Developmental and genetic constraints on neurocranial globularity: Insights from analyses of deformed skulls and quantitative genetics

Evolutionary Biology

Volumn 36, Issue 1, 2009, Pages 37-56

  Martínez Abadías, Neus ^a   Paschetta, Carolina ^b   de Azevedo, Soledad ^b   Esparza, Mireia ^a   González José, Rolando ^b  

^a UNIVERSITY OF BARCELONA   (Spain)

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

Author keywords

Artificial deformation; Constraints; Geometric morphometrics; Morphological integration; Neurocranial globularity; Quantitative genetics

Indexed keywords

EID: 69849101823     PISSN: 00713260     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11692-008-9045-4     Document Type: Article

References (109)

1. Ackermann, R. R., & Cheverud, J. M. (2004). Morphological integration in primate evolution. In M. Pigliucci & K. Preston (Eds.), Phenotypic integration: Studying the ecology and evolution of complex phenotypes (pp. 302-319). Oxford: Oxford University Press.
2. Alberch, P. (1982). Developmental constraints in evolutionary processes. In J. T. Bonner (Ed.), Evolution and development (pp. 313-332). Berlin: Springer.
3. Antón, S. C. (1989). Intentional cranial vault deformation and induced changes of the cranial base and face. American Journal of Physical Anthropology, 79, 253-267. doi:10.1002/ajpa.1330790213.
4. Antón, S. C. (1994). Biomechanical and other perspectives on the Neandertal face. In R. Corruccini & R. Ciochon (Eds.), Integrated pathways to the past (pp. 677-695). Englewood Cliffs, NJ: Prentice-Hall.
5. Antón, S. C., Jaslow, C. R., & Swartz, S. M. (1992). Sutural complexity in artificially deformed human (Homo sapiens) crania. Journal of Morphology, 214, 321-332. doi:10.1002/jmor.1052140307.
6. Antón, S. C., & Weinstein, K. J. (1999). Artificial cranial deformation and fossil Australians revisited. Journal of Human Evolution, 36, 195-209. doi:10.1006/jhev.1998.0266.
7. Antonovics, J., & van Tienderen, P. H. (1991). Ontoecogenophyloconstraints? The chaos of constraint terminology. Trends in Ecology & Evolution, 6, 166-168. doi:10.1016/0169-5347(91)90059-7.
8. Arnold, S. J., Pfrender, M. E., & Jones, A. G. (2001). The adaptive landscape as a conceptual bridge between micro- and macroevolution. Genetica, 112(113), 9-32. doi:10.1023/A:1013373907708.
9. Arthur, W. (1997). The origin of animal body plans: a study in evolutionary developmental biology. Cambridge: Cambridge University Press.
10. Atchley, W. R., & Hall, B. K. (1991). A model for development and evolution of complex morphological structures. Biological Reviews of the Cambridge Philosophical Society, 66, 101-157. doi:10.1111/j.1469-185X.1991.tb01138.x.
11. Babler, W. J., Persing, J. A., Nagorsky, M. J., & Jane, J. A. (1987). Restricted growth at the frontonasal suture: alterations in craniofacial growth in rabbits. The American Journal of Anatomy, 178, 90-98. doi:10.1002/aja.1001780112.
12. Bastir, M. (2004). Análisis de morfometría geométrica de la variación e integración morfológica en el cráneo humano y sus implicaciones para los homínidos de Atapuerca-SH y la evolución de los Neandertales PhD. Dissertation. Madrid: Universidad Autónoma de Madrid.
13. Bastir, M., & Rosas, A. (2004). Facial heights: evolutionary relevance of postnatal ontogeny for facial orientation and skull morphology in humans and chimpanzees. Journal of Human Evolution, 47, 359-381. doi:10.1016/j.jhevol.2004.08.009.
14. Bastir, M., & Rosas, A. (2005). Hierarchical nature of morphological integration and modularity in the human posterior face. American Journal of Physical Anthropology, 128, 26-34. doi:10.1002/ajpa.20191.
