The evolutionary genetics of canalization

Quarterly Review of Biology

Volumn 80, Issue 3, 2005, Pages 287-316

  Flatt, Thomas ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Canalization; Constraint; Epistasis; Genetic architecture; Genetic assimilation; Genetic variance; Genotype by environment interaction; Genotype phenotype map; Phenotypic plasticity; Phenotypic variance; Selection

Indexed keywords

ANIMAL; BIOLOGICAL MODEL; GENOTYPE; HUMAN; MOLECULAR EVOLUTION; PHENOTYPE; REVIEW;

ANIMALS; EVOLUTION, MOLECULAR; GENOTYPE; HUMANS; MODELS, GENETIC; PHENOTYPE;

EID: 25144508573     PISSN: 00335770     EISSN: None     Source Type: Journal    
DOI: 10.1086/432265     Document Type: Review

References (197)

1. Agur Z, Kerszberg M. 1987. The emergence of phenotypic novelties through progressive genetic change. American Naturalist 129:862-875.
2. Ancel L W, Fontana W. 2000. Plasticity, evolvability, and modularity in RNA. Journal of Experimental Zoology Part B: Molecular and Developmental Evolutions 288(3):242-283.
3. Ancel Meyers L, Bull J J. 2002. Fighting change with change: adaptive variation in an uncertain world. Trends in Ecology and Evolution 17:551-557.
4. Arnone M I, Davidson E H. 1997. The hardwiring of development: organization and function of genomic regulatory systems. Development 124:1851-1864.
5. Barkai N, Leibler S. 1997. Robustness in simple biochemical networks. Nature 387:913-917.
6. Barton N H, Charlesworth B. 1998. Why sex and recombination? Science 281:1986-1990.
7. Basson M E, Thorsness M, Rine J. 1986. Saccharomyces cerevisiae contains two functional genes encoding 3-hydroxy-3-methylglutaryl-coenzyme A reductase. Proceedings of the National Academy of Sciences USA 83:5563-5567.
8. Becskei A, Serrano L. 2000. Engineering stability in gene networks by autoregulation. Nature 405:590-593.
9. Bergman A, Siegal M L. 2003. Evolutionary capacitance as a general feature of complex gene networks. Nature 424:549-552.
10. Bernard C. 1865. Introduction à l'Étude de la Médecine Expérimentale. Paris: Baillière.
11. Translated by H C Green. 1957. An Introduction to the Study of Experimental Medicine. New York: Dover Publications.
12. Bernoulli D. 1738. Specimen theoriae novae de mensura sortis. Commentarii Academiae Scientiarum Imperialis Petropolitanae 5:175-192.
13. Translated by L Sommer. 1954. Exposition of a new theory on the measurement of risk. Econometrica 22:23-36.
14. Bhalla U S, Iyengar R. 1999. Emergent properties of networks of biological signaling pathways. Science 283:381-387.
15. Bonner J T. 1988. The Evolution of Complexity by Means of Natural Selection. Princeton (NJ): Princeton University Press.
16. Bornholdt S, Sneppen K. 2000. Robustness as an evolutionary principle. Proceedings of the Royal Society of London B 267:2281-2286.
17. Bradshaw A D. 1991. The Croonian Lecture 1991: Genostasis and the limits of evolution. Philosophical Transactions of the Royal Society of London B 333:289-305.
18. Brodie E D, III. 2000. Why evolutionary genetics does not always add up. Pages 3-19 in Epistasis and the Evolutionary Process, edited by J B Wolf, E D Brodie III, and M J Wade. Oxford and New York: Oxford University Press.
19. Burch C L, Chao L. 2004. Epistasis and its relationship to canalization in the RNA Virus φ6. Genetics 167:559-567.
20. Cannon W B. 1932. The Wisdom of the Body. New York: W. W. Norton.
21. Charlesworth B. 1993. Directional selection and the evolution of sex and recombination. Genetical Research, Cambridge 61:205-224.
