Developmental plasticity in covariance structure of the skull: Effects of prenatal stress

Journal of Anatomy

Volumn 218, Issue 2, 2011, Pages 243-257

  Gonzalez, Paula N ^a   Hallgrímsson, Benedikt ^b   Oyhenart, Evelia E ^c  

^a FACULTAD DE CIENCIAS NATURALES Y MUSEO   (Argentina)

^b UNIVERSITY OF CALGARY   (Canada)

^c Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

Developmental process; Intrauterine growth retardation; Nutritional stress; Variance covariance structure; Wistar rat

Indexed keywords

SOMATOMEDIN;

ARTICLE; CONTROLLED STUDY; COVARIANCE; ENVIRONMENTAL FACTOR; FETUS DEVELOPMENT; INTRAUTERINE GROWTH RETARDATION; MORPHOLOGY; NONHUMAN; NUTRITION; ONTOGENY; PHENOTYPE; PRENATAL DEVELOPMENT; PRENATAL STRESS; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; RAT; SKULL; SKULL RADIOGRAPHY; VARIANCE; WISTAR RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; FEMALE; FETAL GROWTH RETARDATION; MALE; PHENOTYPE; PREGNANCY; RATS; RATS, WISTAR; SKULL; STRESS, PHYSIOLOGICAL;

RATTUS; RATTUS NORVEGICUS;

EID: 78650903456     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2010.01326.x     Document Type: Article

References (70)

