Evolution of morphological integration: Developmental accommodation of stress-induced variation

American Naturalist

Volumn 166, Issue 3, 2005, Pages 382-395

  Badyaev, Alexander V ^a   Foresman, Kerry R ^b   Young, Rebecca L ^a  

^a University of Arizona   (United States)

^b UNIVERSITY OF MONTANA   (United States)

Author keywords

Developmental plasticity; Functional integration; Modularity; Sorex; Stress; Variation

Indexed keywords

ENVIRONMENTAL CHANGE; MORPHOLOGY;

ADAPTATION; ANIMAL; ARTICLE; BIOMETRY; ECOSYSTEM; EVOLUTION; FEMALE; HISTOLOGY; MALE; MANDIBLE; PHYSIOLOGICAL STRESS; SHREW; SKELETAL MUSCLE; STRESS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; BIOMETRY; ECOSYSTEM; EVOLUTION; FEMALE; MALE; MANDIBLE; MUSCLE, SKELETAL; SHREWS; STRESS; STRESS, PHYSIOLOGICAL;

SOREX; SORICIDAE;

EID: 24644477488     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/432559     Document Type: Article

References (99)

1. Alberch, P. 1980. Ontogenesis and morphological diversification. American Zoologist 20:653-667.
2. Ancel, L. W. 1999. A quantitative model of the Simpson-Baldwin effect. Journal of Theoretical Biology 196:197-209.
3. Aparicio, J. M., and R. Bonal. 2002. Why do some traits show higher fluctuating asymmetry than others? a test of hypotheses with tail feathers of birds. Heredity 89:139-144.
4. Ärnbäck-Christie-Linde, A. 1907. Der Bau der Soriciden und ihre Beziehungen zu andern Säugetieren. Gegenbaurs Morphologisches Jahrbuch 36:463-514.
5. Baatz, M., and G. P. Wagner. 1997. Adaptive inertia caused by hidden pleiotropic effects. Theoretical Population Biology 51:49-66.
6. Badyaev, A. V. 1998. Environmental stress and developmental stability in dentition of the Yellowstone grizzly bears. Behavioral Ecology 9:339-344.
7. _. 2005. Stress-induced variation in evolution: from behavioral plasticity to genetic assimilation. Proceedings of the Royal Society of London B 272:877-886.
8. Badyaev, A. V., and K. R. Foresman. 2000. Extreme environmental change and evolution: stress-induced morphological variation is strongly concordant with patterns of evolutionary divergence in shrew mandibles. Proceedings of the Royal Society of London B 267:371-377.
9. _. 2004. Evolution of morphological integration. 1. Functional units channel stress-induced variation. American Naturalist 163:868-879.
10. Badyaev, A. V., K. R. Foresman, and M. V. Fernandes. 2000. Stress and developmental stability: vegetation removal causes increased fluctuating asymmetry in shrews. Ecology 81:336-345.
11. Bijlsma, R., and V. Loeschcke. 1997. Environmental stress, adaptation and evolution. Birkhauser, Basel.
12. Bradshaw, A. D., and K. Hardwick. 1989. Evolution and stress: genotypic and phenotypic components. Biological Journal of the Linnean Society 37:137-155.
13. Caropale, L. H. 1999. Chance favors the prepared genome. Annals of the New York Academy of Sciences 870:1-21.
14. Chapin, F. S., III, K. Autumn, and F. Pugnaire. 1993. Evolution of suites of traits in response to environmental stress. American Naturalist 142(suppl.):S78-S92.
15. Cheverud, J. M. 1982. Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution 36:499-516.
16. Cheverud, J. M., J. J. Rutledge, and W. R. Atchley. 1983. Quantitative genetics of development: genetic correlations among age-specific trait values and the evolution of ontogeny. Evolution 37:895-905.
17. Dannelid, E. 1994. Comparison of pigment and other dental characters of eastern Palearctic Sorex (Mammalia: Soricidae). Pages 217-231 in J. F. Merritt, G. L. J. Kirkland, and R. K. Rose, eds. Advances in the biology of shrews. Carnegie Museum of Natural History, Pittsburgh.
18. Debat, V., and P. David. 2001. Mapping phenotypes: canalization, plasticity and developmental stability. Trends in Ecology & Evolution 16:555-561.
19. Dötsch, C. 1985. Masticatory function in shrews (Soricidae). Acta Zoologica Fennica 173:231-235.
20. _. 1986. Mastication in the musk shrew, Suncus murinus (Mammalia, Soricidae). Journal of Morphology 189:25-43.
21. DuBrul, E. L., and D. M. Laskin. 1961. Preadaptive potentialities of the mammalian skull: an experiment in growth and form. American Journal of Anatomy 109:117-132.
