Phenotypic variability: Its components, measurement and underlying developmental processes

Evolutionary Biology

Volumn 34, Issue 3-4, 2007, Pages 99-120

  Willmore, Katherine Elizabeth ^a   Young, Nathan M ^b   Richtsmeier, Joan T ^c  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NONE

Author keywords

Canalization; Development; Developmental stability; Morphological integration; Phenotype; Variability; Variation

Indexed keywords

EID: 43249108943     PISSN: 00713260     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11692-007-9008-1     Document Type: Article

References (157)

1. Atchley, W. R., & Hall, B. K. (1991). A model for development and evolution of complex morphological structures. Biological Reviews, 66, 101-157.
2. Babbitt, G. A., Kiltie, R., & Bolker, B. (2006) Are fluctuating asymmetry studies adequately sampled? Implications of a new model for size distribution. American Naturalist, 167, 230-245.
3. Bagheri, H. C., & Wagner, G. P. (2004). Evolution of dominance in metabolic pathways. Genetics, 168, 1713-1735.
4. Berg, R. L. (1959). The ecological significance of correlational pleiades. Evolution, 14, 171-180.
5. Bjorksten, T. A., Fowler, K., & Pomiankowski, A. (2000). What does sexual trait FA tell us about stress? TREE, 15, 163-166.
6. Blake, W. J., Kaern, M., Cantor, C. R., & Collins, J. J. (2003). Noise in eukaryotic gene expression. Nature, 422, 633-637.
7. Bradshaw, A. D. (1965). Evolutionary significance of phenotypic plasticity in plants. Advances in Genetics, 13, 115-155.
8. Braendle, C., & Flatt, T. (2006). A role for genetic accommodation in evolution? BioEssays, 28, 868-873.
9. Bresin, A., Johansson, C. B., & Kiliaridis, S. (1994). Effects of occlusal strain on the development of the dentoalveolar process in the growing rat. A morphometric study. European Journal of Experimental Musculoskeletal Research, 3, 112-122.
10. Breuker, C. J., Patterson, J. S., & Klingenberg, C. P. (2006). A single basis for developmental buffering of Drosophila wing shape. PloS ONE 1:e7.
11. Burnett, R. J., & Larkins, B. A. (1999). Opaque2 modifiers alter transcription of the 27-kDA γ-zein genes in maize. Molecular & General Genetics, 261, 908-916.
12. Carroll, S. B., Grenier, J. K., & Weatherbee, S. D. (2005). From DNA to diversity: Molecular genetics and the evolution of animal design (2nd ed.). Malden MA: Blackwell Publishing Ltd.
13. Chernoff, B., & Magwene, P. M. (1999). Morphological integration: Forty years later. In: E. C. Olson, & R. L. Miller (Eds.), Morphological integration (pp. 319-353). Chicago: University of Chicago Press.
14. Cheverud, J. M. (1982). Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution, 36, 499-516.
15. Cheverud, J. M. (1984). Quantitative genetics and developmental constraints on evolution by selection. Journal of Theoretical Biology, 110, 155-171.
16. Cheverud, J. M. (1988). A comparison of genetic and phenotypic correlations. Evolution, 42, 958-968.
17. Cheverud, J. M. (1995). Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. American Naturalist, 145, 63-89.
18. Cheverud, J. M. (1996). Developmental integration and the evolution of pleiotropy. American Zoologist, 36, 44-50.
19. Cheverud, J. M., Routman, E. J., & Irschick, D. J. (1997). Pleiotropic effects of individual gene loci on mandibular morphology. Evolution, 51, 2006-2016.
20. Cheverud, J. M., Ehrich, T. H., Vaughn, T. T., Koreishi, S. F., Linsey, R. B., & Pletscher, L. S. (2004). Pleiotropic effects on mandibular morphology II: Differential epistasis and genetic variation in morphological integration. Journal of Experimental Zoology (Molecular and Development Evolution), 302B, 424-435.
