Covariación ontogénica en el endocráneo de Pan troglodytes / Ontogenetic covariation in the endocranium of Pan troglodytes
Resumen
RESUMEN Diversos estudios proponen que el neurocráneo en Homo sapiens es una estructura integrada y que la morfología de la bóveda y la base se asocia con modificaciones del cerebro. En este estudio se evaluó la covariación ontogénica en el endocráneo de Pan troglodytes, otro primate altamente encefalizado. Se analizaron 52 reconstrucciones 3D derivadas de tomografías computadas de individuos adultos y subadultos. Una vez segmentadas las cavidades endocraneanas, se relevaron 27 landmarks. A partir de su configuración, se obtuvieron el tamaño del centroide y las coordenadas de Procrustes y se realizó Análisis de Componentes Principales, regresión, correlación, ANOVA y análisis F de Goodall a fin de evaluar los cambios de tamaño y forma respecto de la edad y las alometrías. Los cambios en forma están fuertemente integrados y se producen hasta etapas tardías de la ontogenia: elongación de la bóveda y la base, distanciamiento entre el foramen magnun y la placa cribiforme, retroflexión del ángulo basicraneano y descenso de los polos temporales. A partir del análisis PLS se observó que los cambios en la base y la bóveda covarían, pero cuando se ajustó el efecto alométrico, dicha covariación se hizo no significativa, tal como ocurre en Homo sapiens. Esto sugiere que el aumento ontogénico del volumen endocraneano -en relación con el crecimiento cerebral- constituye un factor común de integración entre la bóveda y la base en ambas especies. Sin embargo, es probable que en el chimpancé se sume la influencia de distintas estructuras faciales que promuevan variación y covariación en el endocráneo.
PALABRAS CLAVE chimpancé; tomografía computada; integración; cerebro
ABSTRACT Several studies propose that the neurocranium in Homo sapiens is an integrated structure, being the growing brain the factor that influences the vault and the base morphology. The goal of this study is to assess endocranial ontogenetic covariation in Pan troglodytes, another encephalized primate. Fifty-two 3D reconstructions derived from computed tomographies of adult and subadult specimens were analyzed. After segmentation of the endocranial volumes, twenty-seven landmarks were registered. Through their configuration, centroid size and Procrustes coordinates were obtained, and Principal Components Analysis, regression, correlation, ANOVA and Goodall’s F-test were performed in order to evaluate size and shape changes against age and allometries. The results indicated that significant morphological ontogenetic shape changes are highly integrated and they occur up to the late ontogeny: elongation of the vault and the base, separation of the foramen magnum and the cribiform plate, retroflection of the basicranial angle, and descent of the temporal poles. By means of PLS analysis, a significant covariation between the vault and the base was obtained. However, when the allometric effect was adjusted, the covariation became non-significant, as occurs in Homo sapiens. This suggests that the ontogenetic increase in the endocranial volume —related to the growing brain— may be a common integrative factor between the vault and the base in both species. Nonetheless, different facial structures are also likely to promote variation and covariation in the chimpanzee’s endocranium.
KEY WORDS chimpanzee; computed tomography; integration; brain
doi: 10.17139/raab.2014.0016.02.02
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Aiello L, Dean C. 2002. An introduction to human evolutionary anatomy. Londres: Elsevier Academic Press.
Barbeito-Andrés J, Ventrice F, Anzelmo M, Pucciarelli HM, Sardi ML. 2013. Estudio transversal sobre la covariación ontogénica entre la base y la bóveda craneana humana. En: Avena S, Lois MV, compiladores. Libro de resúmenes. Undécimas Jornadas Nacionales de Antropología Biológica. Buenos Aires. p 93.
