Shape, variance and integration during craniogenesis: Contrasting marsupial and placental mammals

Journal of Evolutionary Biology

Volumn 25, Issue 5, 2012, Pages 862-872

  Goswami, A ^a   Polly, P D ^b   Mock, O B ^c   Sanchez Villagra M R ^d  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b INDIANA UNIVERSITY   (United States)

^c A T STILL UNIVERSITY   (United States)

^d PALÄONTOLOGISCHES INSTITUT UND MUSEUM   (Switzerland)

Author keywords

Constraint; Cranial integration; Marsupials; Ontogeny; Placentals

Indexed keywords

ASSESSMENT METHOD; COMPARATIVE STUDY; CRANIUM; EXTINCTION; FUNCTIONAL MORPHOLOGY; LABORATORY METHOD; MARSUPIAL; NUMERICAL MODEL; ONTOGENY; SHAPE; SMALL MAMMAL; TAXONOMY; VARIANCE ANALYSIS;

ANIMAL; ARTICLE; BONE DEVELOPMENT; COMPARATIVE STUDY; EVOLUTION; FEMALE; GROWTH, DEVELOPMENT AND AGING; MORPHOGENESIS; OPOSSUM; PHYSIOLOGY; PREGNANCY; PRENATAL DEVELOPMENT; PRINCIPAL COMPONENT ANALYSIS; SHREW; SKULL; SPECIES DIFFERENCE; STAINING; TIME;

ANIMALS; BIOLOGICAL EVOLUTION; FEMALE; MONODELPHIS; MORPHOGENESIS; OSTEOGENESIS; PREGNANCY; PRINCIPAL COMPONENT ANALYSIS; SHREWS; SKULL; SPECIES SPECIFICITY; STAINING AND LABELING; TIME FACTORS;

CRYPTOTIS; CRYPTOTIS PARVA; DIDELPHIDAE; EUTHERIA; MAMMALIA; METATHERIA; MONODELPHIS; MONODELPHIS DOMESTICA; MUS;

EID: 84859443927     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2012.02477.x     Document Type: Article

References (60)