15. Bastir, M., Rosas, A., & Kuroe, K. (2004). Petrosal orientation and mandibular ramus breadth: Evidence for an integrated petroso-mandibular developmental unit. American Journal of Physical Anthropology, 123, 340-350. doi:10.1002/ajpa.10313.
16. Bastir, M., Sobral, P. G., Kuroe, K., & Rosas, A. (2007). Human craniofacial sphericity: A simultaneous analysis of frontal and lateral cephalograms of a Japanese population using geometric morphometrics and partial least squares analysis. Archives of Oral Biology, 53, 295-303. doi:10.1016/j.archoralbio.2007.09.011.
17. Biegert, J. (1963). The evaluation of characteristics of the skull, hands and feet for primate taxonomy. In S. L. Washburn (Ed.), Classification and human evolution (pp. 116-145). Chicago: Aldine.
18. Bolker, J. A. (2000). Modularity in development and why it matters to evo-devo. American Zoologist, 40, 740-776. doi:10.1668/0003-1569(2000)040[0770:MIDAWI]2.0.CO;2.
19. Bookstein, F. L., Gunz, P., Mitteroecker, P., Prossinger, H., Schaefer, K., & Seidler, H. (2003). Cranial integration in Homo: Singular warps analysis of the midsagittal plane in ontogeny and evolution. Journal of Human Evolution, 44, 167-187. doi:10.1016/S0047-2484(02)00201-4.
20. Buikstra, J. E., & Ubelaker, D. H. (1994). Standards for data collection from human skeletal remains. Fayetteville, Arkansas: Arkansas archeological Survey Research Series NO 44.
21. Chase, K., Carrier, D. R., Alder, F. R., Jarvik, T., Ostrander, E. A., Lorentzen, T. D., et al. (2002). Genetic basis for systems of skeletal quantitative traits: Principal component analysis of the canid skeleton. Proceedings of the National Academy of Sciences of the United States of America, 99, 9930-9935. doi:10.1073/pnas.152333099.
22. Cheverud, J. M. (1984). Quantitative genetics and developmental constraints on evolution by selection. Journal of Theoretical Biology, 110, 155-171. doi:10.1016/S0022-5193(84)80050-8.
23. Cheverud, J. M. (1996). Developmental integration and the evolution of pleiotropy. American Zoologist, 36, 44-50.
24. Cheverud, J. M., Kohn, L. A., Konigsberg, L. W., & Leigh, S. R. (1992). Effects of fronto-occipital artificial cranial vault modification on the cranial base and face. American Journal of Physical Anthropology, 88, 323-345. doi:10.1002/ajpa.1330880307.
25. Collard, M., & Wood, B. A. (2007). Defining the genus Homo. In W. Henke, T. Hardt, & I. Tattersall (Eds.), Handbook of paleoanthropology (pp. 1575-1610). Berlin-Heidelberg: Springer.
26. Day, M. H., & Stringer, C. B. (1982). A reconsideration of the Omo Kibish remains and the erectus-sapiens transition. In 1er Congr Internat Paleont Hum (pp. 814-846). Prétirage. Nice.
27. Day, M. H., & Stringer, C. B. (1991). Les restes crâniens d'Omo Kibish et leur classification à l'interieur du genre Homo. L'Anthropologie, 95, 573-594.
28. De Beer, G. (1937). The Development of the Vertebrate Skull. Oxford: Clarendon Press.
29. Dembo, A., & Imbelloni, J. (1938). Deformaciones intencionales del cuerpo humano de carácter étnico. Buenos Aires: Humanior.
30. Dryden, I. L., & Mardia, K. V. (1998). Statistical shape analysis. Chichester: Wiley.
31. Enlow, D. (1990). Facial growth. Philadelphia: Saunders.
32. Falconer, D. S., & MacKay, T. F. C. (1996). Introduction to quantitative genetics. Longman Group, Ltd: Essex.
33. González-José, R. (2003). El poblamiento de la Patagonia. Análisis de la variación craneofacial en el contexto del poblamiento Americano. Ph.D. Dissertation. Barcelona: Universitat de Barcelona.