21. Ciochon, R. L., Nisbett, R. A., & Corruccini, R. S. (1997). Dietary consistency and craniofacial development related to masticatory function in minipigs. Journal of Craniofacial Genetics and Developmental Biology, 17, 96-102.
22. Clarke, G. M. (1993). The genetic basis of developmental stability. I. Relationships between stability, heterozygosity and genomic coadaptation. Genetica, 89, 15-23.
23. Clarke, G. M. (1998). The genetic basis of developmental stability, V. Inter- and intra-individual character variation. Heredity, 80, 562-567.
24. Cole, T. M. III. (2002). MI Boot Windows-based software for bootstrap comparison of morphological integration. University of Missouri-Kansas School of Medicine, Kansas, MO.
25. Cole, T. M., III, & Lele, S. (2002). Bootstrap-based methods for comparing morphological integration patterns. American Journal of Physical Anthopology, Supplement, 34, 55.
26. Cottrill, C. P., Archer, C. W., & Wolpert, L. (1987). Cell sorting and chongrogenic aggregate formation in micromass culture. Developmental Biology, 122, 503-515.
27. 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 Royal Society of London, Series B, 267, 423-430.
28. Debat, V., Milton, C. C., Rutherford, S., Klingenberg, C. P., & Hoffmann, A. A. (2006). HSP90 and the quantitative variation of wing shape in Drosophila melanogaster. Evolution, 60, 2529-2538.
29. Depew, M. J., Lufkin, T., & Rubenstein, J. L. R. (2002). Specification of jaw subdivisions by Dlx genes. Science, 298, 381-385.
30. Depew, M. J., Simpson, C. A., Morasso, M., & Rubenstein, J. L. R. (2005). Reassessing the Dlx code: The genetic regulation of branchial arch skeletal pattern and development. Journal of Anatomy, 207, 501-561.
31. Dunn, R. B., & Fraser, A. S. (1958). Selection for an invariant character-"vibrissae number"-in the house mouse. Nature, 181, 1018-1019.
32. Dunn, R. B., & Fraser, A. S. (1959). Selection for an invariant character, vibrissae number in the house mouse. Australian Journal of Biological Sciences, 12, 506-523.
33. Eccleston, A, DeWitt, N., Gunter, C., Marte B., & Nath, D. (2007). Epigenetics. Nature, 447, 395.
34. Ede, D. A. (1983). Cellular condensations and chondrogenesis. In: B. K. Hall (Ed.), Cartilage, development, differentiation and growth, Vol. 2. (pp. 143-186). New York: Academic Press.
35. Ehrich, T. H., Vaughn, T. T., Koreishi, S. F., Linsey, R. B., Pletscher, L. S., & Cheverud, J. M. (2003). Pleiotropic effects on mandibular morphology I. Developmental morphological integration and differential dominance. Journal of Experimental Zoology (Molecular and Development Evolution), 296B, 58-79.
36. Falconer, D. S., & Mackay, T. F. C. (1996). Introduction to quantitative genetics. New York: Longman Press.
37. Fiering, S., Whitelaw, E., & Martin, D. I. K. (2000). To be or not to be active: the stochastic nature of enhancer action. Bioessays, 22, 381-387.
38. Foote, M., & Cowie, R. H. (1988). Developmental buffering as a mechanism for stasis: Evidence from the pulmonate Theba pisana. Evolution, 42, 396-399.
39. Francis-West, P. H., Robson, L., & Evans, D. J. R. (2003). Craniofacial development: The tissue and molecular interactions that control development of the head. In: F. Beck, B. Christ, W. Kriz, W. Kummer, E. Marani, R. Putz, Y. Sano, T. H. Schiebler, G. L. Schoenwolf, & K. Zilles (Eds.), Advances in anatomy and cell biology. Vol. 169. Berlin: Springer-Verlag.
40. Gass, G. L., & Bolker, J. A. (2002). Modularity. In: W. Olson (Ed.), Keywords and concepts in evolutionary developmental biology. Cambridge: Harvard University Press.