1. Adams DC, Rohlf FJ, Slice DE (2004) Geometric morphometrics: ten years of progress following the 'revolution'. Ital J Zool 71, 5-16.
2. Allan GJ, Flint DJ, Patel K (2001) Insulin-like growth factor axis during embryonic development. Reproduction 122, 31-39.
3. Aubin-Horth N, Renn SC (2009) Genomic reaction norms: using integrative biology to understand molecular mechanisms of phenotypic plasticity. Mol Ecol 18, 3763-3780.
4. Badyaev AV (2005) Role of stress in evolution: from individual adaptability to evolutionary adaptation. In: Variation. A Central Concept in Biology (eds Hallgrímsson B, Hall BK), pp. 277-302. New York: Academic Press (Elsevier).
5. Bloomfield FH, Oliver MH, Harding JE (2006) The late effects of fetal growth patterns. Arch Dis Child Fetal Neonatal 91, 299-304.
6. Bookstein FL (1991) Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge: Cambridge University Press.
7. Bookstein FL (1997) Landmark methods for forms without landmarks: localizing group differences in outline shape. Med Image Anal 1, 225-243.
8. Bookstein FL, Streissguth AP, Sampson PD, et al. (2002) Corpus callosum shape and neuropsychological deficits in adult males with heavy fetal alcohol exposure. Neuroimage 15, 233-251.
9. Bulygina E, Mitteroecker P, Aiello L (2006) Ontogeny of facial dimorphism and patterns of individual development within one human population. Am J Phys Anthropol 131, 432-443.
10. Calvalcanti MJ (2008) Mantel for windows, Version 1.18. Freeware available at.
11. Cheverud JM (1996) Developmental integration and the evolution of pleiotropy. Am Zool 36, 44-50.
12. Dahinten S, Pucciarelli HM (1986) Variations in sexual dimorphism in the skulls of rats subjected to malnutrition, castration, and treatment with gonadal hormones. Am J Phys Anthropol 71, 63-67.
13. DeChiara TM, Efstratiadis A, Robertson EJ (1990) A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 345, 78-80.
14. Dressino V, Pucciarelli HM (1996) Efecto nutricional sobre el crecimiento craniofacial de Saimiri sciureus (Cebidae). Un estudio experimental. Rev Arg Antrop Biol 1, 98-112.
15. Fowden AL (2003) The insulin-like growth factors and feto-placental growth. Placenta 24, 803-812.
16. Fowden AL, Giussani DA, Forhead AJ (2006) Intrauterine programming of physiological systems: causes and consequences. Physiology 21, 29-37.
17. Frankino WA, Raff RA (2004) Evolutionary importance and pattern of phenotypic plasticity: insights gained from development. In: Phenotypic Plasticity: Functional and Conceptual Approaches (eds DeWitt TJ, Scheiner SM), pp. 64-81. New York: Oxford University Press.
18. Fu Q, Yu X, Callaway CW, et al. (2009) Epigenetics: intrauterine growth retardation (IUGR) modifies the histone code along the rat hepatic IGF-1 gene. FASEB J 23, 2438-2449.
19. Gilbert SF, Epel D (2009) Ecological Developmental Biology: Integrating Epigenetics, Medicine, and Evolution. Sunderland: Sinauer.
20. Gluckman PD, Hanson MA (2004) Living with the past: evolution, development, and patterns of disease. Science 305, 1733-1736.
21. Gower JC (1971) Statistical methods of comparing different multivariate analyses of the same data. In: Mathematics in the Archaeological and Historical Sciences (eds Hodson FR, Kendall DG, Tautu P), pp. 138-149. Edinburgh: Edinburgh University Press.
22. Hall BK (2003) Evo-devo: evolutionary developmental mechanisms. Int J Dev Biol 47, 491-495.
23. Hallgrímsson B (1999) Ontogenetic patterning of skeletal fluctuating asymmetry in rhesus macaques and humans: evolutionary and developmental implications. Int J Primatol 20, 121-151.
24. Hallgrímsson B, Lieberman DE (2008) Mouse models and the evolutionary developmental biology of the skull. Integr Comp Biol 48, 373-384.
25. Hallgrímsson B, Willmore K, Dorval C, et al. (2004) Craniofacial variability and modularity in macaques and mice. J Exp Zool (Mol Dev Evol) 302, 207-225.
26. Hallgrímsson B, Lieberman DE, Young NM, et al. (2007) Evolution of covariance in the mammalian skull. In: Tinkering - The Microevolution of Development (Novartis Found Symp 284), pp. 164-190. Chichester: John Wiley & Sons Ltd.
27. Hallgrímsson B, Jamniczky H, Young N, et al. (2009) Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic covariation. Evol Biol 36, 355-376.
28. Hingst-Zaher E, Marcus L, Cerqueira R (2000) Application of geometric morphometrics to postnatal size and shape changes in the skull of Calomys expulsus. Hystrix, It J Mamm 11, 99-113.
29. Jackson DA (1995) PROTEST: a Procrustean randomization test of community environment concordance. Écoscience 2, 297-303.
30. Jamniczky HA, Hallgrímsson B (2009) A comparison of covariance structure in wild and laboratory muroid crania. Evolution 63, 1540-1556.
31. Klingenberg CP (2005) Developmental constraints, modules and evolvability. In: Variation. A Central Concept in Biology (eds Hallgrímsson B, Hall BK), pp. 219-247. New York: Academic Press (Elsevier).
32. Le Roith D, Werner H, Beitner-Johnson D, et al. (1995) Molecular and cellular aspects of the insulin-like growth factor I receptor. Endocr Rev 16, 143-163.
33. Le Roith D, Bondy C, Yakar S, et al. (2001) The Somatomedin hypothesis: 2001. Endocr Rev 22, 53-74.
34. Marroig G, Cheverud JM (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.
35. Martín MA, Serradas P, Ramos S, et al. (2005) Protein-caloric food restriction affects insulin-like growth factor system in fetal Wistar rat. Endocrinology 146, 1364-1371.
