Advertisement

Biology & Philosophy

, 23:673 | Cite as

Whither adaptation?

  • Andrew P. HendryEmail author
  • Andrew Gonzalez
Article

Abstract

The two authors of this paper have diametrically opposed views of the prevalence and strength of adaptation in nature. Hendry believes that adaptation can be seen almost everywhere and that evidence for it is overwhelming and ubiquitous. Gonzalez believes that adaptation is uncommon and that evidence for it is ambiguous at best. Neither author is certifiable to the knowledge of the other, leaving each to wonder where the other has his head buried. Extensive argument has revealed that each author thinks his own view is amply supported by both theory and empirical evidence. Further reflection has revealed that the differences in opinion may start with the different disciplines in which we work: evolutionary ecology for Hendry and community ecology for Gonzalez. In the present paper, we each present devastating evidence supporting our own position and thus refuting that of the other. We then identify the critical differences that led to such opposing views. We close by combining our two perspectives into a common framework based on the adaptive landscape, and thereby suggest means by which to assess the prevalence and strength of adaptation.

Keywords

Adaptive divergence Adaptive radiation Adaptive landscape Contemporary evolution Ecological speciation Source–sink dynamics Metapopulation Metacommunities Coevolution Gene flow Constraint 

Notes

Acknowledgements

The motivation for this paper was a multi-day argument between Hendry and Gonzalez whilst teaching in a McGill University field course at the Gault Nature Reserve in Québec, Canada. Our fellow teachers, Irene Gregory-Eaves and Gregor Fussmann, happily added fuel to the fire. Additional helpful comments were provided by Graham Bell, Bernie Crespi, Michel Loreau, Joe Hereford, Gene Hunt, Dolph Schluter, and members of the Hendry lab.