41. Geetha, K. B., Lending, C. R., Lopes, M. A., Wallace, J. C., & Larkins, B. A. (1991). Opaque-2 modifiers increase γ-zein synthesis and alter its spatial distribution in maize endosperm. Plant Cell, 3, 1207-1219.
42. Gibson, G., & van Helden, S. (1997). Is function of the Drosophila homeotic gene Ultrabithorax canalized? Genetics, 147, 1155-1168.
43. Gibson, G., & Wagner, G. (2000). Canalization in evolutionary genetics: a stabilizing theory? BioEssays, 22, 372-380.
44. Gilbert, S. F. (2003). Developmental biology (7th ed.) Massachusetts: Sinauer Associated Inc.
45. Gould, S. J., & Garwood, R. A. (1969). Levels of integration in mammalian dentitions: An analysis of correlations in Nesophontes micrus (Insectivora) and Oryzomys couesi (Rodentia). Evolution, 23, 276-300.
46. Graham, A. (2002). Jaw development: Chinless wonders. Current Biology, 12, 810-812.
47. Graham, J. H., Freeman, D. C., & Emlen, J. M. (1993). Developmental stability: A sensitive indicator of populations under stress. In: M. A. Lewis (Ed.), Environmental toxicology and risk assessment (pp. 136-158). Philadelphia: American Society for Testing and Materials.
48. Graham, J. H., Shimizu, K., Emlen, J. M., Freeman, D. C., & Merkel, J. (2003). Growth model and the expected distribution of fluctuating asymmetry. Biological Journal of the Linnean Society, 80, 57-65.
49. Hall, B. K. (1978). Developmental and cellular skeletal biology. New York: Academic Press.
50. Hall, B. K. (1988). The embryonic development of bone. American Scientist, 76, 174-181.
51. Hall, B. K. (1999). The neural crest in development and evolution. New York: Springer-Verlag.
52. Hallgrímsson, B., Willmore, K., & Hall, B. K. (2002). Canalization, developmental stability, and morphological integration in primate limbs. American Journal of Physical Anthropology Supplement, 35, 131-158.
53. He, T., & Kiliaridis, S. (2003). Effects of masticatory muscle function on craniofacial morphology in growing ferrets (Mustela putorius furo). European Journal of Oral Sciences, 111, 510-517.
54. 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.
55. Hermisson, J., & Wagner, G. P. (2004). Canalization in evolutionary genetics: a stabilizing theory? BioEssays, 22, 372-380.
56. Herring, S. W. (1993). Epigenetic and functional influences on skull growth. In: J. Hanken, & B. K. Hall (Eds.), The skull, Vol. 1 (pp. 153-206). Chicago: University of Chicago Press.
57. Herring, S. W., & Teng, S. (2000). Strain in the braincase and its sutures during function. American Journal of Physical Anthropology, 112, 575-593.
58. Herring, S. W., Decker, J. D., Liu, Z.-J., & Ma, T. (2002). Temporomandibular joint in miniature pigs: anatomy, cell replication, and relation to loading. Anatomical Record, 266, 152-166.
59. Houle, D. (1998). How should we explain variation in genetic variance of traits? Genetica, 102/103, 241-253.
60. Huerta-Sanchez, E., & Durrett, R. (2007). Wagner's canalization model. Theoretical Population Biology, 71, 121-130.
61. Hurle, J. M., Gana, Y., & Marcias, D. (1989). Experimental analysis of the in-vivo chondrogenic potential of the interdigital mesenchyme of the chick leg bud subjected to local ectodermal removal. Developmental Biology, 132, 368-374.
62. Jacob, F. (1977). Evolution and tinkering. Science, 196, 1161-1166.
63. Jernvall, J., & Jung, H. S. (2000). Genotype, phenotype, and developmental biology of molar tooth characters. American Journal of Physical Anthropology, 43, 171-190.
64. Johnson, D. R. (1986). The genetics of the skeleton. Oxford: Clarendon Press.
65. Katsaros, C., Berg, R., & Kiliaridis, S. (2002). Influence of masticatory muscle function on transverse skull dimensions in the growing rat. Journal of Orofacial Orthopedics, 63, 5-13.