22. Eshel, I., and C. Matessi. 1998. Canalization, genetic assimilation and preadaptation: a quantitative genetic model. Genetics 149:2119-2133.
23. Fearnhead, R. W., C. C. D. Shute, and A. D. A. Bellairs. 1955. The temporo-mandibular joint of shrews. Proceedings of the Zoological Society of London 125:795-806.
24. Foresman, K. R. 1994. Comparative embryonic development of the Soricidae. Pages 241-258 in J. F. Merritt, G. L. J. Kirkland, and R. K. Rose, eds. Advances in the biology of shrews. Carnegie Museum of National History, Pittsburgh.
25. Foresman, K. R., and A. V. Badyaev. 2005. Developmental instability and the environment: why are some species better indicators of stress than others? Pages 1-17 in J. F. Merritt, S. Churchfield, R. Hutterer, and B. A. Sheftel, eds. Advances in the biology of shrews. Carnegie Museum of Natural History, Pittsburgh.
26. Foresman, K. R., and R. D. Long. 1998. The reproductive cycle of the vagrant shrew (Sorex vagrans) and the common shrew (Sorex cinereus) in Montana. American Midland Naturalist 139:108-113.
27. Gaughran, G. R. L. 1954. A comparative study of the osteobiology and myology of the cranial and cervical regions of the shrew, Blarina brevicauda, and the mole, Scalopus aquaticus. Miscellaneous Publications Museum of Zoology University of Michigan 80:1-82.
28. Gibson, G., and I. Dworkin. 2004. Uncovering cryptic genetic variation. Nature Reviews 5:681-690.
29. Gibson, G., and G. P. Wagner. 2000. Canalization in evolutionary genetics: a stabilizing theory? BioEssays 22:372-380.
30. Gillihan, S. W., and K. R. Foresman. 2004. Sorex vagrans. Mammalian Species 744:1-5.
31. Goldschmidt, R. B. 1940. The material basis of evolution. Yale University Press, New Haven, CT.
32. Hadany, L., and T. Beker. 2003. On the evolutionary advantage of fitness-associated recombination. Genetics 165:2167-2179.
33. Hall, B. K. 2003. Unlocking the black box between genotype and phenotype: cell condensations as morphogenetic (modular) units. Biology and Philosophy 18:219-247.
34. Hallgrímsson, B. 1998. Fluctuating asymmetry in the mammalian skeleton: evolutionary and developmental implications. Evolutionary Biology 30:187-251.
35. _. 1999. Ontogenetic patterning of skeletal fluctuating asymmetry of rhesus macaques and human: evolutionary and developmental implications. International Journal of Primatology 20:121-151.
36. Hallgrímsson, B., T. Miyake, K. Wilmore, and B. K. Hall. 2003. The embryological origins of developmental stability: size, shape and fluctuating asymmetry in prenatal random bred mice. Journal of Experimental Zoology B 296:40-57.
37. Hallgrímsson, B., K. Willmore, C. Dorval, and D. M. L. Cooper. 2004. Craniofacial variability and modularity in macaques and mice. Journal of Experimental Zoology B 302:207-225.
38. Hanken, J., M. W. Klymkowsky, K. E. Alley, and D. H. Jennings. 1997. Jaw muscle development as evidence for embryonic repatterning in direct-development frogs. Proceedings of the Royal Society of London B 264:1349-1354.
39. Helm, J. W., and R. Z. German. 1996. The epigenetic impact of weaning on craniofacial morphology during growth. Journal of Experimental Zoology 276:243-253.
40. Herring, S. W. 1993. Epigenetic and functional influences on skull growth. Pages 153-206 in J. Hanken and B. K. Hall, eds. The skull. University of Chicago Press, Chicago.
41. Herring, S. W., K. L. Rafferty, Z. J. Liu, and C. D. Marshall. 2001. Jaw muscles and the skull in mammals: the biomechanics of mastication. Comparative Biochemistry and Physiology A 131:207-219.
42. Hoffmann, A. A., and M. J. Hercus. 2000. Environmental stress as an evolutionary force. BioScience 50:217-226.
43. Hoffmann, A. A., and P. A. Parsons. 1997. Extreme environmental change and evolution. Cambridge University Press, Cambridge.
44. Huang, X., G. Zhang, and S. W. Herring. 1994. Age changes in the mastication in the pig. Comparative Biochemistry and Physiology A 107:647-654.
45. Huether, G. 1996. The central adaptation syndrome: psychosocial stress as a trigger for adaptive modifications of brain structure and brain function. Progress in Neurobiology 48:569-612.
46. Imasheva, A. G. 1999. Environmental stress and genetic variation in animal populations. Russian Journal of Genetics 35:343-351.
