The relationship between fluctuating asymmetry and environmental variance in rhesus macaque skulls

Evolution

Volumn 59, Issue 4, 2005, Pages 898-909

  Willmore, Katherine Elizabeth ^a   Klingenberg, Christian Peter ^b   Hallgrímsson, Benedikt ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Canalization; Environmental variance; Fluctuating asymmetry; Macaca mulatta; Morphometrics; Quantitative genetics

Indexed keywords

ADAPTATION; ENVIRONMENTAL CONDITIONS; MORPHOMETRY; PHENOTYPIC PLASTICITY; SKULL;

CRANIA; MACACA; MACACA MULATTA; PROCRUSTES;

EID: 17844390413     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2005.tb01763.x     Document Type: Article

References (61)

1. Barnett, V., and T. Lewis. 1994. Outliers in statistical data. 3rd ed. Wiley series in probability and statistics. John Wiley and Sons, New York.
2. Carroll, S. B., J. K. Grenier, and S. D. Weatherbee. 2005. From DNA to diversity: molecular genetics and the evolution of animal design. 2nd ed. Blackwell Publishing, Malden, MA.
3. Cheverud, J. M. 1982. Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution 36:499-516.
4. Cheverud, J. M., G. P. Wagner, and M. M. Dow. 1989. Methods for the comparative analysis of variation patterns. Syst. Zool. 38:201-213.
5. Clarke, G. M. 1993. The genetic basis of developmental stability. I. Relationships between stability, heterozygosity and genomic coadaptation. Genetica 89:15-23.
6. _. 1998. The genetic basis of developmental stability. V. Inter-and intra-individual character variation. Heredity 80:562-567.
7. Crow, J., and M. Kimura. 1977. An introduction to population genetic theory. Burgess, Minneapolis, MN.
8. Daegling, D. J. 2004. Relationship of strain magnitude to morphological variation in the primate skull. Am. J. Phys. Anthropol. 124:346-352.
9. Debat, V., P. Alibert, P. David, E. Paradis, and J.-C. Auffray. 2000. Independence between developmental stability and canalization in the skull of the house mouse. Proc. R. Soc. Lond. B 267: 423-430.
10. Emlen, J. M., D. C. Freeman, and J. H. Graham. 1993. Nonlinear growth dynamics and the origin of fluctuating asymmetry. Genetica 89:77-96.
11. Falconer, D. S., and T. F. C. Mackay. 1996. Introduction to quantitative genetics. Addison Wesley Longman, Harlow, U.K.
12. Francis-West, P. H., L. Robson, and D. J. R. Evans. 2003. Craniofacial development: the tissue and molecular interactions that control development of the head. Pp. 1-144 in F. Beck, B. Christ, W. Kriz, W. Kummer, E. Marani, R. Putz, Y. Sano, T. H. Schiebler, G. C. Schoenwolf, and K. Zilles, eds. Advances in anatomy embryology and cell biology. Vol. 169. Springer-Verlag, Berlin.
13. Gilbert, S. F. 2003. Developmental biology. 7th ed. Sinauer Associates, Sunderland, MA.
14. Hall, B. K. 1999. The neural crest in development and evolution. Springer-Verlag, New York.
15. Hall, B. K., and T. Miyake. 2000. All for one and one for all: condensations and the initiation of skeletal development. Bioessays 22:138-147.
16. Hallgrímsson, B., K. Willmore, and B. K. Hall. 2002. Canalization, developmental stability, and morphological integration in primate limbs. Yearb. Phys. Anthropol. 45:131-158.
17. Hallgrímsson, B., K. Willmore, C. Dorval, and D. M. L. Cooper. 2004. Craniofacial variability and modularity in macaques and mice. J. Exp. Zool. B Mol. Dev. Evol. 302B:207-225.
18. Hallgrímsson, B., C. J. Dorval, M. L. Zeldtich, and R. Z. German. 2004. Craniofacial variability and morphological integration in mice susceptible to cleft lip and palate. J. Anat. 205:501-517.
19. Hallgrímsson, B., J. J. Y. Brown, and B. K. Hall. 2005. The study of phenotypic variability: an emerging research agenda for understanding the developmental-genetic architecture underlying phenotypic variation. In B. Hallgrímsson and B. K. Hall, eds. Variation: a central concept in biology. Elsevier Academic Press, San Diego, CA. In press.
20. Henderson, J. H., M. T. Longaker, and D. R. Carter. 2004. Sutural bone deposition rate and strain magnitude during cranial development. Bone 34:271-280.
21. Herring, S. W. 1993. Epigenetic and functional influences on skull growth. Pp. 153-206 in J. Hanken, and B. K. Hall, eds. The skull. Vol. 1. Univ. of Chicago Press, Chicago.
22. Herring, S. W., and S. Teng. 2000. Strain in the braincase and its sutures during function. Am. J. Phys. Anthropol. 112:575-593.
23. Herring, S. W., J. D. Decker, Z. L. Liu, and T. Ma. 2002. Temporomandibular joint in miniature pigs: anatomy, cell replication, and relation to loading. Anat. Rec. 266:152-166.
24. Klingenberg, C. P. 2003. A developmental perspective on developmental instability: theory, models, and mechanisms. Pp. 14-34 in M. Polak, ed. Developmental instability: causes and consequences. Oxford Univ. Press, Oxford, U.K.
25. Klingenberg, C. P., and G. S. McIntyre. 1998. Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution 52: 1363-1375.
26. Klingenberg, C. P., and H. F. Nijhout. 1999. Genetics of fluctuating asymmetry: a developmental model of developmental instability. Evolution 53:358-375.