22. Charlesworth B. 1998. Adaptive evolution: the struggle for dominance. Current Biology 8:R502-R504.
23. Charlesworth B, Lande R, Slatkin M. 1982. A neo-Darwinian commentary on macroevolution. Evolution 36:474-498.
24. Cheverud J M, Routman E J. 1995. Epistasis and its contribution to genetic variance components. Genetics 139:1455-1461.
25. Clarke G M. 1997. The genetic and molecular basis of developmental stability: the Lucilia story. Trends in Ecology and Evolution 12:89-91.
26. Clarke G M, McKenzie J A. 1987. Developmental stability of insecticide resistant phenotypes in blowfly: a result of canalizing natural selection. Nature 325:345-346.
27. Davies A G, Game A Y, Chen Z, Williams T J, Goodall S, Yen J L, McKenzie J A, Batterham P. 1996. Scalloped wings is the Lucilia cuprina Notch homologue and a candidate for the modifier of fitness and asymmetry of Diazinon resistance. Genetics 143:1321-1337.
28. Davies E K, Peters A D, Keightley P D. 1999. High frequency of cryptic deleterious mutations in Caenorhabditis elegans. Science 285:1748-1751.
29. Debat V, Alibert P, David P, Paradis E, Auffray J-C. 2000. Independence between developmental stability and canalization in the skull of the house mouse. Proceedings of the Royal Society of London B 267:423-430.
30. Debat V, David P. 2001. Mapping phenotypes: canalization, plasticity and developmental stability. Trends in Ecology and Evolution 16:555-561.
31. De Visser J A G M, Hermisson J, Wagner G P, Ancel Meyers L, Bagheri-Chaichian H, et al. 2003. Perspective: evolution and detection of genetic robustness. Evolution 57:1959-1972.
32. Dobzhansky T. 1971. Genetics of the Evolutionary Process. New York: Columbia University Press.
33. Dover G. 2000. How genomic and developmental dynamics affect evolutionary processes. BioEssays 22(12):1153-1159.
34. Dworkin I, Palsson A, Birdsall K, Gibson G. 2003. Evidence that Egfr contributes to cryptic genetic variation for photoreceptor determination in natural populations of Drosophila melanogaster. Current Biology 13(21):1888-1893.
35. Elena S F, Lenski R E. 2001. Epistasis between new mutations and genetic background and a test of genetic canalization. Evolution 55:1746-1752.
36. Eshel I, Matessi C. 1998. Canalization, genetic assimilation and preadaptation: a quantitative genetic model. Genetics 149:2119-2133.
37. Falconer D S, Mackay T F C. 1996. Introduction to Quantitative Genetics. Fourth Edition. New York: Prentice Hall.
38. Falk R. 2001. Can the norm of reaction save the gene concept? Pages 119-140 in Thinking about Evolution: Historical, Philosophical, and Political Perspectives, edited by R S Singh, C B Krimbas, D B Paul, and J Beatty. Cambridge: Cambridge University Press.
39. Fares M A, Ruiz-González M X, Moya A, Elena S F, Barrio E. 2002. GroEL buffers against deleterious mutations. Nature 417:398.
40. Fay D S, Han M. 2000. The synthetic multivulval genes of C. elegans: functional redundancy, Ras-antagonism, and cell fate determination. Genesis 26:279-284.
41. Felsenstein J. 1976. The theoretical population genetics of variable selection and migration. Annual Review of Genetics 10:253-280.
42. Fenster C B, Galloway L F, Chao L. 1997. Epistasis and its consequences for the evolution of natural populations. Trends in Ecology and Evolution 12:282-286.
43. Ferguson E L, Horvitz H R. 1989. The multivulva phenotype of certain Caenorhabditis elegans mutants results from defects in two functionally redundant pathways. Genetics 123:109-121.
44. Fisher R A. 1930. The Genetical Theory of Natural Selection. Oxford: Clarendon Press. [Reprint. 1999. Oxford and New York: Oxford University Press.]
