The evolutionary potential of developmental instability

Journal of Evolutionary Biology

Volumn 13, Issue 2, 2000, Pages 326-335

  Van Dongen, S ^a   Lens, L ^a,b  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b INSTITUTE OF PRIMATE RESEARCH   (Kenya)

Author keywords

Developmental instability; Evolvability; Fluctuating asymmetry; Heritability; Organism wide asymmetry; Review

Indexed keywords

DEVELOPMENTAL BIOLOGY; EVOLUTIONARY BIOLOGY; FLUCTUATING ASYMMETRY; HERITABILITY; INSTABILITY;

EID: 0034000206     PISSN: 1010061X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1420-9101.2000.00169.x     Document Type: Article

References (77)

1. Björklund, M. & Merilä, J. 1997. Why some measures of fluctuating asymmetry are so sensitive to measurement error. Annales Zool. Fennici 34: 133-137.
2. Blanckenhorn, W.U., Reusch, T. & MühlhäuSeries, C. 1998. Fluctuating asymmetry, body size and sexual selection in the dung fly Sepsis cynipsea - testing the good genes assumptions and predictions. J. Evol Biol. 11: 735-753.
3. Crespi, B.J. & Vanderkist, B.A. 1997. Fluctuating asymmetry in vestigial and functional traits of a haplodiploid insect. Heredity 79: 624-630.
4. Clarke, G.M., Oldroyd, B.P. & Hunt, P. 1992. The genetic basis of developmental stability in Apis mellifera: heterozygosity vs. genic balance. Evolution 46: 753-762.
5. Clarke, G.M. 1998a. The genetic basis of developmental stability. IV. Individual and population asymmetry parameters. Heredity 80: 553-561.
6. Clarke, G.M. 1998b. Developmental stability and fitness: the evidence is not quite so clear. Am. Natur. 152: 762-766.
7. Corruccini, R.S. & Potter, R.H.Y. 1981. Developmental correlates of crown component asymmetry and occlusal discrepancy. Am. J. Physiol. Anthropol. 55: 21-31.
8. Crnokrak, P. & Roff, D.A. 1995. Dominance variance: associations with selection and fitness. Heredity 75: 530-540.
9. Dufour, K.W. & Weatherhead, P.J. 1996. Estimation of organism-wide asymmetry in red-winged blackbirds and its relation to studies of mate selection. Proc. Royal Soc. London Series B 263: 769-775.
10. Efron, B. & Tibshirani, R.J. 1993. An introduction to the bootstrap. Monographs on Statistics and Applied Probability, Vol. 57. Chapman & Hall, NY.
11. Falconer, D.S. & Mackay, T.F.C. 1996. An Introduction to Quantitative Genetics, 4th edn. Longman, New York.
12. Fowler, K. & Whitlock, M. 1994. Fluctuating asymmetry does not increase with moderate inbreeding in Drosophila melanogaster. Heredity 73: 373-376.
13. Gangestad, S.W. & Thornhill, R. 1999. Individual differences in developmental precision and fluctuating asymmetry: a model and its implications. J. Evol. Biol. 12: 402-416.
14. Goodnight, C.J. 1988. Epistasis and the effect of founder events on the additive genetic variance. Evolution 42: 441-454.
15. Graham, J.H., Freedman, D.C. & Emlen, J.M. 1993. Antisymmetry, directional asymmetry, and dynamic morphogenesis. Genetica 89: 121-137.
16. Hoffmann, A.A. & Parsons, P.A. 1991. Evolutionary Genetics and Environmental Stress. Oxford University Press, Oxford.
17. Hoffmann, A.A. & Parsons, P.A. 1997. Consistent heritability changes under poor growth conditions. Trends Ecol. Evolution 12: 460-461.
18. Houle, D. 1992. Comparing evolvability and variability of quantitative traits. Genetics 130: 195-204.
19. Houle, D. 1997. Comment on 'A meta-analysis of the heritability of developmental stability' by Møller & Thornhill. J. Evol. Biol. 10: 17-20.
20. Jenkins, N.L., Sgró, C.M. & Hoffmann, A.A. 1997. Environmental stress and the expression of genetic variation. In: Environmental Stress, Adaptation and Evolution (R. Bijlsma & V. Loeschcke, eds), pp. 79-96. Birkäuser-Verlag, Basel.
21. Klingenberg, C.P. & Nijhout, H.F. 1999. Genetics of fluctuating asymmetry: a developmental model of developmental instability. Evolution 53: 358-375.
22. Leamy, L. 1993. Morphological integration of fluctuating asymmetry in the mouse mandible. Genetica 89: 139-153.
23. Leamy, L. 1997. Is developmental stability heritable? J. Evol. Biol. 10. 21-29.
