, J. Clobert, and E. Danchin. 2001. Perspective on the study of dispersal evolution. Pages 341-357 in J. Clobert, E. Danchin, J. D. Nichols, and A. A. Dhondt, eds. Dispersal. Oxford University Press, Oxford.
112. Rosenzweig, M. L. 1974. On the evolution of habitat selection. Pages 401-404 in Proceedings of the First International Congress of Ecology, Wageningen. Centre for Agricultural Publishing and Documentation, The Hague.
113. -1981. A theory of habitat selection. Ecology 62:327-335.
114. Rueffler, C., T. J. M., Van Dooren, and J. A. J. Metz. 2004. Adaptive walks on changing landscapes: Levins' approach extended. Theoretical Population Biology 65:165-178.
115. -2006a. The evolution of resource specialization through frequency-dependent and frequency-independent mechanisms. American Naturalist 167:81-93.
116. Rueffler, C., M. Egas, and J. A. J. Metz. 2006b. Evolutionary predictions should be based on individual-level traits. American Naturalist 168:E148-E162.
117. Rueffler, C., T. J. M. Van Dooren, and J. A. J. Metz. 2007. The interplay between behavior and morphology in the evolutionary dynamics of resource specialization. American Naturalist 169:E34E52.
118. Sasaki, A., and G. de Jong. 1999. Density dependence and unpredictable selection in a heterogeneous environment: compromise and polymorphism in the ESS reaction norm. Evolution 53:1329-1342. (Pubitemid 29524128)
119. Smiley, J. 1978. Plant chemistry and evolution of host specificity: new evidence from Heliconius and Passiflora. Science 201:745-747. (Pubitemid 9007680)
120. Spichtig, M., and T. J. Kawecki. 2004. The maintenance (or not) of polygenic variation by soft selection in heterogeneous environments. American Naturalist 164:70-84. (Pubitemid 38991833)
121. Stamps, J. A., and J. M. Davis. 2006. Adaptive effects of natal experience on habitat selection by dispersers. Animal Behaviour 72: 1279-1289. (Pubitemid 44779522)
122. Taper, M. L., and T. J. Case. 1992. Models of character displacement and the theoretical robustness of taxon cycles. Evolution 46:317-333.
123. Taylor, P. D. 1989. Evolutionary stability in one-parameter models under weak selection. Theoretical Population Biology 36:125-143.
124. Templeton, A. R., and L. D. Rothman. 1981. Evolution in fine-grained environments. II. Habitat selection as a homeostatic mechanism. Theoretical Population Biology 19:326-340.
125. van Tienderen, P. H. 1991. Evolution of generalists and specialists in spatially heterogeneous environments. Evolution 45:1317-1331.
126. 1997. Generalists, specialists, and the evolution of pheno- typic plasticity in sympatric populations of distinct species. Evolution 51:1372-1380.
127. Wallace, B. 1975. Hard and soft selection revisited. Evolution 29:465-473.
128. Ward, S. A. 1987. Optimal habitat selection in time-limited dispersers. American Naturalist 129:568-579.
129. Wiener, P., and M. W. Feldman. 1993. The effects of the mating system on the evolution of migration in a spatially heterogeneous population. Evolutionary Ecology 7:251-269. (Pubitemid 24412289)
130. Wilson, D. S., and M. Turelli. 1986. Stable underdominance and the evolutionary invasion of empty niches. American Naturalist 127: 835-850.
131. Wilson, D. S., and J. Yoshimura. 1994. On the coexistence of specialists and generalists. American Naturalist 144:692-707.
132. Yukilevich, R., and J. R. True. 2006. Divergent outcomes of reinforcement speciation: the relative importance of assortative mating and migration modification. American Naturalist 167:638-654. (Pubitemid 43748950)