45. Fontana W, Schuster P. 1998. Continuity in evolution: on the nature of transitions. Science 280:1451-1455.
46. Frank S A. 1999. Population and quantitative genetics of regulatory networks. Journal of Theoretical Biology 197(3):281-294.
47. Gass G L, Bolker J A. 2003. Modularity. Pages 260-267 in Keywords and Concepts in Evolutionary Developmental Biology, edited by B K Hall and W M Olson. Cambrigde (MA): Harvard University Press.
48. Gavrilets S, Hastings A. 1994. A quantitative-genetic model for selection on developmental noise. Evolution 48:1478-1486.
49. Gerhart J, Kirschner M. 1997. Cells, Embryos and Evolution: Toward a Cellular and Developmental Understanding of Phenotypic Variation and Evolutionary Adaptability. Malden (MA): Blackwell Science.
50. Gibson G. 1996. Epistasis and pleiotropy as natural properties of transcriptional regulation. Theoretical Population Biology 49:58-89.
51. Gibson G, Dworkin I. 2004. Uncovering cryptic genetic variation. Nature Reviews Genetics 5:681-690.
52. Gibson G, Hogness D S. 1996. Effect of polymorphism in the Drosophila regulatory gene Ultrabithorax on homeotic stability. Science 271:200-203.
53. Gibson G, van Helden S. 1997. Is function of Drosophila homeotic gene Ultrabithorax canalized? Genetics 147:1155-1168.
54. Gibson G, Wagner G P. 2000. Canalization in evolutionary genetics: a stabilizing theory? BioEssays 22(4):372-380.
55. Gibson G, Wemple M, van Helden S. 1999. Potential variance affecting homeotic Ultrabithorax and Antennapedia phenotypes in Drosophila melanogaster. Genetics 151:1081-1091.
56. Gilbert S F. 2000. Diachronic biology meets evo-devo: C. H. Waddington's approach to evolutionary developmental biology. American Zoologist 40:729-737.
57. Gimelfarb A. 1989. Genotypic variation for a quantitative character maintained under stabilizing selection without mutations: epistasis. Genetics 123:217-228.
58. Goss P J E, Peccoud J. 1998. Quantitative modeling of stochastic systems in molecular biology by using stochastic Petri nets. Proceedings of the National Academy of Sciences USA 95:6750-6755.
59. Gu Z, Steinmetz L M, Gu X, Scharfe C, Davis R M, Li W-H. 2003. Role of duplicate genes in genetic robustness against null mutations. Nature 421:63-66.
60. 1 phase in yeast. Proceedings of the National Academy of Sciences USA 86:6255-6259.
61. Hall B K 1992. Waddington's legacy in development and evolution. American Zoologist 32:113-122.
62. Hall B K. 1999. Evolutionary Developmental Biology. Second Edition. Dordrecht (The Netherlands): Kluwer Academic Publishers.
63. Hall B K, Olson W M, eds. 2003. Keywords and Concepts in Evolutionary Developmental Biology. Cambridge (MA): Harvard University Press.
64. Hallgrímsson B, Willmore K, Hall B K. 2002. Canalization, developmental stability, and morphological integration in primate limbs. Yearbook of Physical Anthropology 45:131-158.
65. Hansen T F, Houle D. 2004. Evolvability, stabilizing selection, and the problem of stasis. Pages 107-129 in The Evolutionary Biology of Complex Phenotypes, edited by M Pigliucci and K Preston. Oxford: Oxford University Press.
66. Hansen T F, Wagner G P. 2001. Modeling genetic architecture: a multilinear theory of gene interaction. Theoretical Population Biology 59:61-86.
67. Hartl D L, Dykhuizen D E, Dean A M. 1985. Limits of adaptation: the evolution of selective neutrality. Genetics 111:655-674.
68. Hartman J L, IV, Garvik B, Hartwell L. 2001. Principles for the buffering of genetic variation. Science 291:1001-1004.
69. Hartwell L H, Hopfield J J, Leibler S, Murray A W. 1999. From molecular to modular cell biology. Nature 402(Supplement):C47-C52.