34. González-José, R., Escapa, I., Neves, W. A., Cuneo, R., & Pucciarelli, H. M. (2008). Cladistic analysis of continuous modularized traits provides phylogenetic signals in Homo evolution. Nature, 453, 775-778. doi:10.1038/nature06891.
35. González-José, R., García-Moro, C., Dahinten, S., & Hernández, M. (2002). Origin of Fueguian-Patagonians: an approach to population history and structure using R matrix and matrix permutation methods. American Journal of Human Biology, 14, 308-320. doi:10.1002/ajhb.10033.
36. González-José, R., Martínez-Abadías, N., Van der Molen, S., García-Moro, C., Dahinten, S., & Hernández, M. (2004a). Hipótesis acerca del poblamiento de Tierra del Fuego-Patagonia a partir del análisis genético-poblacional de la variación craneofacial. Magallania, 32, 78-79.
37. González-José, R., Ramírez-Rozzi, F., Sardi, M., Martínez-Abadías, N., Hernández, M., & Pucciarelli, H. M. (2005). Functional-cranial approach to the influence of economic strategy on skull morphology. American Journal of Physical Anthropology, 128, 757-771. doi:10.1002/ajpa.20161.
38. González-José, R., Van der Molen, S., González-Pérez, E., & Hernández, M. (2004b). Patterns of phenotypic covariation and correlation in modern humans as viewed from morphological integration. American Journal of Physical Anthropology, 123, 69-77. doi:10.1002/ajpa.10302.
39. Gould, S. J. (1989). A developmental constraint in Cerion, with comments on the definition and interpretation of constraint in evolution. Evolution; International Journal of Organic Evolution, 43, 516-539. doi:10.2307/2409056.
40. Gunz, P., & Harvati, K. (2007). The Neanderthal "chignon": variation, integration, and homology. Journal of Human Evolution, 52, 262-274. doi:10.1016/j.jhevol.2006.08.010.
41. Hall, B. K. (1996). Baupläne, phylotypic stages and constraint. Why are there so few types of animals. In M. K. Hecht (Ed.), Evolutionary Biology (Vol. 29, pp. 215-261). New York: Plenum Press.
42. Hall, B. K. (2005). Bones and cartilage: Developmental and evolutionary skeletal biology. San Diego, CA: Elsevier Academic Press.
43. Hallgrímsson, B., & Lieberman, D. E. (2008). Mouse models and the evolutionary developmental biology of the skull. Integrative and Comparative Biology, 48, 373-384. doi:10.1093/icb/icn076.
44. Hallgrímsson, B., Lieberman, D. E., Liu, W., Ford-Hutchinson, A. F., & Jirik, F. R. (2007a). Epigenetic interactions and the structure of phenotypic variation in the cranium. Evolution & Development, 9, 76-91. doi:10.1111/j.1525-142X.2006.00139.x.
45. Hallgrímsson, B., Lieberman, D. E., Young, N. M., Parsons, T., & Wat, S. (2007b). Evolution of covariance in the mammalian skull. Novartis Foundation Symposium, 284, 164-185. doi:10.1002/9780470319390.ch12.
46. Howells, W. W. (1973). Cranial variation in man. Papers of the peabody museum of archaeology and ethnology. Cambridge, Massachusetts, USA: Harvard University.
47. Jiang, X., Iseki, S., Maxson, R. E., Sucov, H. M., & Morriss-Kay, G. M. (2002). Tissue origins and interactions in the mammalian skull vault. Developmental Biology, 241, 106-116. doi:10.1006/dbio.2001.0487.
48. Klingenberg, C. P. (2005). Developmental constraints, modules, and evolvability. In B. Hallgrímsson & B. K. Hall (Eds.), Variation. A central concept in biology (pp. 219-247). San Diego (CA): Elsevier Academic Press.
49. Klingenberg, C. P. (2008). MorphoJ. Faculty of Life Sciences, University of Manchester, UK. http://www.flywings.org.uk/MorphoJ_page.htm.
50. Klingenberg, C. P., & Leamy, L. J. (2001). Quantitative genetics of geometric shape in the mouse mandible. Evolution; International Journal of Organic Evolution, 55, 2342-2352.
