A heuristic model on the role of plasticity in adaptive evolution: Plasticity increases adaptation, population viability and genetic variation

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1771, 2013, Pages

  Gomez Mestre, Ivan ^a   Jovani, Roger ^a  

^a DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

Author keywords

Adaptation; Bottleneck; Developmental plasticity; Genetic accommodation; Genetic variation; Heterogeneous environment

Indexed keywords

ADAPTATION; ENVIRONMENTAL CUE; GENE EXPRESSION; GENETIC VARIATION; HERITABILITY; HEURISTICS; PHENOTYPIC PLASTICITY; POPULATION VIABILITY ANALYSIS;

EID: 84884583442     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.1869     Document Type: Article

References (69)

1. Futuyma DJ. 2009 Evolution. Sunderland, MA: Sinauer Associates.
2. Moczek AP. 2007 Developmental capacitance, genetic accommodation, and adaptive evolution. Evol. Dev. 9, 299-305. (doi:10.1111/j.1525-142X. 2007.00162.x)
3. Pigliucci M, Müller GB. 2010 Elements of an extended evolutionary synthesis. In Evolution: the extended synthesis (eds M Pigliucci, GB Müller), pp. 3-17. Cambridge, MA: MIT Press.
4. Gillespie JH, Turelli M. 1989 Genotype-environment interactions and the maintenance of polygenic variation. Genetics 121, 129-138.
5. Byers DL. 2005 Evolution in heterogeneous environments and the potential of maintenance of genetic variation in traits of adaptive significance. Genetica 123, 107-124. (doi:10.1007/s10709-003-2721-5)
6. Barrett RDH, Schluter D. 2008 Adaptation from standing genetic variation. Trends Ecol. Evol. 23, 38-44. (doi:10.1016/j.tree.2007.09.008)
7. West-Eberhard MJ. 2003 Developmental plasticity and evolution, p. 794. Oxford, UK: Oxford University Press.
8. Pigliucci M. 2001 Phenotypic plasticity: beyond nature and nurture, p. 384. Baltimore, MA: Johns Hopkins University Press.
9. Cabej NR. 2012 Epigenetic principles of evolution. London, UK: Elsevier.
10. Aubin-Horth N, Renn SCP. 2009 Genomic reaction norms: using integrative biology to understand molecular mechanisms of phenotypic plasticity. Mol. Ecol. 18, 3763-3780. (doi:10.1111/j.1365-294X. 2009.04313.x)
11. Sultan SE, Spencer HG. 2002 Metapopulation structure favors plasticity over local adaptation. Am. Nat. 160, 271-283. (doi:10.1086/341015)
12. Scheiner SM, Barfield M, Holt RD. 2012 The genetics of phenotypic plasticity. XI. Joint evolution of plasticity and dispersal rate. Ecol. Evol. 2, 2027-2039. (doi:10.1002/ece3.327)
13. Hallsson LR, Björklund M. 2012 Selection in a fluctuating environment leads to decreased genetic variation and facilitates the evolution of phenotypic plasticity. J. Evol. Biol. 25, 1275-1290. (doi:10. 1111/j.1420-9101.2012.02512.x)
14. Roff DA. 1997 Evolutionary quantitative genetics. New York, NY: Chapman & Hall.
15. Losos JB et al. 2013 Evolutionary Biology for the 21st Century. PLoS Biol. 11, e1001466. (doi:10.1371/journal.pbio.1001466)
16. West-Eberhard MJ. 2002 Development and selection in adaptive evolution. Trends Ecol. Evol. 17, 65. (doi:10.1016/S0169-5347(01)02413-2)
17. Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP. 2010 Phenotypic plasticity's impacts on diversification and speciation. Trends Ecol. Evol. 25, 459-467. (doi:10.1016/j.tree. 2010.05.006)
18. Moczek AP, Sultan S, Foster S, Ledon-Rettig C, Dworkin I, Nijhout HF, Abouheif E, Pfennig DW. 2011 The role of developmental plasticity in evolutionary innovation. Proc. R. Soc. B 278, 2705-2713. (doi:10.1098/rspb.2011.0971)
19. Ancel LW. 1999 A quantitative model of the Simpson - Baldwin effect. J. Theor. Biol. 196, 197-209. (doi:10.1006/jtbi.1998.0833)
20. Berrigan D, Scheiner SM. 2004 Modeling the evolution of phenotypic plasticity. In Phenotypic plasticity (eds TJ DeWitt, SM Scheiner), pp. 82-97. Oxford, UK: Oxford University Press.
21. de Jong G. 2005 Evolution of phenotypic plasticity: patterns of plasticity and the emergence of ecotypes. New Phytol. 166, 101-118. (doi:10.1111/j.1469-8137.2005.01322.x)