70. Hedrick P W. 1986. Genetic polymorphism in heterogeneous environments: a decade later. Annual Review of Ecology and Systematics 17:535-566.
71. Hermisson J, Wagner G P. 2004. The population genetic theory of hidden variation and genetic robustness. Genetics 168:2271-2284.
72. Hermisson J, Hansen T F, Wagner G P. 2003. Epistasis in polygenic traits and the evolution of genetic architecture under stabilizing selection. American Naturalist 161:708-734.
73. Ho M W, Bolton E, Saunders P T. 1983a. Bithorax phenocopy and pattern formation. I. Spatiotemporal characteristics of the phenocopy response. Experimental Cell Biology 51(5):282-290.
74. Ho M W, Saunders P T, Bolton E. 1983b. Bithorax phenocopy and pattern formation. II. A model of prepattern formation. Experimental Cell Biology 51(5):291-299.
75. Ho M W, Tucker C, Keeley D, Saunders P T. 1983c. Effects of successive generations of ether treatment on penetrance and expression of the bithorax phenocopy in Drosophila melanogaster. Journal of Experimental Zoology 225:357-368.
76. Hoffmann A A, Woods R. 2001. Trait variability and stress: canalization, developmental stability and the need for a broad approach. Ecology Letters 4:97-101.
77. Houle D. 1991. Genetic covariance of fitness correlates: what genetic correlations are made of and why it matters. Evolution 45:630-648.
78. Houle D. 1992. Comparing evolvability and variability of quantitative traits. Genetics 130:195-204.
79. Houle D. 1998. How should we explain variation in the genetic variance of traits? Genetica 102/103:241-253.
80. Houle D. 2001. Characters as the units of evolutionary change. Pages 109-140 in The Character Concept in Evolutionary Biology, edited by G P Wagner. San Diego (CA): Academic Press.
81. Imasheva A G, Loeschcke V, Zhivotovsky L A, Lazebny O E. 1997. Effects of extreme temperatures on phenotypic variation and developmental stability in Drosophila melanogaster and Drosophila buzzatii. Biological Journal of the Linnean Society 61:117-126.
82. Jansen R C, Van Ooijen J W, Stam P, Lister C, Dean C. 1995. Genotype by environment interaction in genetic mapping of multiple quantitative trait loci. Theoretical and Applied Genetics 91:33-37.
83. Kacser H, Burns J A. 1981. The molecular basis of dominance. Genetics 97:639-666.
84. Kataoka T, Powers S, McGill C, Fasano O, Strathern J, Broach J, Wigler M. 1984. Genetic analysis of yeast RAS1 and RAS2 genes. Cell 37:437-445.
85. Kauffman S A. 1993. The Origins of Order: Self-Organization and Selection in Evolution. Oxford and New York: Oxford University Press.
86. Kawecki T J. 2000. The evolution of genetic canalization under fluctuating selection. Evolution 54:1-12.
87. Kitcher P. 2001. Battling the undead: how (and how not) to resist genetic determinism. Pages 396-414 in Thinking about Evolution: Historical, Philosophical, and Political Perspectives, edited by R S Singh, C B Krimbas, D B Paul, and J Beatty. Cambridge: Cambridge University Press.
88. Lande R. 1980. Genetic variation and phenotypic evolution during allopatric speciation. American Naturalist 116:463-479.
89. Laubichler M D. 2000. Homology in development and the development of the homology concept. American Zoologist 40:777-788.
90. Layzer D. 1980. Genetic variation and progressive evolution. American Naturalist 115:809-826.
91. Leamy L J, Routman E J, Cheverud J M. 1998. Quantitative trait loci for fluctuating asymmetry of discrete skeletal characters in mice. Heredity 80:509-518.
92. Lerner I M. 1954. Genetic Homeostasis. Edinburgh: Oliver and Boyd; New York: Wiley.
93. Lenski R E, Ofria C, Collier T C, Adami C. 1999. Genome complexity, robustness and genetic interactions in digital organisms. Nature 400:661-664.