51. Klingenberg, C. P., Leamy, L. J., Routman, E. J., & Cheverud, J. M. (2001). Genetic architecture of mandible shape in mice: Effects of quantitative trait loci analyzed by geometric morphometrics. Genetics, 157, 785-802.
52. Klingenberg, C. P., & Monteiro, L. R. (2005). Distances and directions in multidimensional shape spaces: implications for morphometric applications. Systematic Biology, 54, 678-688. doi:10.1080/10635150590947258.
53. Kohn, L. A., Leigh, S. R., & Cheverud, J. M. (1995). Asymmetric vault modification in Hopi crania. American Journal of Physical Anthropology, 98, 173-195. doi:10.1002/ajpa.1330980207.
54. Kohn, L. A., Leigh, S. R., Jacobs, S. C., & Cheverud, J. M. (1993). Effects of annular cranial vault modification on the cranial base and face. American Journal of Physical Anthropology, 90, 147-168. doi:10.1002/ajpa.1330900203.
55. Kovac, M., & Groeneveld, E. (2003). VCE-5, User's guide and reference manual. Version 5.1.
56. Kreiborg, S. (1981). Crouzon syndrome. A clinical and roentgencephalometric study. Scandinavian Journal of Plastic and Reconstructive Surgery. Supplementum, 18, 1-198.
57. Kruuk, L. E. (2004). Estimating genetic parameters in natural populations using the "animal model". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 359, 873-890. doi:10.1098/rstb.2003.1437.
58. Lahr, M. M. (1996). The evolution of modern human diversity: a study of cranial variation. Cambridge: Cambridge University Press.
59. Lande, R. (1979). Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry. Evolution; International Journal of Organic Evolution, 33, 402-416. doi:10.2307/2407630.
60. Lande, R., & Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution; International Journal of Organic Evolution, 37, 1210-1226. doi:10.2307/2408842.
61. Lieberman, D. E. (1995). Testing hypotheses about recent human evolution from skulls. Current Anthropology, 36, 159-197. doi:10.1086/204348.
62. Lieberman, D. E. (1997). Making behavioral and phylogenetic inferences from hominid fossils: considering the developmental influence of mechanical forces. Annual Review of Anthropology, 26, 185-210. doi:10.1146/annurev.anthro.26.1.185.
63. Lieberman, D. E., Krovitz, G. E., & McBratney-Owen, B. (2004). Testing hypotheses about tinkering in the fossil record: The case of the human skull. Journal of Experimental Zoology. Part B. Molecular and Developmental Evolution, 302, 284-301.
64. Lieberman, D. E., McBratney, B. M., & Krovitz, G. (2002). The evolution and development of cranial form in Homo sapiens. Proceedings of the National Academy of Sciences of the United States of America, 99, 1134-1139. doi:10.1073/pnas.022440799.
65. Lieberman, D. E., & McCarthy, R. C. (1999). The ontogeny of cranial base angulation in humans and chimpanzees and its implications for reconstructing pharyngeal dimensions. Journal of Human Evolution, 36, 487-517. doi:10.1006/jhev.1998.0287.
66. Lieberman, D. E., Pearson, O. M., & Mowbray, K. M. (2000). Basicranial influence on overall cranial shape. Journal of Human Evolution, 38, 291-315. doi:10.1006/jhev.1999.0335.
67. Luis, M. A., Lustig, A. L., Sardi, M. L., Ponce, P. V., & Pucciarelli, H. M. (1999). Posición de los araucanos en un contexto asiático-europeo II: Metodología Howelliana. Revista Argentina de Antropología Biológica, 2, 187-200.
68. Lynch, J. M., & Walsh, B. (1998). Genetic analysis of quantitative traits. Sunderland, MA: Sinauer Associates.
69. Marroig, G., & Cheverud, J. M. (2005). Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in New World monkeys. Evolution; International Journal of Organic Evolution, 59, 1128-1142.