66. Kaufmann, W. K., & Paules, R. S. (1996). DNA damage and cell cycle checkpoints. The FASEB Journal, 10, 238-247.
67. Klingenberg, C. P. (2003). A developmental perspective on developmental instability: Theory, models and mechanisms. In: M. Polak (Ed.), Developmental Instability (DI): Causes and Consequences (pp. 14-34). Oxford: Oxford University Press.
68. Klingenberg, C. P., & McIntyre, G. S. (1998). Geometric Morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution, 52, 1363-1375.
69. Klingenberg, C. P., & Zaklan, S. D. (2000). Morphological integration between developmental compartments in the Drosophila wing. Evolution, 54, 1273-1285.
70. Klingenberg, C. P., Leamy, L. J., Routman, E. J., & Cheverud, J. M. (2001). Genetic architecture of mandible shape in mice: Effects of quantitative trait loci analyzed by geometric morphometrics. Genetics, 157, 785-802.
71. Kuratani, S. (2005). Developmental studies of the lamprey and hierarchical evolutionary steps towards the acquisition of the jaw. Journal of Anatomy, 207, 489-499.
72. Leamy, L. J., Routman, E. J., & Cheverud, J. M. (2002). An epistatic genetic basis for fluctuating asymmetry of mandible size in mice. Evolution, 56, 642-653.
73. Lens, L., VanDongen, S., Kark, S., & Matthysen, E. (2002). Fluctuating asymmetry as an indicator of fitness: Can we bridge the gap between studies? Biological Reviews, 77, 27-38.
74. Leung, B., Forbes, M. R., & Houle, D. (2000). Fluctuating asymmetry as an indicator of stress: comparing efficacy of analyses involving multiple traits. American Naturalist, 155, 101-115.
75. Ludwig, W. (1932). Das Rechts-links problem im Teirreich und beim Menschen. Berlin (Germany): Springer.
76. Lund, J. P., & Kolta, A. (2006). Generation of the central masticatory pattern and its modification by sensory feedback. Dysphagia, 21, 167-174.
77. Manning, J. T., & Chamberlain, A. T. (1994). Fluctuating asymmetry in gorilla canines: a sensitive indicator of environmental stress. Proceedings of Royal Society of London, Series B, 255, 189-193.
78. Marriog, G., & Cheverud, J. M. (2001). A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of new world monkeys. Evolution, 55, 2576-2600.
79. McAdams, H. H., & Arkin, A. (1999). It's a noisy business! Genetic regulation at the nanomolar scale. Trends in Genetics, 15, 65-69.
80. Mills, K. D., Ferguson, D. O., & Alt, F. W. (2003). The role of DNA breaks in genomic instability and tumorigenesis. Immunological Reviews, 194, 77-94.
81. Milton, C. C., Huynh, B., Batterham, P., Rutherford, S. L., & Hoffmann, A. A. (2003). Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of canalization and developmental stability. Proceedings of National Academy of Sciences of the United States of America, 100, 13396-13401.
82. Mohrenweiser, H. W., Wilson, D. M., & Jones, I. M. (2003). Challenges and complexities in estimating both the functional impact and the disease risk associated with the extensive genetic variation in human DNA repair genes. Mutation Research, 526, 93-125.
83. Moran, P. A. P. (1992). The evolutionary maintenance of alternative phenotypes. American Naturalist, 139, 971-989.
84. Moro, G. L., Habben, J. E., Hamaker, B. R., & Larkins, B. A. (1996). Characterization of the variability in lysine content for normal and opaque2 maize endosperm. Crop Science, 36, 1651-1659.
85. Moss, M. (1971). Functional cranial analysis and the functional matrix. American Speech Hearing Association Report, 6, 5-18.
86. Moss, M., & Young, R. (1960). A functional approach to craniology. American Journal of Physical Anthropology, 18, 281-292.