24. Leamy, L. 1999. Heritability of directional and fluctuating asymmetry for mandibular characters in random-bred mice. J. Evol. Biol. 12: 146-155.
25. Leamy, L., Routman, E.J. & Cheverud, J.M. 1997. A search for quantitative trait loci affecting asymmetry of mandibular characters in mice. Evolution 51: 957-969.
26. Leamy, L., Routman, E.J. & Cheverud, J.M. 1998. Quantitative trait loci for fluctuating asymmetry of discrete skeletal characters in mice. Heredity 80: 509-518.
27. Leary, R.F., Allendorf, F.W. & Knudsen, K.L. 1983. Developmental stability and enzyme heterozygosity in rainbow trout. Nature 301: 71-72.
28. Leary, R.P., Allendorf, F.W. & Knudsen, K.L. 1985. Inheritance of meristic variation and the evolution of developmental stability in rainbow trout. Evolution 39: 308-314.
29. Lens, L. & Van Dongen, S. 1999. Evidence for organism-wide asymmetry in five bird species of a fragmented afrotropical forest. Proc. Royal Soc. London Series B 266: 1055-1060.
30. Leung, B. & Forbes, M.R. 1996. Fluctuating asymmetry in relation to stress and fitness: effects of trait type as revealed by meta-analysis. Ecoscience 3: 400-413.
31. Littell, R.C., Milliken, G.A., Stroup, W.W. & Wolfinger, R.D. 1996. SAS® System for Mixed Models. SAS Institute Inc., New York.
32. Ludwig, W. 1932. Das Rechts-Links Problem Im Tierreich und Beim Menschen. Springer Berlin.
33. Lynch, M. & Walsh, B. 1997. Genetics and Analysis of Quantitative Traits. Sinaur Ass. Inc., Sunderland, MA.
34. Manning, J.T. & Chamberlain, A.T. 1994. Fluctuating asymmetry in gorilla canines: a sensitive indicator of environmental stress. Proc. Royal Soc. London Series B 255: 189-193.
35. Markow, T.A. 1995. Evolutionary ecology and developmental instability. Annu. Rev. Entomology 40: 105-120.
36. Markow, T.A. & Clarke, G.M. 1997. Meta-analysis of the heritability of developmental stability: a giant step backward. J. Evol. Biol. 10: 31-37.
37. Markusson, E. & Folstad, I. 1997. Reindeer antlers: visual indicators of individual quality? Oecologia 110: 501-507.
38. Merilä, J. 1997. Expression of genetic variation in body size of the collared flycatcher under different environmental conditions. Evolution 51: 526-536.
39. Møller, A.P. 1997. Developmental stability and fitness: a review. Am. Naturalist 149: 916-932.
40. Møller, A.P. & Pomiankowski, A. 1993. Fluctuating asymmetry and sexual selection. Genetica 89: 267-279.
41. Møller, A.P. & Thornhill, R. 1997. A meta-analysis of the heritability of developmental stability. J. Evol. Biol. 10: 1-16.
42. Møller, A.P. & Thornhill, R. 1998. Bilateral symmetry and sexual selection: a meta-analysis. Am. Naturalist 151: 174-192.
43. Neter, J., Wasserman, W. & Kutner, M.H. 1990. Applied Linear Statistical Models. Irwin Inc., Boston, MA.
44. Otronen, M. 1998. Male asymmetry and postcopulatory sexual selection in the fly Dryomyza anilis. Behav Ecol. Sociobiology 42: 185-191.
45. Palmer, A.R. 1994. Fluctuating asymmetry analyses: a primer. In: Developmental Instability: its Origins and Evolutionary Implications (T. A. Markow, ed.), pp. 355-363. Kluwer Academic Publishers, Dordrecht.
46. Palmer, A.R. 1996. Waltzing with asymmetry. Bioscience 46: 518-532.
47. Palmer, A.R. & Strobeck, C. 1986. Fluctuating asymmetry: measurement, analysis, patterns. Annu. Rev. Ecol. Syst 17: 391-421.
48. 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 Zool. Fennica 191: 57-72.
49. Pomiankowski, A. 1997. Genetic variation in fluctuating asymmetry. J. Evol. Biol. 10: 51-55.
50. Radesäter, T. & Halldórsdóttir, H. 1993. Fluctuating asymmetry and forceps size in earwigs, Forficula auricularia. Anim. Behav. 45: 626-628.
51. Rowe, L., Repasky, R.R. & Palmer, A.R. 1997. Size dependent asymmetry: fluctuating asymmetry versus antisymmetry and its relevance to condition-dependent signaling. Evolution 51: 1401-1408.
52. Scheiner, S.M., Caplan, R.L. & Lyman, R.F. 1991. The genetics of phenotypic plasticity. III. Genetic correlations and fluctuating asymmetries. J. Evol. Biol. 4: 51-68.