47. Jablonka, E., and M. J. Lamb. 1995. Epigenetic inheritance and evolution: the Lamarckian dimension. Oxford University Press, Oxford.
48. Juste, J., C. Lopez-Gonzalez, and R. E. Strauss. 2001. Analysis of asymmetries in the African fruit bats Eidolon helvum and Rousettus egyptiacus (Mammalis: Magachiroptera) from the islands of the Gulf of Guinea. II. Integration and levels of multivariate fluctuating asymmetry across a geographical range. Journal of Evolutionary Biology 14:672-680.
49. Klingenberg, C. P., and G. S. McIntyre. 1998. Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution 53:1363-1375.
50. Klingenberg, C. P., A. V. Badyaev, S. M. Sowry, and N. J. Beckwith. 2001. Inferring developmental modularity from morphological integration: analysis of individual variation and asymmetry in bumblebee wings. American Naturalist 157:11-23.
51. Lauder, G. V. 1981. Form and function: structural analysis in evolutionary morphology. Paleobiology 7:430-442.
52. Leamy, L. J. 1993. Morphological integration of fluctuating asymmetry in the mouse mandible. Genetica 89:139-153.
53. Legrell, P. E., and A. Isberg. 1999. Mandibular length and midline asymmetry after experimentally induced temporomandibular joint disk displacement in rabbits. American Journal of Orthodontics and Dentofacial Orthopedics 115:247-253.
54. Lens, L., and S. Van Dongen. 2000. Fluctuating and directional asymmetry in natural bird populations exposed to different levels of habitat disturbance, as revealed by mixture analysis. Ecology Letters 3:516-522.
55. Lipson, H., J. B. Pollack, and N. P. Suh. 2002. On the origin of modular variation. Evolution 56:1549-1556.
56. Mabee, P. M., K. L. Olmstead, and C. C. Cubbage. 2000. An experimental study of intraspecific variation, developmental timing, and heterochrony in fishes. Evolution 54:2091-2106.
57. Meiklejohn, C. D., and D. L. Hartl. 2002. A single mode of canalization. Trends in Ecology & Evolution 17:468-473.
58. Meyer, A. 1990. Morphometrics and allometry in the trophically polyphenic cichlid fish, Cichlasoma citrinellum: alternative adaptations and ontogenetic changes in shape. Journal of Zoology (London) 221:237-260.
59. Moss, M. L., and L. Salentijn. 1969. The primary role of functional matrices in facial growth. American Journal of Orthodontics 55:566-577.
60. Nanjundiah, V. 2003. Phenotypic plasticity and evolution by genetic assimilation. Pages 245-263 in G. B. Muller and S. Newman, eds. Origination of organismal form: beyond the gene in developmental and evolutionary biology. MIT Press, Cambridge, MA.
61. Newman, S. A., and G. B. Muller. 2000. Epigenetic mechanisms of character origination. Journal of Experimental Zoology 288:304-314.
62. Neyfakh, A. A., and D. L. Hartl. 1993. Genetic control of the rate of embryonic development: selection for faster development at elevated temperatures. Evolution 47:1625-1631.
63. Nijhout, H. F. 2002. The nature of robustness in development. BioEssays 24:553-563.
64. Oyama, S. 2000. The ontogeny of information: developmental systems and evolution. Duke University Press, Durham, NC.
65. Palmer, A. R. 2004. Symmetry breaking and the evolution of development. Science 306:828-833.
66. Palmer, A. R., and C. Strobeck. 2003. Fluctuating asymmetry analyses revisited. Pages 279-319 in M. Polak, ed. Developmental instability: causes and consequences. Oxford University Press, Oxford.
67. Pankakoski, E., I. Koivisto, and H. Hyvärinen. 1992. Reduced developmental stability as an indicator of heavy metal pollution in the common shrew Sorex araneus. Acta Zoologica Fennica 191:137-144.
68. Polak, M., A. P. Moller, S. W. Gangestad, D. E. Kroeger, J. T. Manning, and R. Thornhill. 2003. Does an individual asymmetry parameter exist? a meta-analysis. Pages 81-98 in M. Polak, ed. Developmental instability: causes and consequences. Oxford University Press, Oxford.
69. Price, T. D., A. Qvarnstrom, and D. E. Irwin. 2003. The role of phenotypic plasticity in driving genetic evolution. Proceedings of the Royal Society of London B 270:1433-1440.
70. Reichling, T. D., and R. Z. German. 2000. Bones, muscles and visceral organs of protein-malnourished rats (Rattus norvegicus) grow more slowly but for longer durations to reach normal final size. Journal of Nutrition 130:2326-2332.