87. Nijhout, F. H. (1999). Control mechanisms of polyphonic development in insects. BioScience, 49, 181-192.
88. Nijhout, H. F., & Davidowitz, G. (2003). Developmental perspectives on phenotypic variation: canalization, and fluctuating asymmetry. In: M. Polak (Ed.), Developmental instability (DI): Causes and consequences (pp. 3-13). Oxford: Oxford University Press.
89. Nilsson-Ehle, H. (1914). Vilka erfarenheter hava hittills vunnits rörande möjligheten av växters acklimatisering? Kungl Landtbruksakad Hand Tidskr, 53, 537-572.
90. Olson, E. C., & Miller, R. L. (1951). A mathematical model applied to a study of the evolution of species. Evolution, 5, 256-338.
91. Olson, E. C., & Miller, R. L. (1958). Morphological integration. Chicago: University of Chicago Press.
92. Palmer, A. R. (1996). Waltzing with asymmetry. BioScience, 46, 518-532.
93. Palmer, A. R., & Strobeck, C. (1986). Fluctuating Asymmetry: Measurement, Analysis, Patterns. Annual Review Ecology Systematics, 17, 391-421.
94. 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.
95. Palmer, R., & Strobeck, C. (2003). Fluctuating asymmetry analysis unplugged. In: M. Polak (Ed.), Developmental instability (DI): Causes and consequences (pp. 279-319). Oxford: Oxford University Press.
96. Qiu, M., Bulfone, A., Ghattas, I., Meneses, J. J., Christensen, L., Sharpe, P. T., Presley, R., Pederson, R. A., & Rubenstein, J. L. R. (1997). Role of the Dlx homeobox genes in proximodistal patterning of the branchial arches: Mutations of Dlx-1, Dlx-2 and -2 alter morphogenesis of proximal skeletal and soft tissue structures derived from first and second arches. Developmental Biology, 185, 165-184.
97. Rafferty, K. L., Herring, S. W., & Artese, F. (2000). Three-dimensional loading and growth of the zygomatic arch. Journal of Experimental Biology, 203, 2093-3004.
98. Rasmuson, M. (2002). Fluctuating asymmetry-indicator of what? Hereditas, 136, 177-183.
99. Réale, D., & Roff, D. A. (2003). Inbreeding, developmental stability, and canalization in the sand cricket Gryllus firmus. Evolution, 57, 597-605.
100. Reeve, E. C. R. 1960. Some genetic tests on asymmetry of sternopleural chaetae number in Drosophila. Genetical Research, 1, 151-172.
101. Reeve, E. C. R., & Robertson, F. W. (1953). Analysis of environmental variability in quantitative inheritance. Nature, 171, 874-875.
102. Rendel, J. M. (1959). Canalization of the scute phenotype of Drosophila. Evolution, 13, 425-439.
103. Richtsmeier, J. T., Aldridge, K. A., DeLeon, V. B., Panchal, J., Kane, A. A., Marsh, J. L., Yan, P., Cole, T. M., III. 2006. Phenotypic integration of neurocranium and brain. Journal of Experimental Zoology (Molecular and Development Evolution), 306B, 1-19.
104. Routman, E. J., & Cheverud, J. M. (1997). Gene effects on a quantitative trait: two-locus epistatic effects measured at microsatellite markers and at estimated QTL. Evolution, 51, 1654-1662.
105. Rutherford, S. L. (2000). From genotype to phenotype: buffering mechanisms and the storage of genetic information. Bioessays, 22, 1095-1105.
106. Rutherford, S. L., & Lindquist, S. (1998). Hsp90 as a capacitor for morphological evolution. Nature, 396, 336-342.
107. Salazar-Ciudad, I., Newman, S. A., Solé RV. 2001a. Phenotypic and dynamical transitions in model genetic networks I. Emergence of patterns and genotype-phenotype relations. Evolution & Development, 3, 84-94.
108. Salazar-Ciudad, I., Solé RV, Newman SA. 2001b. Phenotypic and dynamical transitions in model genetic networks II. Application to the evolution of segmentation mechanisms. Evolution & Development, 3, 95-103.