53. Sgró, C.M. & Hoffmann, A.A. 1998a. Effects of stress combinations on the expression of additive genetic variation for fecundity in Drosophila melanogaster. Genet. Res. 72: 13-18.
54. Sgró, C.M. & Hoffmann, A.A. 1998b. Effects of temperature extremes on genetic variances for life-history traits in Drosophila melanogaster as determined by parent-offspring comparisons. J. Evol. Biol. 11: 1-20.
55. Simons, A.M. & Johnston, M.O. 1997. Developmental instability as a bet-hedging strategy. Oikos 80: 401-406.
56. Soulé, M.E. 1982. Allomeric variation. I. The theory and some consequences. Am. Naturalist 120: 751-764.
57. Soulé, M.E. & Cuzin-Roudy, J. 1982. Allometric variation. 2. Developmental instability of extreme phenotypes. Am. Naturalist 120: 765-786.
58. Swaddle, J.P. 1997. Developmental stability and predation success in an insect predator-prey system. Behav. Ecol. 8: 433-436.
59. Swaddle, J.P. & Witter, M.S. 1997. On the ontogeny of developmental stability in a stabilised trait. Proc. R. Soc. Lond. B 264: 329-334.
60. Tsubaki, Y. & Matsumoto, K. 1998. Fluctuating asymmetry and male mating success in a Sphragis-Bearing butterfly Luehdorfia japonica (Lepidoptera: Papilionidae). J. Insect Behaviour 11: 571-582.
61. Van Dongen, S. 1997. The population structure of the winter moth Operophtera brumata in relation to local adaptation and habitat fragmentation. PhD dissertation, Antwerp.
62. Van Dongen, S. 1998a. How repeatable is the estimation of individual fluctuating asymmetry. Proc. Royal Soc. London Series B 263: 1423-1427.
63. Van Dongen, S. 1998b. The distribution of individual fluctuating asymmetry: why are the coefficients of variation so high? Annalles Zool. Fennici 35: 79-85.
64. Van Dongen, S. 1999. Accuracy and power in the statistical analysis of fluctuating asymmetry: effects of between individual heterogeneity in developmental instability. Annalles Zool. Fennici 36: 45-52.
65. Van Dongen, S., Sprengers, E., Löfstedt, C. & Matthysen, E. 1999a. Heritability of tibia fluctuating asymmetry and developmental instability in the winter moth (Operophtera brumata L.) (Lepidoptera, Geometridae). Heredity 82: 535-542.
66. Van Dongen, S., Sprengers, E. & Löfstedt, C. 1999b. Correlated development, organism-wide asymmetry and patterns of asymmetry in two moth species. Genetica 105: 81-91.
67. Van Dongen, S., Lens, L. & Molenberghs, G. 1999c. Mixture analysis of asymmetry: modeling directional asymmetry, antisymmetry and heterogeneity in fluctuating asymmetry. Ecol. Lett. 6: 387-396.
68. Van Valen, L. 1962. A study of fluctuating asymmetry. Evolution 16: 125-142.
69. Verbeke, G. & Molenberghs, G. 1997. Linear mixed models in practice: A SAS oriented approach. Lecture Notes in Statistics, Vol. 126. Springer, NY.
70. Wade, M.J., Shuster, S.M. & Stevens, L. 1996. Inbreeding: its effect on response to selection for pupal weight and the heritable variance in fitness in the flour beetle, Tribolium castaneum. Evolution 50: 723-733.
71. Wang, J., Caballero, A., Keightley, P.D. & Hill, W.G. 1998. Bottleneck effect on genetic variance: a theoretical investigation of the role of dominance. Genetics 150: 435-447.
72. Whitlock, M. 1996. The heritability of fluctuating asymmetry and the genetic control of developmental stability. Proc. Royal Soc. London Series B 263: 849-854.
73. Whitlock, M. 1998. The repeatability of fluctuating asymmetry: a revision and extension. Proc. Royal Soc. London Series B 265: 1428-1430.
74. Whitlock, M. & Fowler, K. 1997. The instability of studies of instability. J. Evol. Biol. 10: 63-67.
75. Willis, J.H. & Orr, H.A. 1993. Increased heritable variation following population bottlenecks: the role of dominance. Evolution 47: 949-957.
76. Windig, J.J. 1998. Evolutionary genetics of fluctuating asymmetry in the peacock butterfly (Inachis io). Heredity 80: 382-392.
77. Zakharov, V.M. 1992. Population phenogenetics: analysis of developmental stability in natural populations. Acta Zool. Fennica 191: 7-30.