94. Levin D A. 1970. Developmental instability and evolution in peripheral isolates. American Naturalist 104:343-353.
95. Lewontin R C. 1956. Studies on homeostasis and heterozygosity I. General considerations. Abdominal bristle number in second chromosome homozygotes of Drosophila melanogaster. American Naturalist 90:237-255.
96. Lewontin R C. 1974a. The Genetic Basis of Evolutionary Change. New York: Columbia University Press.
97. Lewontin R C. 1974b. Annotation: the analysis of variance and the analysis of causes. American Journal of Human Genetics 26:400-411.
98. Little J W, Shepley D P, Wert D W. 1999. Robustness of a gene regulatory circuit. EMBO Journal 18(15):4299-4307.
99. Magwene P M. 2001. New tools for studying integration and modularity. Evolution 55:1734-1745.
100. Maynard Smith J. 1999. Shaping Life: Genes, Embryos and Evolution. New Haven (CT): Yale University Press.
101. Maynard Smith J, Burian R, Kauffman S, Alberch P, Campbell J, Goodwin B, Lande R, Raup D, Wolpert L. 1985. Developmental constraints and evolution: a perspective from the Mountain Lake Conference on development and evolution. Quarterly Review of Biology 60:265-287.
102. Maynard Smith J, Sondhi K C. 1960. The genetics of a pattern. Genetics 45:1039-1050.
103. McAdams H H, Arkin A. 1997. Stochastic mechanisms in gene expression. Proceedings of the National Academy of Sciences USA 94:814-819.
104. McAdams H H, Arkin A. 1999. It's a noisy business! Genetic regulation at the nanomolar scale. Trends in Genetics 15:65-69.
105. Meiklejohn C D, Hartl D L. 2002. A single mode of canalization. Trends in Ecology and Evolution 17:468-473.
106. Mendel G. 1865. Versuche ūber Pflanzen-Hybriden. Verhandlungen des Naturforschenden Vereines in Brünn Band IV(1865):3-47.
107. Milton C C, Huynh B, Batterham P, Rutherford S L, Hoffmann A A. 2003. Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of genetic canalization and developmental stability. Proceedings of the National Academy of Sciences USA 100:13396-13401.
108. Moreno G. 1994. Genetic architecture, genetic behavior, and character evolution. Annual Review of Ecology and Systematics 25:31-44.
109. Nijhout H F. 2002. The nature of robustness in development. BioEssays 24(6):553-563.
110. Nijhout H F, Paulsen S M. 1997. Developmental models and polygenic characters. American Naturalist 149:394-405.
111. Nowak M A, Boerlijst M C, Cooke J, Maynard Smith J. 1997. Evolution of genetic redundancy. Nature 388:167-171.
112. Orr H A. 2000. Adaptation and the cost of complexity. Evolution 54:13-20.
113. Ozbudak E M, Thattai M, Kurtser I, Grossman A D, van Oudenaarden A. 2002. Regulation of noise in the expression of a single gene. Nature Genetics 31:69-73.
114. Pál C, Miklós I. 1999. Epigenetic inheritance, genetic assimilation and speciation. Journal of Theoretical Biology 200:19-37.
115. Palmer A R. 1994. Fluctuating asymmetry analyses: a primer. Pages 335-364 in Developmental Instability: Its Origins and Evolutionary Implications, edited by T A Markow. Dordrecht (The Netherlands): Kluwer.
116. Palmer A R, Strobeck C. 1986. Fluctuating asymmetry: measurement, analysis, patterns. Annual Review of Ecology and Systematics 17:391-421.
117. Palmer A R, Strobeck C. 1992. Fluctuating asymmetry as a measure of developmental stability: implications of non-normal distributions and power of statistical tests. Acta Zoologica Fennica 191:57-72.
118. Partridge L, Barton N H. 2000. Evolving evolvability. Nature 407:457-458.
119. Pigliucci M. 1996. How organisms respond to environmental changes: from phenotypes to molecules (and vice versa). Trends in Ecology and Evolution 11:168-173.