70. Martínez-Abadías, N. (2007). Evolutionary patterns of the human skull. A quantitative genetic analysis of craniofacial phenotypic variation. Ph.D. Dissertation. Barcelona: Universitat de Barcelona.
71. Maynard Smith, J., Burian, R., Kauffman, S. A., Alberch, P., Campbell, J., Goodwin, B. C., et al. (1985). Developmental constraints and evolution. The Quarterly Review of Biology, 60, 265-287. doi:10.1086/414425.
72. McCarthy, R. C., & Lieberman, D. E. (2001). Posterior maxillary (PM) plane and anterior cranial architecture in primates. The Anatomical Record, 264, 247-260. doi:10.1002/ar.1167.
73. McGuigan, K. (2006). Studying phenotypic evolution using multivariate quantitative genetics. Molecular Ecology, 15, 883-896. doi:10.1111/j.1365-294X.2006.02809.x.
74. Merilä, J., & Björklund, M. (2004). Phenotypic integration as a constraint and adaptation. In M. Pigliucci & K. Preston (Eds.), Phenotypic integration: Studying the ecology and evolution of complex phenotypes (pp. 107-129). Oxford: Oxford University Press.
75. Moss, M. L. (1959). The pathogenesis of premature cranial synostosis in man. Acta Anatomica, 37, 351-370. doi:10.1159/000141479.
76. Moss, M. L. (1968). The primacy of functional matrices in orofacial growth. Transactions of the British Society of Study of Orthodontics and Dental Practice, 19, 65-73.
77. Moss, M., & Young, R. (1960). A functional approach to craniology. American Journal of Physical Anthropology, 18, 281-291. doi:10.1002/ajpa.1330180406.
78. Olson, E. C., & Miller, R. L. (1958). Morphological integration. Chicago: University of Chicago Press.
79. Paschetta, C.A., de Azevedo, S., Castillo, L., Martínez-Abadías, N., Hernández, M., Lieberman, D.E., & González-José, R. (2008). The influence of masticatory loading on craniofacial morphology: A test case across technological transitions in the Ohio Valley (submitted paper).
80. Pigliucci, M., & Preston, K. (2004). Phenotypic integration. Studying the ecology and evolution of complex phenotypes. New York: Oxford University Press.
81. Ponce de León, M. S., & Zollikofer, C. P. (2001). Neanderthal cranial ontogeny and its implications for late hominid diversity. Nature, 412, 534-538. doi:10.1038/35087573.
82. Pucciarelli, H. M. (1978). The influence of experimental deformation on craniofacial development in rats. American Journal of Physical Anthropology, 48, 455-461. doi:10.1002/ajpa.1330480403.
83. Raff, R. A. (1996). The shape of life; genes, development and the evolution of animal form. Chicago: University of Chicago Press.
84. Richardson, M. K., & Chipman, A. D. (2003). Developmental constraints in a comparative framework: A test case using variations in phalanx number during amniote evolution. The Journal of Experimental Zoology, 296B, 8-22. doi:10.1002/jez.b.13.
85. Richtsmeier, J. T. (1987). Comparative study of normal, Crouzon, and Apert craniofacial morphology using finite element scaling analysis. American Journal of Physical Anthropology, 74, 473-493. doi:10.1002/ajpa.1330740407.
86. Richtsmeier, J. T. (1988). Craniofacial growth in apert syndrome as measured by finite-element scaling analysis. Acta Anatomica, 133, 50-56. doi:10.1159/000146614.
87. Richtsmeier, J. T. (2002). Cranial vault dysmorphology and growth in craniosynostosis. In M. P. Mooney, & M. I. Siegel (Eds.), Understanding craniofacial anomalies. The ethiopathogenesis of craniosynostoses and facial clefting (pp. 321-341). Wiley-Liss.
88. Rightmire, G. P. (2007). Later middle Pleistocene Homo. In W. Henke, T. Hardt, & I. Tattersall (Eds.), Handbook of paleoanthropology (pp. 1695-1715). Berlin-Heidelberg: Springer.