71. Rice, S. H. 1998. Evolution of canalization and the breaking of von Baer's laws: modeling the evolution of development with epistasis. Evolution 52:647-656.
72. Riska, B. 1986. Some models for development, growth, and morphometric correlation. Evolution 40:1303-1311.
73. _. 1989. Composite traits, selection response, and evolution. Evolution 43:1172-1191.
74. Rohlf, F. J., and D. Slice. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology 39:40-59.
75. Roth, G., and D. B. Wake. 1985. Trends in the functional morphology and sensorimotor control of feeding behavior in salamanders: an example of the role of internal dynamics in evolution. Acta Biotheoretica 34:175-192.
76. Rutherford, S. L. 2003. Between genotype and phenotype: protein chaperones and evolvability. Nature Reviews 4:263-274.
77. SAS Institute. 1989. SAS/STAT user's guide. SAS Institute, Cary, NC.
78. Schlichting, C. D., and M. Pigliucci. 1998. Phenotypic evolution: a reaction norm perspective. Sinauer, Sunderland, MA.
79. Schlichting, C. D., and H. Smith. 2002. Phenotypic plasticity: linking mechanisms with evolutionary outcomes. Evolutionary Ecology 16:189-211.
80. Schmalhausen, I. I. 1949. Factors of evolution. Blakiston, Philadelphia.
81. Sharma, D. R. 1958. Studies on the anatomy of the Indian insectivore, Suncus murinus. Journal of Morphology 102:427-553.
82. Siegal, M. L., and A. Bergman. 2002. Waddington's canalization revisited: developmental stability and evolution. Proceedings of the National Academy of Sciences of the USA 99:10528-10532.
83. Smits, J. D., F. Witte, and G. D. E. Povel. 1996a. Differences between inter- and intraspecific architectonic adaptations to pharyngeal mollusc crushing in cichlid fishes. Biological Journal of the Linnean Society 59:367-387.
84. Smits, J. D., F. Witte, and F. G. Van Veen. 1996b. Functional changes in the anatomy of the pharyngeal jaw apparatus of Astatoreochromis alluaudi (Pisces, Cichlidae), and their effects on adjacent structures. Biological Journal of the Linnean Society 59:389-409.
85. 2 exposure. Honors thesis. University of Montana, Missoula.
86. Sun, Z., E. Lee, and S. W. Herring. 2004. Cranial sutures and bones: growth and fusion in relation to masticatory strain. Anatomical Record A 276:150-161.
87. Swaddle, J. P., and M. S. Witter. 1997. On the ontogeny of developmental stability in a stabilized trait. Proceedings of the Royal Society of London B 264:329-334.
88. Thompson, E. N., A. R. Biknevicius, and R. Z. German. 2003. Ontogeny of feeding function in the gray short-tailed opossum Monodelphis domestica: empirical support for the constrained model of jaw biomechanics. Journal of Experimental Biology 206:923-932.
89. Waddington, C. H. 1941. Evolution of developmental systems. Nature 147:108-110.
90. _. 1952. Genetic assimilation of an acquired character. Evolution 7:118-126.
91. Wagner, G. P. 1990. A comparative study of morphological integration in Apis mellifera (Insecta, Hymenoptera). Zeitschrift für Zoologische Systematik und Evolutionsforschung 28:48-61.
92. Wagner, G. P., and L. Altenberg. 1996. Complex adaptation and the evolution of evolvability. Evolution 50:967-976.
93. Wagner, G. P., G. Booth, and H. Bagheri-Chaichian. 1997. A population genetic theory of canalization. Evolution 51:329-347.
94. Waxman, D., and J. R. Peck. 1998. Pleiotropy and the preservation of perfection. Science 279:1210-1213.
95. West-Eberhard, M. J. 1989. Phenotypic plasticity and the origins of diversity. Annual Review of Ecology and Systematics 20:249-278.
96. _. 2003. Developmental plasticity and evolution. Oxford University Press, Oxford.
97. Wills, C. 1983. The possibility of stress-triggered evolution. Lecture Notes in Biomathematics 53:299-312.
98. Wimberger, P. H. 1991. Plasticity of jaw and skull morphology in the neotropical cichlids Geophagus brasiliensis and G. steindachneri. Evolution 45:1545-1563.
99. Zakharov, V. M., E. Pankakoski, B. I. Sheftel, A. Peltonen, and I. Hanski. 1991. Developmental stability and population dynamics in the common shrew, Sorex araneus. American Naturalist 138:797-810.