References

  1. Arnold SJ, Pfrender ME, Jones AG (2001) The adaptive landscape as a bridge between micro- and macroevolution. Genetica 112–113:9–32. doi: 10.1023/A:1013373907708 Google Scholar
  2. Barton N, Partridge L (2000) Limits to natural selection. Bioessays 22:1075–1084. doi :10.1002/1521-1878(200012)22:12<1075::AID-BIES5>3.0.CO;2-MGoogle Scholar
  3. Bell G (2001) Neutral macroecology. Science 293:2413–2418. doi: 10.1126/science.293.5539.2413 Google Scholar
  4. Bell G (2008) Selection: the mechanism of evolution, 2nd edn. Oxford University Press, Oxford, UKGoogle Scholar
  5. Benkman CW (2003) Divergent selection drives the adaptive radiation of crossbills. Evol Int J Org Evol 57:1176–1181Google Scholar
  6. Berry RJ (1964) The evolution of an island population of the house mouse. Evol Int J Org Evol 18:468–483. doi: 10.2307/2406357 Google Scholar
  7. Bolnick DI, Nosil P (2007) Natural selection in populations subject to migration load. Evol Int J Org Evol 61:2229–2243. doi: 10.1111/j.1558-5646.2007.00179.x Google Scholar
  8. Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81–83. doi: 10.1038/nature04539 Google Scholar
  9. Brandon R (1990) Adaptation and environment. Princeton University Press, PrincetonGoogle Scholar
  10. Burt A (1995) The evolution of fitness. Evol Int J Org Evol 49:1–8. doi: 10.2307/2410288 Google Scholar
  11. Byars SG, Papst W, Hoffmann AA (2007) Local adaptation and cogradient selection in the alpine plant, Poa hiemata, along a narrow altitudinal gradient. Evol Int J Org Evol 61:2925–2941. doi: 10.1111/j.1558-5646.2007.00248.x Google Scholar
  12. Case TJ, Taper ML (2000) Interspecific competition, environmental gradients, gene flow, and the coevolution of species’ borders. Am Nat 155:583–605. doi: 10.1086/303351 Google Scholar
  13. Caswell H (1976) Community structure: a neutral model analysis. Ecol Monogr 46:327–354. doi: 10.2307/1942257 Google Scholar
  14. Charlesworth B, Lande R, Slatkin M (1982) A neo-Darwinian commentary on macroevolution. Evol Int J Org Evol 36:474–498. doi: 10.2307/2408095 Google Scholar
  15. Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago Press, ChicagoGoogle Scholar
  16. Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366. doi: 10.1146/annurev.ecolsys.31.1.343 Google Scholar
  17. Cox GW (2004) Alien species and evolution. Island Press, WashingtonGoogle Scholar
  18. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, SunderlandGoogle Scholar
  19. Crespi BJ (2000) The evolution of maladaptation. Heredity 84:623–629. doi: 10.1046/j.1365-2540.2000.00746.x Google Scholar
  20. Dieckmann U, Ferrière R (2004) Adaptive dynamics and evolving biodiversity. In: Ferrière R, Dieckmann U, Couvet D (eds) Evolutionary conservation biology. Cambridge University Press, Cambridge, UK, pp 188–224Google Scholar
  21. Dieckmann U, Doebeli M, Metz JAJ, Tautz D (2004) Adaptive speciation. Cambridge University Press, CambridgeGoogle Scholar
  22. Endler JA (1986) Natural selection in the wild. Princeton University Press, PrincetonGoogle Scholar
  23. Estes S, Arnold SJ (2007) Resolving the paradox of stasis: models with stabilizing selection explain evolutionary divergence on all timescales. Am Nat 169:227–244. doi: 10.1086/510633 Google Scholar
  24. Facon B, Genton BJ, Shykoff J, Jarne P, Estoup A, David P (2006) A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol Evol 21:130–135. doi: 10.1016/j.tree.2005.10.012 Google Scholar
  25. Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford, UKGoogle Scholar
  26. Frank S (2007) Maladaptation and the paradox of robustness in evolution. PLoS One 10:e1021Google Scholar
  27. Funk DJ, Nosil P, Etges WJ (2006) Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proc Natl Acad Sci USA 103:3209–3213. doi: 10.1073/pnas.0508653103 Google Scholar
  28. Fussmann GF, Loreau M, Abrams PA (2007) Eco-evolutionary dynamics of communities and ecosystems. Funct Ecol 21:465–477. doi: 10.1111/j.1365-2435.2007.01275.x Google Scholar
  29. Gaggiotti OE, Smouse PE (1996) Stochastic migration and maintenance of genetic variation in sink populations. Am Nat 147:919–945. doi: 10.1086/285886 Google Scholar
  30. Gandon S, Michalakis Y (2002) Local adaptation, evolutionary potential and host parasite coevolution: interactions between migration, mutation, population size and generation time. J Evol Biol 15:451–462. doi: 10.1046/j.1420-9101.2002.00402.x Google Scholar
  31. Gandon S, Ebert D, Olivieri I, Michalakis Y (1998) Differential adaptation in spatially heterogeneous environments and host-parasite coevolution. In: Mopper S, Strauss SY (eds) Genetic structure and local adaptation in natural insect populations: effects of ecology, life history ad behavior. Chapman and Hall, New York, pp 325–342Google Scholar