1. Ackermann, R.R. 2005. Ontogenetic integration of the hominoid face. J. Hum. Evol. 48: 175-197.
2. Ackermann, R.R. & Cheverud, J.M. 2004. Morphological integration in primate evolution. In: Phenotypic Integration (M. Pigliucci & K. Preston, eds), pp. 302-319. Oxford University Press, Oxford.
3. Bennett, C.V. & Goswami, A. 2011a. Does reproductive strategy drive limb integration in marsupials and monotremes? Mammalian Biol. 76: 79-83.
4. Bennett, C.V. & Goswami, A. (2011b) Morphological constraint in the metatherian cranium. In: Society of Vertebrate Paleontology Annual Meeting, Program and Abstracts. pp., Las Vegas, USA.
5. Boughner, J.C., Wat, S., Diewert, V.M., Young, N.M., Browder, L.W. & Hallgrimsson, B. 2008. Short-faced mice and developmental interactions between the brain and the face. J. Anat. 213: 646-662.
6. Burt, C. 1948. Factor analysis and canonical correlations. Br. J. Psychol. 1: 95-106.
7. Goswami, A. 2006a. Cranial modularity shifts during mammalian evolution. Am. Nat. 168: 270-280.
8. Goswami, A. 2006b. Morphological integration in the carnivoran skull. Evolution 60: 169-183.
9. Goswami, A. 2007a. Cranial integration, phylogeny, and diet in australodelphian marsupials. PLoS ONE 2: e995.
10. Goswami, A. 2007b. Cranial modularity and sequence heterochrony in mammals. Evol. Dev. 9: 290-298.
11. Goswami, A. & Polly, P.D. 2010a. The influence of modularity on cranial morphological diversity in Carnivora and Primates (Mammalia; Placentalia). PLoS ONE 5: e9517.
12. Goswami, A. & Polly, P.D. (2010b). Methods for studying morphological integration and modularity. In: Quantitative Methods in Paleobiology (J. Alroy & E.G. Hunt, eds). Paleontological Society Papers 16: 213-243.
13. Goswami, A., Weisbecker, V. & Sánchez-Villagra, M.R. 2009. Developmental modularity and the marsupial-placental dichotomy. J. Exp. Zool. 312B: 186-195.
14. Goswami, A., Milne, N. & Wroe, S. 2011. Biting through constraints: cranial morphology, disparity, and convergence across living and fossil carnivorous mammals. Proc. Biol. Sci. 278: 1831-1839.
15. Hallgrimsson, B., Willmore, K., Dorval, C. & Cooper, D.M.L. 2004. Craniofacial variability and modularity in macaques and mice. J. Exp. Zool. B Mol. Dev. Evol. 302B: 207-225.
16. Hallgrimsson, B., Jamniczky, H., Young, N.M., Rolian, C., Parsons, T.E., Boughner, J.C. et al. 2009. Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic covariation. Evol. Biol. 36: 355-376.
17. Hotelling, H. 1936. Relations between two sets of variates. Biometrika 28: 321.
18. Kelly, E.M. & Sears, K.E. 2011. Reduced integration in marsupial limbs and the implications for mammalian evolution. Biol. J. Linn. Soc. 102: 22-36.
19. Keyte, A.L. & Smith, K.K. (2008). Opossum (Monodelphis domestica): a marsupial developmental model. In: Emerging Model Organisms: A Laboratory Manual, Vol. 1 (D.A. Crotty & A. Gann, eds), pp. 557-576. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
20. Klingenberg, C.P. (2008a). MorphoJ. . Faculty of Life Sciences, University of Manchester, Manchester, UK.
21. Klingenberg, C.P. 2008b. Morphological integration and developmental modularity. Ann. Rev. Ecol. Evol. Syst. 39: 115-132.
22. Klingenberg, C.P. 2010. Evolution and development of shape: integrating quantitative approaches. Nat. Genet. 11: 623-635.
23. Koyabu, D., Endo, H., Mitgutsch, C., Suwa, G., Catania, K.C., Zollikofer, C.P.E. et al. 2011. Heterochrony and developmental modularity of cranial osteogenesis in lipotyphlan mammals. EvoDevo 2: 21.
24. Lillegraven, J.A. 1975. Biological considerations of the marsupial-placental dichotomy. Evolution 29: 707-722.
25. Mantel, N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Res. 27: 209-220.
26. Marroig, G. & Cheverud, J.M. 2004. Cranial evolution in sakis (Pithecia, platyrrhini) I: interspecific differentiation and allometric patterns. Am. J. Phys. Anthropol. 125: 266-278.
27. Marroig, G., Vivo, M. & Cheverud, J.M. 2004. Cranial evolution in sakis (Pithecia, Platyrrhini) II: evolutionary processes and morphological integration. J. Evol. Biol. 17: 144-155.
28. Marroig, G., Shirai, L., Porto, A., de Oliveira, F.B. & De Conto, V. 2009. The evolution of modularity in the mammalian skull II: evolutionary consequences. Evol. Biol. 36: 136-148.
29. Mitteroecker, P. & Bookstein, F. 2009. The ontogenetic trajectory of the phenotypic covariance matrix, with examples from craniofacial shape in rats and humans. Evolution 63: 727-737.
30. Mock, O.B. 1982. The least shrew (Cryptotis parva) as a laboratory animal. Lab. Anim. Sci. 32: 177-179.