109. Salazar-Ciudad, I., & Jernvall, J. (2002). A gene network model accounting for development and evolution of mammalian teeth. Proceedings of National Academy of Sciences of the United States of America, 99, 8116-8120.
110. Salazar-Ciudad, I., & Jernvall, J. (2004). How different types of pattern formation mechanisms affect the evolution of form and development. Evolution & Development, 6, 6-16.
111. Salazar-Ciudad, I., & Jernvall, J. (2005). Graduality and innovation in the evolution of complex phenotypes: Insights from development. Journal of Experimental Zoology (Molecular and Development Evolution), 304B, 619-631.
112. Santos, M., Fernández Iriarte, P., & Céspedes, W. (2005). Genetics and geometry of canalization and developmental stability in Drosophila subobscura. BMC Evolutionary Biology, 5, 7.
113. Scharloo, W. (1991). Canalization: Genetic and developmental aspects. Annual Review of Ecology Systematics, 22, 65-93.
114. Scheiner, S. M. (1993). Genetics and evolution of phenotypic plasticity. Annual Review of Ecology Systematics, 24, 35-68.
115. Schlichting, C. D. (1986). The evolution of phenotypic plasticity in plants. Annual Review of Ecology Systematics, 17, 667-693.
116. Schlichting, C. D., & Pigliucci, M. (1998). Phenotypic evolution: A reaction norm perspective. Sunderland MA: Sinauer.
117. Schmalhausen, I. I. (1949). Factors of evolution. Chicago: University of Chicago Press.
118. Siegal, M. L., & Bergman, A. (2002). Waddington's canalization revisited: developmental stability and evolution. Proceedings of National Academy of Sciences of the United States of America, 99, 10528-10532.
119. Stearns, S. C. (1989). The evolutionary significance of phenotypic plasticity. BioScience, 39, 436-445.
120. Stock, D. W. (2005). The Dlx complement of the leopard shark, Triakis semifasciata, resembles that of mammals: Implications for genomic and morphological evolution of jawed vertebrates. Genetics, 169, 807-817.
121. Suzuki, D. T., Griffiths, A. J. F., Miller, J. H., & Lewontin, R. C. (1986). An introduction to genetic analysis. New York: WH Freeman.
122. Thomas, J. H. (1993). Thinking about genetic redundancy. Trends in Genetics, 9, 305-309.
123. Thorogood, P. (1983). Morphogenesis of cartilage. In: B. K. Hall (Ed.), Cartilage, development, differentiation and growth. Vol. 2. (pp. 223-255). New York: Academic Press.
124. Turman, J. E., Jr. 2007. The development of mastication in rodents: From neurons to behaviors. Archives of Oral Biology, 52, 313-316.
125. Van Dongen, S. (2006). Fluctuating asymmetry and developmental instability in evolutionary biology: past, present and future. Journal of Evolutionary Biology, 19, 1727-1743.
126. Van Valen, L. (1962). A study of fluctuating asymmetry. Evolution, 16, 125-142.
127. von Dassow, G., Meir, E., Munro, E., & Odell, G. (2000). The segment polarity network is a robust development module. Nature, 406, 188-192.
128. Waddington, C. H. (1942). The canalisation of development and the inheritance of acquired characters. Nature, 150, 563.
129. Waddington, C. H. (1953). Genetic assimilation of an acquired character. Evolution, 7, 118-126.
130. Waddington, C. H. (1956). Genetic assimilation of the bithorax phenotype. Evolution, 10, 1-13.
131. Waddington, C. H. (1957). Strategy of the genes. New York: MacMillan.
132. Waddington, C. H. (1959). Canalization of development and genetic assimilation of acquired characters. Nature, 183, 1654-1655.
133. Waddington, C. H. (1961). Genetic assimilation. Advances in Genetics, 10, 257-293.
134. Waddington, C. H. (1975). The Evolution of an evolutionist. Ithaca, New York: Cornell University Press.
135. Wagner, A. (1999). Redundant gene functions and natural selection. Journal of Evolutionary Biology, 12, 1-16.
136. Wagner, A. (2005). Distributed robustness versus redundancy as causes of mutational robustness. BioEssays, 27, 176-188.