  32. Garant D, Forde SE, Hendry AP (2007) The multifarious effects of dispersal and gene flow on contemporary adaptation. Funct Ecol 21:434–443. doi: 10.1111/j.1365-2435.2006.01228.x Google Scholar
  33. García-Ramos G, Kirkpatrick M (1997) Genetic models of adaptation and gene flow in peripheral populations. Evol Int J Org Evol 51:21–28. doi: 10.2307/2410956 Google Scholar
  34. García-Ramos G, Rodríguez D (2002) Evolutionary speed of species invasions. Evol Int J Org Evol 56:661–668. doi: 10.1554/0014-3820(2002)056[0661:ESOSI]2.0.CO;2 Google Scholar
  35. Gienapp P, Teplitsky C, Alho JS, Mills JA, Merilä J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178Google Scholar
  36. Gillespie JH (1991) The causes of molecular evolution. Oxford Univ Press, OxfordGoogle Scholar
  37. Gonzalez A, Holt RD (2002) The inflationary effects of environmental fluctuations in source–sink systems. Proc Natl Acad Sci USA 99:14872–14877. doi: 10.1073/pnas.232589299 Google Scholar
  38. Gonzalez A, Lawton JH, Gilbert FS, Blackburn TM, Evans-Freke I (1998) Metapopulation dynamics, abundance and distribution in a microecosystem. Science 281:2045–2047. doi: 10.1126/science.281.5385.2045 Google Scholar
  39. Gould SJ (2002) The structure of evolutionary theory. The Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  40. Gould SJ, Lewontin RC (1979) The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B Biol Sci 205:581–598. doi: 10.1098/rspb.1979.0086 CrossRefGoogle Scholar
  41. Grant PR, Grant BR (2002) Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296:707–711. doi: 10.1126/science.1070315 Google Scholar
  42. Gyllenberg M, Parvinen K (2001) Necessary and sufficient conditions for evolutionary suicide. Bull Math Biol 63:981–993. doi: 10.1006/bulm.2001.0253 Google Scholar
  43. Hairston NG Jr, Ellner SP, Geber MA, Yoshida T, Fox JA (2005) Rapid evolution and the convergence of ecological and evolutionary time. Ecol Lett 8:1114–1127. doi: 10.1111/j.1461-0248.2005.00812.x Google Scholar
  44. Haldane JBS (1930) A mathematical theory of natural and artificial selection. VI. Isolation. Proc Camb Philos Soc 26:220–230Google Scholar
  45. Haldane JBS (1956) The relation between density regulation and natural selection. Proc R Soc Lond B Biol Sci 145:306–308. doi: 10.1098/rspb.1956.0039 Google Scholar
  46. Hansen TF (1997) Stabilizing selection and the comparative analysis of adaptation. Evol Int J Org Evol 51:1341–1351. doi: 10.2307/2411186 Google Scholar
  47. Hansen TF, Carter AJR, Pélabon C (2006) On adaptive accuracy and precision in natural populations. Am Nat 168:168–181. doi: 10.1086/505768 Google Scholar
  48. Hanski I, Saccheri I (2006) Molecular-level variation affects population growth in a butterfly metapopulation. PLoS Biol 4:e129. doi: 10.1371/journal.pbio.0040129 Google Scholar
  49. Hendry AP (2005) The power of natural selection. Nature 433:694–695. doi: 10.1038/433694a Google Scholar
  50. Hendry AP, Kinnison MT (1999) The pace of modern life: measuring rates of contemporary microevolution. Evol Int J Org Evol 53:1637–1653. doi: 10.2307/2640428 Google Scholar
  51. Hendry AP, Taylor EB (2004) How much of the variance in adaptive divergence can be explained by gene flow? An evaluation using lake-stream stickleback pairs. Evol Int J Org Evol 58:2319–2331Google Scholar
  52. Hendry AP, Nosil P, Rieseberg LH (2007) The speed of ecological speciation. Funct Ecol 21:455–464. doi: 10.1111/j.1365-2435.2007.01240.x Google Scholar
  53. Hendry AP, Farrugia TJ, Kinnison MT (2008) Human influences on rates of phenotypic change in wild animal populations. Mol Ecol 17:20–29Google Scholar
  54. Hereford J, Hansen TF, Houle D (2004) Comparing strengths of directional selection: how strong is strong? Evol Int J Org Evol 58:2133–2143Google Scholar
  55. Hersch EI, Phillips PC (2004) Power and potential bias in field studies of natural selection. Evol Int J Org Evol 58:479–485Google Scholar
  56. Hoeksema JD, Forde SE (2008) A meta-analysis of factors affecting local adaptation between interaction species. Am Nat 171:275–290. doi: 10.1086/527496 Google Scholar
  57. Holt RD (1985) Population dynamics in two-patch environments: some anomalous consequences of an optimal habitat distribution. Theor Popul Biol 28:181–208. doi: 10.1016/0040-5809(85)90027-9 Google Scholar
  58. Holt RD, Gomulkiewicz R (1997) How does immigration influence local adaptation? A reexamination of a familiar paradigm. Am Nat 149:563–572. doi: 10.1086/286005 Google Scholar
  59. Holt RD, Gomulkiewicz R (2004) Conservation implications of niche conservatism and evolution in heterogeneous environments. In: Ferrière R, Dieckmann U, Couvet D (eds) Evolutionary conservation biology. Cambridge University Press, Cambridge, UK, pp 244–264Google Scholar