36. Miller JP, German RZ (1999) Protein malnutrition affects the growth trajectories of the craniofacial skeleton in rats. J Nutr 129, 2061-2069.
37. Mitteroecker P, Bookstein FL (2007) The conceptual and statistical relationship between modularity and morphological integration. Syst Biol 56, 818-836.
38. Mitteroecker P, Bookstein FL (2009) The ontogenetic trajectory of the phenotypic covariance matrix, with examples from craniofacial shape in rats and humans. Evolution 63, 727-737.
39. Mitteroecker P, Gunz P, Bernhard M, et al. (2004) Comparison of cranial ontogenetic trajectories among hominoids. J Hum Evol 46, 679-698.
40. Monteiro LS, Falconer DS (1966) Compensatory growth and sexual maturity in mice. Anim Prod 8, 179-192.
41. Moss ML, Vilmann H (1978) Studies on orthocephalization of the rat head. I. A model system for the study of adjustive cranial growth processes. Gegenbaurs Morphol Jahrb 124, 559-579.
42. Nijhout HF (2003) The control of growth. Development 130, 5863-5867.
43. Noble D (2002) The rise of computational biology. Nature 3, 460-463.
44. Nonaka K, Nakata M (1988). Genetic and environmental factors in the longitudinal growth of rats. III. Craniofacial shape change. J Craniofac Genet Dev Biology 8, 337-344.
45. Oyhenart EE, Orden B, Fucini MC, et al. (2003) Sexual dimorphism and postnatal growth of intrauterine growth retarded rats. Growth Dev Aging 67, 73-83.
46. Pavlicev M, Cheverud JM, Wagner GP (2009) Measuring morphological integration using eigenvalue variance. Evol Biol 36, 157-170.
47. Peres-Neto PR, Jackson DA (2001) How well do multivariate data sets match? The advantages of a Procrustean superimposition approach over the Mantel test. Oecologia 129, 169-178.
48. Perez SI, Bernal V, Gonzalez PN (2006) Differences between methods to sliding semi-landmarks: its importance in human population analyses. J Anat 208, 769-784.
49. Pigliucci M (2004) Studying the plasticity of phenotypic integration in a model organism. In: Phenotypic Integration. Studying the Ecology and Evolution of Complex Phenotypes (eds Pigliucci M, Preston K), pp. 155-175. New York: Oxford University Press.
50. Pigliucci M, Cammell K, Schmitt J (1999) Evolution of phenotypic plasticity a comparative approach in the phylogenetic neighbourhood of Arabidopsis thaliana. J Evol Biol 12, 779-791.
51. Pucciarelli HM, Dressino V (1996) Orthocephalization in the postweaning squirrel monkey. Am J Phys Anthropol 101, 173-181.
52. R Development Core Team (2008) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing,.
53. Relyea RA (2004) Integrating phenotypic plasticity when death is on the line: insights from predator-prey systems. In: Phenotypic Integration. Studying the Ecology and Evolution of Complex Phenotypes (eds Pigliucci M, Preston K), pp. 176-190. New York: Oxford University Press.
54. Revell RJ (2007) Skewers software. Available at /~liam/programs/.
55. Riska B, Atchley WR, Rutledge JJ (1984) A genetic analysis of targeted growth in mice. Genetics 107, 79-101.
56. Roff D (2000) The evolution of the G matrix: selection or drift? Heredity 84, 135-142.
57. Rohlf FJ (1993) Relative warps analysis and an example of its application to Mosquito wings. In: Contributions to Morphometrics (eds Marcus LF, Bello E, García-Valdecasas A), pp. 132-159. Madrid: Monografías del Museo Nacional de Ciencias Naturales.
58. Rohlf FJ (2007) tps serie softwares. Available at.
59. Rohlf FJ, Slice DE (1990) Extensions of the procrustes method for the optimal superimposition of landmarks. Syst Zool 39, 40-59.
60. Salazar-Ciudad I, Jernvall J, Newman SA (2003) Mechanisms of pattern formation in development and evolution. Development 130, 2027-2037.
61. Sheets HD (2003) IMP-Integrated Morphometrics Package. Buffalo, NY: Department of Physics, Canisius College.
62. Sultan SE, Stearns SC (2005) Environmentally contingent variation: phenotypic plasticity and norms of reaction. In: Variation. A Central Concept in Biology (eds Hallgrímsson B, Hall BK), pp. 303-332. New York: Academic Press (Elsevier).
63. Wagner GP (1990) A comparative study of morphological integration in Apis mellifera (Insecta, Hymenoptera). Z Zool Syst Evolut-forsch 28, 48-61.
64. Wagner GP, Pavlicev M, Cheverud J (2007) The road to modularity. Nat Genet 8, 921-931.
65. Willmore KE, Leamy L, Hallgrímsson B (2006) Effects of developmental and functional interactions on mouse cranial variability through late ontogeny. Evol Dev 8, 550-567.
66. Zelditch ML (2005) Variation developmental regulation of variability. In: Variation. A Central Concept in Biology (eds Hallgrímsson B, Hall BK), pp. 249-276. New York: Academic Press (Elsevier).
67. Zelditch ML, Carmichael AC (1989) Ontogenetic variation in patterns of developmental and functional integration in skulls of Sigmodon fulviventer. Evolution 43, 814-824.
68. Zelditch ML, Bookstein FL, Lundrigan BL (1992) Ontogeny of integrated skull growth in the cotton rat Sigmodon fulviventer. Evolution 46, 1164-1180.
69. Zelditch ML, Lundrigan BL, Garland T (2004) Developmental regulation of skull morphology. I. Ontogenetic dynamics of variance. Evol Dev 6, 194-206.
70. Zelditch ML, Mezey J, Sheets HD, et al. (2006) Developmental regulation of skull morphology II: ontogenetic dynamics of covariance. Evol Dev 8, 46-60.