120. Pigliucci M, Murren C T. 2003. Perspective: genetic assimilation and a possible evolutionary paradox: can macroevolution sometimes be so fast as to pass us by? Evolution 57:1455-1464.
121. Polak M, Starmer W T. 2001. The quantitative genetics of fluctuating asymmetry. Evolution 55:498-511.
122. Proulx S R, Phillips P C. 2005. The opportunity for canalization and the evolution of genetic networks. American Naturalist 165:147-162.
123. Queitsch C, Sangster T A, Lindquist S. 2002. Hsp90 as a capacitor of phenotypic variation. Nature 417:618-624.
124. Real L A, Ellner S. 1992. Life history evolution in stochastic environments: a graphical mean-variance approach. Ecology 73:1227-1236.
125. Rendel J M. 1967. Canalisation and Gene Control. London: Logos Press; New York: Academic Press.
126. Rice S H. 1998. The evolution of canalization and the breaking of Von Baer's laws: modeling the evolution of development with epistasis. Evolution 52:647-656.
127. Rice S H. 2000. The evolution of developmental interactions: epistasis, canalization, and integration. Pages 82-98 in Epistasis and the Evolutionary Process, edited by J B Wolf, E D Brodie III, and M J Wade. Oxford and New York: Oxford University Press.
128. Rice S H. 2002. A general population genetic theory for the evolution of developmental interactions. Proceedings of the National Academy of Sciences USA 99:15518-15523.
129. Roff D A. 1997. Evolutionary Quantitative Genetics. New York: Chapman and Hall.
130. Rollo C D. 1994. Phenotypes: Their Epigenetics, Ecology and Evolution. London and New York: Chapman and Hall.
131. Rose M R. 1982. Antagonistic pleiotropy, dominance, and genetic variation. Heredity 48:63-78.
132. Routman E, Cheverud J M. 1994. Individual genes underlying quantitative traits: molecular and analytical methods. Pages 593-606 in Molecular Ecology and Evolution: Approaches and Applications, edited by B Schierwater, B Streit, G P Wagner, and R DeSalle. Basel (Switzerland): Birkhāuser Verlag.
133. Rutherford S L. 2000. From genotype to phenotype: buffering mechanisms and the storage of genetic information. BioEssays 22(12):1095-1105.
134. Rutherford S L. 2003. Between genotype and phenotype: protein chaperones and evolvability. Nature Reviews Genetics 4:263-274.
135. Rutherford S L, Lindquist S. 1998. Hsp90 as a capacitor for morphological evolution. Nature 396:336-342.
136. Sagaret A. 1826. Considerations sur la productions des hybrides des variantes et des variétés en general, et sur celles de Cucurbitacées en particulier. Annales des Sciences Naturelles, Serie 1 8:294-314.
137. Savageau M A. 1971. Parameter sensitivity as a criterion for evaluating and comparing the performance of biochemical systems. Nature 229:542-544.
138. Schank J C, Wimsatt W C. 2001. Evolvability: adaptation and modularity. Pages 322-335 in Thinking about Evolution: Historical, Philosophical, and Political Perspectives, edited by R S Singh, C B Krimbas, D B Paul, and J Beatty. Cambridge: Cambridge University Press.
139. Scharloo W. 1987. Constraints in selection response. Pages 125-149 in Genetic Constraints on Adaptive Evolution, edited by V Loeschcke. Berlin: Springer-Verlag.
140. Scharloo W. 1988. Selection on morphological patterns. Pages 230-250 in Population Genetics and Evolution, edited by G de Jong. Berlin: Springer-Verlag.
141. Scharloo W. 1991. Canalization: genetic and developmental aspects. Annual Review of Ecology and Systematics 22:65-93.
142. Scheiner S M. 1993. Genetics and evolution of phenotypic plasticity. Annual Review of Ecology and Systematics 24:35-68.