137. Wagner, G. P. (1996). Homologues, natural kinds and the evolution of modularity. American Zoologist, 36, 36-43.
138. Wagner, G. P., & Altenberg, L. (1996). Complex adaptations and the evolution of evolvability. Evolution, 50, 967-976.
139. Wagner, G. P., Booth, G., Bagheri-Chaichian, H. 1997. A population genetic theory of canalization. Evolution, 51, 329-347.
140. Wagner, G. P., Laubichle, MD, Bagheri-Chaichian, H. (1998). Genetic measurement theory of epistatic effects. Genetica, 102-103, 569-580.
141. Weiss, K. M., & Fullerton, S. M. (2000). Phenogenetic drift and the evolution of genotype-phenotype relations. Theoretical Population Biology, 57, 187-195.
142. Weiss, K. M., & Buchanan, A. V. (2004). Genetics and The logic of Evolution. New York: John Wiley.
143. Weiss, P. A. (1971). The basic concept of hierarchic systems. In: P. A. Weiss (Ed.), Hierarchically organized systems in theory and practice (pp. 1-43.). New York: Hafner Publishing Company.
144. West-Eberhard, M. J. (1986). Alternative adaptations, speciation, and phylogeny. Proceedings of National Academy of Sciences of the United States of America, 83, 1388-1392.
145. West-Eberhard, M. J. (2003). Developmental plasticity and evolution. New York: Oxford University Press.
146. West-Eberhard, M. J. (2005). Phenotypic accommodation: Adaptive innovation due to developmental plasticity. Journal of Experimental Zoology (Molecular and Development Evolution), 304B, 610-618.
147. Willmore, K. E., Klingenberg, C. P., Hallgrímsson, B. 2005. The relationship between fluctuating asymmetry and environmental variance in Rhesus macaque skulls. Evolution, 59, 898-909.
148. Willmore, K. E., Hallgrímsson, B. (2005). Within individual variation: Developmental noise versus developmental stability. In: B. Hallgrímsson, & B. K. Hall (Eds.), Variation: A central concept in biology (pp. 191-218). New York: Elsevier Academic Press.
149. Willmore, K. E., Leamy, L., Hallgrímsson, B. (2006). Effects of developmental and functional interactions on mouse cranial variability through late ontogeny. Evolution & Development, 8, 550-567.
150. Woltereck, R. (1909). Weitere experimentelle untersuchungen über artveränderung, speziell über das wesen quantitaver artunterschiede bei Daphnien. Verh Deutsch Zool Gesellsch, 19, 110-173.
151. Woods, R. E., Sgrò CM, Hercus, M. J., & Hoffmann, A. A. (1999). The association between fluctuating asymmetry, trait variability, trait heritability, and stress: A multiply replicated experiment on combined stresses in Drosophila melanogaster. Evolution, 53, 493-505.
152. Yamada, K., & Kimmel, D. B. (1991). The effect of dietary consistency on bone mass and turnover in the growing rat mandible. Archives of Oral Biology, 36, 129-138.
153. Young, N.M. (2006). Function, ontogeny and canalization of shape vairance in the primate scapula. Journal of Anatomy, 209, 623-636.
154. Young, N.M., Hallgrímsson, B. (2005). Serial homology and the evolution of mammalian limb covariation structure. Evolution, 59, 2691-2704.
155. Zakharaov, V. M. (1992). Population phenotgenetics: analysis of developmental stability in natural populations. Acta Zoologica Fennica, 191, 7-30.
156. Zelditch, M. L., Bookstein, F. L., & Lundrigan, B. L. (1993). The ontogenetic complexity of developmental constraints. Journal of Evolutionary Biology, 6, 621-641.
157. Zelditch, M. L., Lundrigan, B. L., & Garland, T. (2004). Developmental regulation of skull morphology. I. Ontogenetic dynamics of variance. Evolution & Development, 6, 194-206.