27. Klingenberg, C. P., and S. D. Zaklan. 2000. Morphological integration between developmental compartments in the Drosophila wing. Evolution 54:1273-1285.
28. 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. Am. Nat. 157:11-23.
29. Klingenberg, C. P., M. Barluenga, and A. Meyer. 2002. Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56:1909-1920.
30. Klingenberg, C. P., K. Mebus, and J.-C. Auffray. 2003. Developmental integration in a complex morphological structure: How distinct are the modules in the mouse mandible? Evol. Dev. 5: 522-531.
31. Lande, R. 1977. On comparing coefficients of variation. Syst. Zool. 26:214-217.
32. Leamy, L. J., E. J. Routman, and J. M. Cheverud. 2002. An epistatic genetic basis for fluctuating asymmetry of mandible size in mice. Evolution 56:642-653.
33. Lele, S., and J. T. Richtsmeier. 2001. An invariant approach to the statistical analysis of shapes. Chapman and Hall, Boca Raton, FL.
34. Lewontin, R. C. 1966. On the measurement of relative variability. Syst. Zool. 15:141-142.
35. Lieberman, D. E., C. F. Ross, and M. J. Ravosa. 2000. The primate cranial base: ontogeny, function, and integration. Yearb. Phys. Anthropol. 43:117-169.
36. Marquez, E. 2004. Mace3D. University of Michigan Museum of Zoology, Ann Arbor, MI.
37. Milton, C. C., B. Huynh, P. Batterham, S. L. Rutherford, and A. A. Hoffmann. 2003. Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of canalization and developmental stability. Proc. Natl. Acad. Sci. USA 100:13396-13401.
38. Moss, M. L. 1968. The primacy of functional matrices in orogacial growth. Dental Practitioner 19:65-73.
39. Noden, D. M. 1978. The control of avian cephalic neural crest cytodifferentiation. I. Skeletal and connective tissue. Dev. Biol. 69:296-312.
40. O'Higgins, P., and N. Jones. 1998. Morphologika. University College, London.
41. Palmer, A. R. 1994. Fluctuating asymmetry analyses: a primer. Pp. 355-364 in T. A. Markow, ed. Developmental instability: its origins and evolutionary implications. Kluwer Academic Publishers, Dordrecht, The Netherlands.
42. Palmer, A. R., and C. Strobeck. 1986. Fluctuating asymmetry: measurement, analysis, patterns. Annu. Rev. Ecol. Syst. 17:391-421.
43. _. 2003. Fluctuating asymmetry analysis revisited. Pp. 279-319 in M. Polak, ed. Developmental instability: causes and consequences. Oxford Univ. Press, Oxford, U.K.
44. Queitsch, C., T. A. Sangster, and S. Lindquist. 2002. Hsp90 as a capacitor of phenotypic variation. Nature 417:618-624.
45. Rafferty, K. L., S. W. Herring, and F. Artese. 2000. Three-dimensional loading and growth of the zygomatic arch. J. Exp. Biol. 203:2093-3004.
46. Rawlins, R. G., and M. J. Kessler. 1986. Demography of the free-ranging Cayo Santiago macaques (1976-1983). Pp. 47-72 in R. G. Rawlins and M. J. Kessler, eds. The Cayo Santiago macaques: history, behavior and biology. State Univ. of New York Press, Albany, NY.
47. Réale, D., and D. A. Roff. 2003. Inbreeding, developmental stability, and canalization in the sand cricket Gryllus firmus. Evolution 57:597-605.
48. Richtsmeier, J. T., V. Burke de Leon, and S. R. Lele. 2002. The promise of geometric morphometrics. Yearb. Phys. Anthropol. 45:63-91.
49. Rutherford, S. L. 2000. From genotype to phenotype: buffering mechanisms and the storage of genetic information. BioEssays 22:1095-1105.
50. Rutherford, S. L., and S. Lindquist. 1998. Hsp90 as a capacitor for morphological evolution. Nature 396:336-342.
51. Schmalhausen, I. I. 1949. Factors of evolution: the theory of stabilizing selection. Univ. of Chicago Press, Chicago.
52. Siegal, M. L., and A. Bergman. 2002. Waddington's canalization revisited: developmental stability and evolution. Proc. Natl. Acad. Sci. USA 99:10528-10532.
53. Slice, D. E. 1994-1999. Morpheus. State University of New York, Stony Brook, NY.
54. VanValen, L. M. 1978. The statistics of variation. Evol. Theor. 4: 33-43.
55. Waddington, C. H. 1957. The strategy of the genes. MacMillan, New York.
56. Wood, B., and D. E. Lieberman. 2001. Craniodental variation in Paranthropus boisei: a developmental and functional perspective. Am. J. Phys. Anthropol. 116:13-25.
57. Woods, R. E., C. M. Sgrò, M. J. Hercus, and A. A. Hoffmann. 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.
58. Wright, S. 1952. The genetics of quantitative variability. Pp. 5-41 in E. C. R. Reeve and C. Waddington, eds. Quantitative inheritance. Her Majesty's Stationery Office, London.
59. Zakharov, V. M. 1992. Population phenogenetics: analysis of developmental stability in natural populations. Acta. Zool. Fenn. 191:7-30.
60. Zelditch, M. L., D. L. Swiderski, H. D. Sheets, and W. L. Fink. 2004a. Geometric morphometrics for biologists: a primer. Elsevier Academic Press, San Diego, CA.
61. Zelditch, M. L., B. L. Lundrigan, and T. Garland Jr. 2004b. Developmental regulation of skull morphology. I. Ontogenetic dynamics of variance. Evol. Dev. 6:194-206.