22. Lande R. 2009 Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J. Evol. Biol. 22, 1435-1446. (doi:10.1111/j.1420-9101.2009.01754.x)
23. DeWitt TJ, Sih A, Wilson DS. 1998 Costs and limits of phenotypic plasticity. Trends Ecol. Evol. 13, 77-81. (doi:10.1016/S0169-5347(97)01274-3)
24. Auld JR, Agrawal AA, Relyea RA. 2009 Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc. R. Soc. B 277, 503-511. (doi:10. 1098/rspb.2009.1355)
25. Pigliucci M, Murren CJ. 2003 Genetic assimilation and a possible evolutionary paradox: can macroevolution sometimes be so fast as to pass us by? Evolution 57, 1455-1464.
26. Crispo E. 2007 The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution 61, 2469-2479. (doi:10.1111/j. 1558-5646.2007.00203.x)
27. Foster SA, Wund MA. 2011 Epigenetic contributions to adaptive radiations: insights from threespine sticklebacks. In Epigenetics linking genotype and phenotype in development and evolution (eds B Hallgrimsson, BK Hall), pp. 317-336. Berkeley, CA: University of California Press.
28. Waddington CH. 1952 Selection of the genetic basis for an acquired character. Nature 169, 278. (doi:10.1038/169278a0)
29. Waddington CH. 1959 Canalization of development and the inheritance of acquired characters. Nature 183, 1654-1655. (doi:10.1038/1831654a0)
30. Suzuki Y, Nijhout HF. 2006 Evolution of a polyphenism by genetic accommodation. Science 311, 650-652. (doi:10.1126/science. 1118888)
31. Gomez-Mestre I, Buchholz DR. 2006 Developmental plasticity mirrors differences among taxa in spadefoot toads linking plasticity and diversity. Proc. Natl Acad. Sci. USA 103, 19 021-19 026. (doi:10. 1073/pnas.0603562103)
32. Ledon-Rettig CC, Pfennig DW, Nascone-Yoder N. 2008 Ancestral variation and the potential for genetic accommodation in larval amphibians: implications for the evolution of novel feeding strategies. Evol. Dev. 10, 316-325. (doi:10.1111/j. 1525-142X.2008.00240.x)
33. Simpson GG. 1953 The Baldwin effect. Evolution 7, 110-117. (doi:10.2307/2405746)
34. Orr HA. 1999 Evolutionary biology: an evolutionary dead end? Science 285, 343-344. (doi:10.1126/science.285.5426.343)
35. Jablonka E, Lamb MJ. 2010 Transgenerational epigenetic inheritance. In Evolution: the extended synthesis (eds M Pigliucci, GB Müller), pp. 137-174. Cambridge, MA: The MIT Press.
36. Holeski LM, Jander G, Agrawal AA. 2012 Transgenerational defense induction and epigenetic inheritance in plants. Trends Ecol. Evol. 27, 618-626. (doi:10.1016/j.tree.2012.07.011)
37. Grimm V, Railsback SF. 2005 Individual-based modeling and ecology. Princeton, NJ: Princeton University Press.
38. Grimm V et al. 2006 A standard protocol for describing individual-based and agent-based models. Ecol. Model. 198, 115-126. (doi:10.1016/j. ecolmodel.2006.04.023)
39. Grimm V, Berger U, DeAngelis DL, Polhill JG, Giske J, Railsback SF. 2010 The ODD protocol: a review and first update. Ecol. Model. 221, 2760-2768. (doi:10. 1016/j.ecolmodel.2010.08.019)
40. Wilensky U. 1999 NetLogo. Center for Connected Learning and Computer-Based Modeling, Northwestern University, Evanston, IL, USA. See http://ccl.northwestern.edu/netlogo.
41. Scheiner SM. 1998 The genetics of phenotypic plasticity. VII. Evolution in a spatially-structured environment. J. Evol. Biol. 11, 303-320.
42. Chevin LM, Lande R. 2011 Adaptation to marginal habitats by evolution of increased phenotypic plasticity. J. Evol. Biol. 24, 1462-1476. (doi:10. 1111/j.1420-9101.2011.02279.x)
43. Scheiner SM, Holt RD. 2012 The genetics of phenotypic plasticity. X. Variation versus uncertainty. Ecol. Evol. 2, 751-767. (doi:10.1002/ece3.217)
44. Davidson AM, Jennions M, Nicotra AB. 2011 Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecol. Lett. 14, 419-431. (doi:10. 1111/j.1461-0248.2011.01596.x)
45. Scoville AG, Pfrender ME. 2010 Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proc. Natl Acad. Sci. USA 107, 4260-4263. (doi:10.1073/pnas.0912748107)
46. Charmantier A, McCleery RH, Cole LR, Perrins C, Kruuk LEB, Sheldon BC. 2008 Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800-803. (doi:10. 1126/science.1157174)