  60. Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton, NJGoogle Scholar
  61. Hunt G (2007) The relative importance of directional change, random walks, and stasis in the evolution of fossil lineages. Proc Natl Acad Sci USA 104:18404–18408. doi: 10.1073/pnas.0704088104 Google Scholar
  62. Hunt G, Bell MA, Travis MP (2008) Evolution toward a new adaptive optimum: phenotypic evolution in a fossil stickleback lineage. Evol Int J Org Evol . doi: 10.1111/j.1558-5646.2007.00310.x Google Scholar
  63. Jain SK, Bradshaw AD (1966) Evolutionary divergence among adjacent plant populations. I. The evidence and its theoretical analysis. Heredity 21:407–441. doi: 10.1038/hdy.1966.42 Google Scholar
  64. Johnston RF, Selander RK (1964) House sparrows: rapid evolution of races in North America. Science 144:548–550. doi: 10.1126/science.144.3618.548 Google Scholar
  65. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. doi: 10.1111/j.1461-0248.2004.00684.x Google Scholar
  66. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge, UKGoogle Scholar
  67. Kingsolver JG, Pfennig DW (2007) Patterns and power of phenotypic selection in nature. Bioscience 57:561–572. doi: 10.1641/B570706 Google Scholar
  68. Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SN, Hill CE et al (2001) The strength of phenotypic selection in natural populations. Am Nat 157:245–261. doi: 10.1086/319193 Google Scholar
  69. Kinnison MT, Hairston NG Jr (2007) Eco-evolutionary conservation biology: contemporary evolution and the dynamics of persistence. Funct Ecol 21:444–454. doi: 10.1111/j.1365-2435.2007.01278.x Google Scholar
  70. Kinnison MT, Hendry AP (2001) The pace of modern life II: from rates of contemporary microevolution to pattern and process. Genetica 112–113:145–164. doi: 10.1023/A:1013375419520 Google Scholar
  71. Kinnison MT, Unwin MJ, Quinn TP (2008) Eco-evolutionary versus habitat contributions to invasion in salmon: experimental evaluation in the wild. Mol Ecol 17:405–414Google Scholar
  72. Kirkpatrick M, Barton NH (1997) Evolution of a species’ range. Am Nat 150:1–23. doi: 10.1086/286054 Google Scholar
  73. Knapcyzk FN, Conner JK (2007) Estimates of the average strength of natural selection are not inflated by sampling error or publication bias. Am Nat 170:501–508. doi: 10.1086/521239 Google Scholar
  74. Lack D (1947) Darwin’s finches. Cambridge University Press, Cambridge, UKGoogle Scholar
  75. Lande R, Shannon S (1996) The role of genetic variation in adaptation and population persistence in a changing environment. Evol Int J Org Evol 50:434–437. doi: 10.2307/2410812 Google Scholar
  76. Leigh EG Jr (2007) Neutral theory: a historical perspective. J Evol Biol 20:2075–2091. doi: 10.1111/j.1420-9101.2007.01410.x Google Scholar
  77. Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189. doi: 10.1016/S0169-5347(02)02497-7 Google Scholar
  78. Lenski RE, Travasino M (1994) Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc Natl Acad Sci USA 91:6808–6814. doi: 10.1073/pnas.91.15.6808 Google Scholar
  79. Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Inv 8:1535–1545. doi: 10.1007/s10530-005-5845-y Google Scholar
  80. Matsuda H, Abrams PA (1994) Timid consumers: self-extinction due to adaptive change in foraging and anti-predator effort. Theor Popul Biol 45:76–91. doi: 10.1006/tpbi.1994.1004 Google Scholar
  81. Matthews DP, Gonzalez A (2007) The inflationary effects of environmental fluctuations ensure the persistence of sink metapopulations. Ecology 88:2848–2856. doi: 10.1890/06-1107.1 Google Scholar
  82. Moore J-S, Gow JL, Taylor EB, Hendry AP (2007) Quantifying the constraining influence of gene flow on adaptive divergence in the lake-stream threespine stickleback system. Evol Int J Org Evol 61:2015–2026. doi: 10.1111/j.1558-5646.2007.00168.x Google Scholar
  83. Mouquet N, Loreau M (2002) Coexistence in metacommunities: the regional similarity hypothesis. Am Nat 159:420–426. doi: 10.1086/338996 Google Scholar
  84. Nagy ES (1997) Selection for native characters in hybrids between two locally adapted plant subspecies. Evol Int J Org Evol 51:1469–1480. doi: 10.2307/2411199 Google Scholar
  85. Nesse RM (2005) Maladaptation and natural selection. Q Rev Biol 80:62–70. doi: 10.1086/431026 Google Scholar
  86. Nuismer SL, Gandon S (2008) Moving beyond common-garden and transplant designs: insight into the causes of local adaptation in species interactions. Am Nat 171:658–668. doi: 10.1086/587077 Google Scholar
  87. O’Neil P (1999) Selection on flowering time: an adaptive fitness surface for nonexistent character combinations. Ecology 80:806–820Google Scholar
  88. Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461. doi: 10.1126/science.1121407 Google Scholar