143. Scheiner S M, Lyman R F. 1991. The genetics of phenotypic plasticity. II. Response to selection. Journal of Evolutionary Biology 3:23-50.
144. Schlichting C D, Pigliucci M. 1998. Phenotypic Evolution: A Reaction Norm Perspective. Sunderland (MA): Sinauer Associates.
145. Schmalhausen I I. 1938. The Integrating Factors of Evolution. Leningrad: Nature (Priroda).
146. Schmalhausen I I. 1949. Factors of Evolution: The Theory of Stabilizing Selection. Philadelphia (PA):Blakiston. [Reprint. 1986. Chicago (IL): University of Chicago Press.]
147. Siegal M L, Bergman A. 2002. Waddington's canalization revisited: developmental stabiligy and evolution. Proceedings of the National Academy of Sciences USA 99:10528-10532.
148. Slack J M W. 2002. Timeline: Conrad Hal Waddington: the last Renaissance biologist? Nature Reviews Genetics 3:889-895.
149. Sollars V, Lu X, Xiao L, Wang X, Garfinkel M D, Ruden D M. 2003. Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution. Nature Genetics 33:70-74.
150. Stearns S C. 1982. The role of development in the evolution of life histories. Pages 237-258 in Evolution and Development, edited by J T Bonner. Berlin: Springer-Verlag.
151. Stearns S C. 1989a. The evolutionary significance of phenotypic plasticity. BioScience 39:436-445.
152. Stearns S C. 1989b. Comparative and experimental approaches to the evolutionary ecology of development. Geobios (mémoire spéciale) I2:349-355.
153. Stearns S C. 1993. The evolutionary links between fixed and variable traits. Acta Palaeontologica Polonica 38(3/4):215-232.
154. Stearns S C. 2000. Daniel Bernoulli (1738): evolution and economics under risk. Journal of Biosciences. 25(3):221-228.
155. Stearns S C, Kaiser M, Kawecki T J. 1995. The differential genetic and environmental canalization of fitness components in Drosophila melanogaster. Journal of Evolutionary Biology 8:539-557.
156. Stearns S C, Kawecki T J. 1994. Fitness sensitivity and the canalization of life-history traits. Evolution 48:1438-1450.
157. Stearns S C, Koella J C. 1986. The evolution of phenotypic plasticity in life-history traits: predictions of reaction norms for age and size at maturity. Evolution 40:893-913.
158. Stephens D W, Krebs J R. 1986. Foraging Theory. Princeton (NJ): Princeton University Press.
159. Stern C. 1958. Selection for subthreshold differences and the origin of pseudoexogenous adaptations. American Naturalist 92:313-316.
160. Stern D. 2000. Perspective: evolutionary developmental biology and the problem of variation. Evolution 54:1079-1091.
161. Sternberg P W, Han M. 1998. Genetics of RAS signaling in C. elegans. Trends in Genetics 14:466-472.
162. Tautz D. 1992. Redundancies, development and the flow of information. BioEssays 14(4):263-266.
163. Thatcher J W, Shaw J M, Dickinson W J. 1998. Marginal fitness contributions of nonessential genes in yeast. Proceedings of the National Academy of Sciences USA 95:253-257.
164. Thoday J M. 1955. Balance, heterozygosity and developmental stability. Cold Spring Harbor Symposium of Quantitative Biology 20:318-326.
165. Thoday J M. 1958. Homeostasis as a selection experiment. Heredity 12:401-415.
166. True H L, Lindquist S L. 2000. A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407:477-483.
167. True H L, Berlin I, Lindquist S L. 2004. Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 431:184-187.
168. Turelli M. 1988. Phenotypic evolution, constant covariances, and the maintenance of additive variance. Evolution 42:1342-1347.
169. Van Dongen S, Lens L. 2000. The evolutionary potential of developmental instability. Journal of Evolutionary Biology 13:326-335.
170. Via S. 1994. The evolution of phenotypic plasticity: what do we really know? Pages 35-57 in Ecological Genetics, edited by L A Real. Princeton (NJ): Princeton University Press.