89. Rohlf, F. J., & Corti, M. (2000). Use of two-block partial least-squares to study covariation in shape. Systematic Biology, 49, 740-753. doi:10.1080/106351500750049806.
90. Rohlf, F. J., & Slice, D. E. (1990). Extensions of Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39, 40-59. doi:10.2307/2992207.
91. Ross, C. F., & Ravosa, M. J. (1993). Basicranial flexion, relative brain size, and facial kyphosis in nonhuman primates. American Journal of Physical Anthropology, 91, 305-324. doi:10.1002/ajpa.1330910306.
92. Sardi, M. L., & Pucciarelli, H. M. (2001). Influencia de la deformación artificial indeterminada en las comparaciones craneanas interpoblacionales. Revista Argentina de Antropología Biológica, 3, 23-34.
93. Schwenk, K. (1995). A utilitarian approach to evolutionary constraint. Zoology (Jena, Germany),98, 251-262.
94. Sciulli, P. W. (1998). Evolution of the dentition in prehistoric Ohio Valley Native Americans: II. Morphology of the deciduous dentition. American Journal of Physical Anthropology, 106, 189-205. doi:10.1002/(SICI)1096-8644(199806)106:2<189::AID-AJPA6>3.0.CO;2-L.
95. Sciulli, P. W. (2001). Evolution of dentition in prehistoric Ohio Valley Native Americans III. Metrics of deciduous dentition. American Journal of Physical Anthropology, 116, 140-153. doi:10.1002/ajpa.1107.
96. Sheets, H. D. (2004). IMP ThreeDStand6.
97. Sheets, H. D. (2005). IMP PLS3d.
98. Sjøvold, T. (1984). A report on the heritability of some cranial measurements and non-metric traits. In G. N. Van Vark & W. W. Howells (Eds.), Multivariate statistical methods in physical anthropology (pp. 223-246). Dordrecht: Reidel Publishing Company.
99. Sjøvold, T. (1995). Testing assumptions for skeletal studies by means of identified skulls from Hallstat, Austria. In S. R. Saunders & A. Herring (Eds.), Grave reflections: Portraying the past through cemetery studies (pp. 241-281). Toronto: Canadian Scholars Press Inc.
100. Sperber, G. (2001). Craniofacial development. London: BC Decker Inc.
101. Steppan, S. J., Phillips, P. C., & Houle, D. (2002). Comparative quantitative genetics: Evolution of the G matrix. Trends in Ecology & Evolution, 17, 320-327. doi:10.1016/S0169-5347(02)02505-3.
102. Strait, D. S. (2001). Integration, phylogeny, and the hominid cranial base. American Journal of Physical Anthropology, 114, 273-297. doi:10.1002/ajpa.1041.
103. Strait, D. S., & Grine, F. E. (2004). Inferring hominoid and early hominid phylogeny using craniodental characters: the role of fossil taxa. Journal of Human Evolution, 47, 399-452. doi:10.1016/j.jhevol.2004.08.008.
104. Strait, D. S., Grine, F. E., & Fleagle, J. G. (2007). Analyzing hominid phylogeny. In W. Henke, T. Hardt, & I. Tattersall (Eds.), Handbook of paleoanthropology (pp. 1782-1806). Berlin-Heidelberg: Springer.
105. Tatarek, N. E., & Sciulli, P. W. (2000). Comparison of population structure in Ohio's late archaic and late prehistoric periods. American Journal of Physical Anthropology, 112, 363-376. doi:10.1002/1096-8644(200007)112:3<363::AID-AJPA7>3.0.CO;2-Y.
106. Tattersall, I. (2002). The Monkey in the mirror: Essays on the science of what makes us human. Oxford: Oxford University Press.
107. Weidenreich, F. (1941). The brain and its role in the phylogenetic transformation of the human skull. Transactions of the American Philosophical Society, 31, 320-442. doi:10.2307/1005610.
108. Wolpoff, M. H. (1980). Paleoanthropology. New York: McGraw-Hill.
109. Zelditch, M. L., Swiderski, D. L., Sheets, H. D., & Fink, W. L. (2004). Geometric morphometric for biologists. London: Elsevier Academic Press.