  89. Pease CPR, Lande R, Bull JJ (1989) A model of population growth, dispersal, and evolution in a changing environment. Ecology 70:1644–1657. doi: 10.2307/1938100 Google Scholar
  90. Pelletier F, Clutton-Brock T, Pemberton J, Tuljapurkar S, Coulson T (2007) The evolutionary demography of ecological change: linking trait variation and population growth. Science 315:1571–1574. doi: 10.1126/science.1139024 Google Scholar
  91. Phillips PA, Arnold SJ (1989) Visualizing multivariate selection. Evol Int J Org Evol 43:1209–1220. doi: 10.2307/2409357 Google Scholar
  92. Phillips BL, Brown GP, Webb JK, Shine R (2006) Invasion and the evolution of speed in toads. Nature 439:803. doi: 10.1038/439803a Google Scholar
  93. Reznick DN, Ghalambor CK (2001) The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112–113:183–198. doi: 10.1023/A:1013352109042 Google Scholar
  94. Reznick DN, Shaw FH, Rodd FH, Shaw RG (1997) Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275:1934–1937. doi: 10.1126/science.275.5308.1934 Google Scholar
  95. Ricciardi A, Ward JM (2006) Comment on “Opposing effects of native and exotic herbivores on plant invasions”. Science 313:298aGoogle Scholar
  96. Riechert SE (1993) Investigation of potential gene flow limitation of behavioral adaptation in an aridlands spider. Behav Ecol Sociobiol 32:355–363Google Scholar
  97. Rose MR, Lauder GV (1996) Adaptation. Academic Press, New YorkGoogle Scholar
  98. Rosenzweig ML (1973) Evolution of the predator isocline. Evol Int J Org Evol 27:84–94. doi: 10.2307/2407121 Google Scholar
  99. Roy M, Holt RD, Barfield M (2005) Temporal autocorrelation can enhance the persistence and abundance of metapopulations comprised of coupled sinks. Am Nat 166:246–261. doi: 10.1086/431286 Google Scholar
  100. Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352. doi: 10.1111/j.1461-0248.2004.00715.x Google Scholar
  101. Saccheri I, Hanski I (2006) Natural selection and population dynamics. Trends Ecol Evol 21:341–347. doi: 10.1016/j.tree.2006.03.018 Google Scholar
  102. Sax DF, Brown JH (2000) The paradox of invasion. Glob Ecol Biogeogr 9:363–371. doi: 10.1046/j.1365-2699.2000.00217.x Google Scholar
  103. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford, UKGoogle Scholar
  104. Schluter D, Grant PR (1984) Determinants of morphological patterns in communities of Darwin’s finches. Am Nat 123:175–196. doi: 10.1086/284196 Google Scholar
  105. Sheets HD, Mitchell CE (2001) Why the null matters: statistical tests, random walks and evolution. Genetica 112–113:105–125. doi: 10.1023/A:1013308409951 Google Scholar
  106. Simpson GG (1944) Tempo and mode in evolution. Columbia University Press, New YorkGoogle Scholar
  107. Simpson GG (1953) The major features of evolution. Columbia University Press, New YorkGoogle Scholar
  108. Slatkin M, Maynard Smith J (1979) Models of coevolution. Q Rev Biol 54:233–266. doi: 10.1086/411294 Google Scholar
  109. Stearns SC, Sage RD (1980) Maladaptation in a marginal population of the mosquito fish, Gambusia affinis. Evol Int J Org Evol 34:65–75. doi: 10.2307/2408315 Google Scholar
  110. Svensson E, Sinervo B (2000) Experimental excursions on adaptive landscapes: density-dependent selection on egg size. Evol Int J Org Evol 54:1396–1403Google Scholar
  111. Thompson JN, Nuismer SL, Gomulkiewicz R (2002) Coevolution and maladaptation. Integr Comp Biol 42:381–387. doi: 10.1093/icb/42.2.381 Google Scholar
  112. Urban MC (2006) Maladaptation and mass effects in a metacommunity: consequences for species coexistence. Am Nat 168:28–40. doi: 10.1086/505159 Google Scholar
  113. Vellend M, Geber MA (2005) Connections between species diversity and genetic diversity. Ecol Lett 8:767–781. doi: 10.1111/j.1461-0248.2005.00775.x Google Scholar
  114. Virgl JA, Messier F (2000) Assessment of source–sink theory for predicting demographic rates among habitats that exhibit temporal changes in quality. Can J Zool 78:1483–1493. doi: 10.1139/cjz-78-8-1483 Google Scholar
  115. Webb C (2003) A complete classification of Darwinian extinction in ecological interactions. Am Nat 161:181–205. doi: 10.1086/345858 Google Scholar
  116. Williams GC (1966) Adaptation and natural selection. Princeton University Press, PrincetonGoogle Scholar
  117. Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666. doi: 10.2307/2265769 Google Scholar
  118. Yoshida T, Jones LE, Ellner SP, Fussmann GF, Hairston NG Jr (2003) Rapid evolution drives ecological dynamics in a predator-prey system. Nature 424:303–306. doi: 10.1038/nature01767 Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Redpath Museum and Department of BiologyMcGill UniversityMontrealCanada
  2. 2.Department of BiologyMcGill UniversityMontrealCanada

Personalised recommendations