171. Waddington C H. 1942. Canalization of development and the inheritance of acquired characters. Nature 150:563-565.
172. Waddington C H. 1953. Genetic assimilation of an acquired character. Evolution 7:118-126.
173. Waddington C H. 1956. Genetic assimilation of the bithorax phenotype. Evolution 10:1-13.
174. Waddington C H. 1957. The Strategy of the Genes: A Dismission of Some Aspects of Theoretical Biology. London: Allen and Unwin; New York: MacMillan.
175. Waddington C H. 1960. Experiments on canalizing selection. Genetical Research, Cambridge 1:140-150.
176. Waddington C H. 1961. Genetic assimilation. Advances in Genetics 10:257-293.
177. Wade M J, Winther R G, Agrawal A F, Goodnight C J. 2001. Alternative definitions of epistasis: dependence and interaction. Trends in Ecology and Evolution 16:498-504.
178. Wagner A. 1996. Does evolutionary plasticity evolve? Evolution 50:1008-1023.
179. Wagner A. 1999. Redundant gene functions and natural selection. Journal of Evolutionary. Biology 12:1-16.
180. Wagner A. 2000a. The role of population size, pleiotropy and fitness effects of mutations in the evolution of overlapping gene functions. Genetics 154:1389-1401.
181. Wagner A. 2000b. Robustness against mutations in genetic networks of yeast. Nature Genetics 24:355-361.
182. Wagner A, Stadler P F. 1999. Viral RNA and evolved mutational robustness. Journal of Experimental Zoology 285:119-127.
183. Wagner G P. 1996. Homologues, natural kinds and the evolution of modularity. American Zoologist 36:36-43.
184. Wagner G P, Altenberg L. 1996. Perspective: complex adaptations and the evolution of evolvability. Evolution 50:967-976.
185. Wagner G P, Booth G, Bagheri-Chaichian H. 1997. A population genetic theory of canalization. Evolution 51:329-347.
186. Wagner G P, Laubichler M D, Bagheri-Chaichian H. 1998. Genetic measurement theory of epistatic effects. Genetica 102/103:569-580.
187. Whitlock M C, Phillips P C, Moore F B-G, Tonsor S J. 1995. Multiple fitness peaks and epistasis. Annual Review of Ecology and Systematics 26:601-629.
188. Wijngaarden P J, Koch P B, Brakefield P M. 2002. Artificial selection on the shape of reaction norms for eyespot size in the butterfly Bicyclus anynana: direct and correlated responses. Journal of Evolutionary Biology 15:290-300.
189. Wilke C O, Wang J L, Ofria C, Lenski R E, Adami C. 2001. Evolution of digital organisms at high mutation rate leads to survival of the flattest. Nature 412:331-333.
190. Wilkins A S. 1997. Canalization: a molecular genetic perspective. BioEssays 19(3):257-262.
191. Wolf J B, Brodie E D, III, Wade M J, eds. 2000. Epistasis and the Evolutionary Process. Oxford and New York: Oxford University Press.
192. Wolf J B, Frankino W A, Agrawal A F, Brodie E D, III, Moore A J. 2001. Developmental interactions and the constituents of quantitative variation. Evolution 55:232-245.
193. Woltereck R. 1909. Weitere, experimentelle Untersuchungen über Artverānderung, speziell über das Wesen quantitativer Artunterschiede bei Daphniden. Verhandlungen der Deutschen Zoologischen Gesellschaft 1909:110-172.
194. Wright S. 1934. Physiological and evolutionary theories of dominance. American Naturalist 68:24-53.
195. Wright S. 1977. Evolution and the Genetics of Populations, Volume 3: Experimental Results and Evolutionary Deductions. Chicago (IL): University of Chicago Press.
196. Wu R. 1998. The detection of plasticity genes in heterogeneous environments. Evolution 52:967-977.
197. Zakharov V M. 1992. Population phenogenetics: analysis of developmental stability in natural populations. Acta Zoologica Fennica 191:7-30.