47. Draghi JA, Whitlock MC. 2012 Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolution 66, 2891-2902. (doi:10.1111/j. 1558-5646.2012.01649.x)
48. Price TD, Qvarnstrom A, Irwin DE. 2003 The role of phenotypic plasticity in driving genetic evolution. Proc. R. Soc. Lond. B 270, 1433-1440. (doi:10. 1098/rspb.2003.2372)
49. Ghalambor CK, McKay JK, Carroll SP, Reznick DN. 2007 Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21, 394-407. (doi:10.1111/j.1365-2435.2007.01283.x)
50. Flatt T. 2005 The evolutionary genetics of canalization. Q. Rev. Biol. 80, 287-316. (doi:10. 1086/432265)
51. Gibson G, Dworkin I. 2004 Uncovering cryptic genetic variation. Nat. Rev. Genet. 5, 681-690. (doi:10.1038/nrg1426)
52. Le Rouzic A, Carlborg N. 2008 Evolutionary potential of hidden genetic variation. Trends Ecol. Evol. 23, 33-37. (doi:10.1016/j.tree.2007.09.014)
53. West-Eberhard MJ. 1989 Phenotypic plasticity and the origins of diversity. Annu. Rev. Ecol. Syst. 20, 249-278. (doi:10.1146/annurev.es.20.110189. 001341)
54. Wund M, Baker JA, Clancy B, Golub JL, Foster SA. 2008 A test of the 'Flexible Stem' model of evolution: ancestral plasticity, genetic accommodation, and morphological divergence in the threespine stickleback radiation. Am. Nat. 172, 449-462. (doi:10.1086/590966)
55. Wund MA, Valena S, Wood S, Baker JA. 2012 Ancestral plasticity and allometry in threespine stickleback reveal phenotypes associated with derived, freshwater ecotypes. Biol. J. Linn. Soc. 105, 573-583. (doi:10.1111/j.1095-8312.2011. 01815.x)
56. Losos JB, Creer DA, Glossip D, Goellner R, Hampton A, Roberts G, Haskell N, Taylor P, Ettling J. 2000 Evolutionary implications of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei. Evolution 54, 301-305.
57. Adams CE, Huntingford FA. 2004 Incipient speciation driven by phenotypic plasticity? Evidence from sympatric populations of Arctic charr. Biol. J. Linn. Soc. 81, 611-618. (doi:10.1111/j. 1095-8312.2004.00314.x)
58. Scheiner SM, Berrigan D. 1998 The genetics of phenotypic plasticity. VIII. The cost of plasticity in Daphnia pulex. Evolution 52, 368-378. (doi:10. 2307/2411074)
59. Johansson F. 2002 Reaction norms and production costs of predator-induced morphological defences in a larval dragonfly (Leucorrhinia dubia: Odonata). Can. J. Zool. 80, 944-950. (doi:10.1139/z02-073)
60. Van Buskirk J, Steiner UK. 2009 The fitness costs of developmental canalization and plasticity. J. Evol. Biol. 22, 852-860. (doi:10.1111/j.1420-9101.2009.01685.x)
61. DeWitt TJ. 1998 Costs and limits of phenotypic plasticity: tests with predator-induced morphology and life history in a freshwater snail. J. Evol. Biol. 11, 465-480. (doi:10.1007/s000360050100)
62. Agrawal AA, Conner JK, Johnson MTJ, Wallsgrove R. 2002 Ecological genetics of an induced plant defense against herbivores: additive genetic variance and costs of phenotypic plasticity. Evolution 56, 2206-2213.
63. Relyea RA. 2002 Costs of phenotypic plasticity. Am. Nat. 159, 272-282. (doi:10.1086/338540)
64. Kulkarni SS, Gomez-Mestre I, Moskalik CL, Storz BL, Buchholz DR. 2011 Evolutionary reduction of developmental plasticity in desert spadefoot toads. J. Evol. Biol. 24, 2445-2455. (doi:10.1111/j.1420-9101.2011.02370.x)
65. Ricklefs RE, Schluter D. 1993 Species diversity in ecological communities: historical and geographical perspectives. Chicago, IL: University of Chicago Press.
66. Scheiner SM. 1993 Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst. 24, 35-68. (doi:10.1146/annurev.es.24.110193.000343)
67. Bossdorf O, Richards CL, Pigliucci M. 2008 Epigenetics for ecologists. Ecol. Lett. 11, 106-115.
68. Carroll SB. 2008 Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134, 25-36. (doi:10. 1016/j.cell.2008.06.030)
69. Richards CL, Bossdorf O, Pigliucci M. 2010 What role does heritable epigenetic variation play in phenotypic evolution? BioScience 60, 232-237. (doi:10.1525/bio.2010.60.3.9)