31. Noden, D.M. & Schneider, R.A. 2006 Neural crest cells and the community of plan for craniofacial development: historical debates and current perspectives. In: Neural Crest Induction and Differentiation, Vol. 589 (J.-P. Saint-Jeannet, ed.), pp. 1-23. Advances in Experimental Medicine and Biology. Landes Bioscience, Georgetown, TX.
32. Nowak, R.M. 1999. Walker's Mammals of the World, 6th edn. Johns Hopkins University Press, Baltimore, MD.
33. de Oliveira, F.B., Porto, A. & Marroig, G. 2009. Covariance structure in the skull of Catarrhini: a case of pattern stasis and magnitude evolution. J. Hum. Evol. 56: 417-430.
34. Olson, E.C. & Miller, R.L. 1958. Morphological Integration. University of Chicago Press, Chicago.
35. Pavlicev, M., Cheverud, J.M. & Wagner, G.P. 2009. Measuring morphological integration using eigenvalue variance. Evol. Biol. 36: 157-170.
36. Porto, A., de Oliveira, F.B., Shirai, L., De Conto, V. & Marroig, G. 2009. The evolution of modularity in the mammalian skull I: morphological integration patterns and magnitudes. Evol. Biol. 36: 118-135.
37. Prochel, J. 2006. Early skeletal development in Talpa europaea, the common European mole. Zool. Sci. 23: 427-434.
38. Rohlf, F.J. 1990. Rotational fit (procrustes) methods. In: Proceedings of the Michigan Morphometrics Workshop (F.J. Rohlf & F.L. Bookstein, eds), pp. 227-236. University of Michigan Museum of Zoology, Ann Arbor.
39. Sánchez-Villagra, M.R. 2002. Comparative patterns of postcranial ontogeny in therian mammals: an analysis of relative timing of ossification events. J. Exp. Zool. B Mol. Dev. Evol. 294B: 264-273.
40. Sánchez-Villagra, M.R., Goswami, A., Weisbecker, V., Mock, O. & Kuratani, S. 2008. Conserved relative timing of cranial ossification patterns in early mammalian evolution. Evol. Dev. 10: 519-530.
41. Schlosser, G. & Wagner, G.P. 2004. Introduction. In: Modularity in Development and Evolution (G. Schlosser & G.P. Wagner, eds), pp. 1-11. University of Chicago Press, Chicago.
42. Schoch, R.R. 2006. Skull ontogeny: developmental patterns of fishes conserved across major tetrapod clades. Evol. Dev. 8: 524-536.
43. Sears, K.E. 2004. The role of constraints in the morphological evolution of marsupial shoulder girdles: evidence from comparative anatomy, paleontology, and embryology. Evolution 58: 2353-2370.
44. Smith, K.K. 1996. Integration of craniofacial structures during development in mammals. Am. Zool. 36: 70-79.
45. Smith, K.K. 1997. Comparative patterns of craniofacial development in eutherian and metatherian mammals. Evolution 51: 1663-1678.
46. Smith, K.K. 2001. Heterochrony revisited: the evolution of developmental sequences. Biol. J. Linn. Soc. 73: 169-186.
47. Smith, K.K. 2002. Sequence heterochrony and the evolution of development. J. Morphol. 252: 82-97.
48. Smith, K.K. 2006. Craniofacial development in marsupial mammals: developmental origins of evolutionary change. Dev. Dyn. 236: 1181-1193.
49. Wagner, G.P. 1996. Homologues, natural kinds and the evolution of modularity. Am. Zool. 36: 36-43.
50. Wagner, G.P. & Altenberg, L. 1996. Perspective: complex adaptations and the evolution of evolvability. Evolution 50: 967-976.
51. Weisbecker, V., Goswami, A., Wroe, S. & Sánchez-Villagra, M.R. 2008. Ossification heterochrony in the therian postcranial skeleton and the marsupial-placental dichotomy. Evolution 59: 2691-2704.
52. Willmore, K.E., Leamy, L. & Hallgrimsson, B. 2006. Effects of developmental and functional interactions on mouse cranial variability through late ontogeny. Evol. Dev. 8: 550-567.
53. Wilson, L.A.B. 2011. Comparison of prenatal and postnatal ontogeny: cranial allometry in the African striped mouse Rhabodomys pumilio. J. Mammal. 92: 407-420.
54. Young, N. & Hallgrimsson, B. 2005. Serial homology and the evolution of mammalian limb covariation structure. Evolution 59: 2691-2704.
55. Zelditch, M.L. 1988. Ontogenetic variation in patterns of phenotypic integration in the laboratory rat. Evolution 42: 28-41.
56. Zelditch, M.L. & Carmichael, A.C. 1989a. Growth and intensity of integration through postnatal growth in the skull of Sigmodon fulviventer. J. Mammal. 70: 477-484.
57. Zelditch, M.L. & Carmichael, A.C. 1989b. Ontogenetic variation in patterns of developmental and functional integration in skulls of Sigmodon fuliviventer. Evolution 43: 814-824.
58. Zelditch, M.L., Bookstein, F.L. & Lundrigan, B.L. 1992. Ontogeny of integrated skull growth in the cotton rat Sigmodon fulviventer. Evolution 46: 1164-1180.
59. Zelditch, M.L., Lundrigan, B.L. & Garland, T. 2004. Development regulation of skull morphology I. Ontogenetic dynamics of variance. Evol. Dev. 6: 194-206.
60. Zelditch, M.L., Mezey, J.G., Sheets, H.D., Lundrigan, B.L. & Garland, T., Jr 2006. Developmental regulation of skull morphology II: ontogenetic dynamics of covariance. Evol. Biol. 8: 46-60.