Bastir M, Rosas A. 2004. Comparative ontogeny in humans and chimpanzees: similarities, differences and paradoxes in postnatal growth and development of the skull. Ann Anat 186:503-509. doi:10.1016/S0940-9602(04)80096-7
Bastir M, Rosas A, O’Higgins P. 2006. Craniofacial levels and morphological maturation of the human skull. J Anat 209:637-654. doi:10.1111/j.1469-7580.2006.00644.x
Berge C, Penin X. 2004. Ontogenetic allometry, heterochrony, and interspecific differences in the skull of African apes, using tridimensional Procrustes analysis. Am J Phys Anthropol 124:124-138. doi:10.1002/ajpa.10333
Bookstein FL. 1991. Morphometric tools for landmark data: geometry and biology. Cambridge: Cambridge University Press.
Bookstein FL, Gunz P, Miteroecker P, Prossinger H, Schaefer K, Seidler H. 2003. Cranial integration in Homo: singular warps analysis of the midsagittal plane in ontogeny and evolution. J Hum Evol 44:167-187. doi:10.1016/S0047-2484(02)00201-4
Bruner E, Ripani M. 2008. A quantitative and descriptive approach to morphological variation of the endocranial base in modern humans. Am J Phys Anthropol 137:31-40. doi:10.1002/ajpa.20837
Chernoff B, Magwene PM. 1999. Morphological integration: forty years later. En: Olson EC, Miller RL, editores. Morphological integration. Chicago: The University of Chicago. p 319-353.
Cobb SN, O’Higgins P. 2004. Hominins do not share a common postnatal facial ontogenetic shape trajectory. J Exper Zool (Mol Dev Evol) 302B:302-321. doi:10.1002/jez.b.21005
Coqueugniot H, Hublin JJ. 2012. Age-related changes of digital endocranial volume during human ontogeny: results from an osteological reference collection. Am J Phys Anthropol 147:312-318. doi:10.1002/ajpa.21655
Coqueugniot H, Hublin J-J, Veillon F, Houët J-J, Jacob T. 2004. Early brain growth in Homo erectus and implications for cognitive ability. Nature 431:299-302. doi:10.1038/nature02852
Dean MC, Wood BA. 1981. Developing pongid dentition and its use for ageing individual crania in comparative cross-sectional growth studies. Folia Primatol 36:111-127. doi:10.1159/000156011
Dean MC, Wood BA. 1984. Phylogeny, neoteny and growth of the cranial base in hominoids. Folia Primatol 43:157-180. doi:10.1159/000156177
DeSilva J, Lesnik J. 2006. Chimpanzee neonatal brain size: implications for brain growth in Homo erectus. J Hum Evol 51:207-212. doi:10.1016/j.jhevol.2006.05.006
Dryden IL, Mardia KV. 1998. Statistical shape analysis. London: John Wiley.
Durrleman S, Pennec X, Trouvé A, Ayache N, Braga J. 2012. Comparison of the endocranial ontogenies between chimpanzees and bonobos via temporal and spatiotemporal registration. J Hum Evol 62:74-88. doi:10.1016/j.jhevol.2011.10.004
Goodall CR. 1991. Procrustes methods and the statistical analysis of shape. J Roy Statist Soc B 53:285-340.
Gould SJ. 1977. Ontogeny and phylogeny. Cambridge: Harvard University Press.
Gower JC. 1975. Generalised Procrustes analysis. Psychmetrika 40:33-50. doi:10.1007/BF02291478
Hadziselimovic H, Cus M. 1966. The appearance of internal structures of the brain in relation to configuration of the human skull. Cells Tissues Organs 63:289-299. doi:10.1159/000142794
Hadziselimovic H, Ruzdic N. 1966. Appearance of the base of the brain in relation to the configuration of human skull. Cells Tissues Organs 65:146-156. doi:10.1159/000142869
Hallgrímsson B, Lieberman DE, Young NM, Parsons T, Wat S. 2007a. Evolution of covariance in the mammalian skull. Novartis Found Symp 284:164-190. doi:10.1002/9780470319390.ch12
Hallgrímsson B, Lieberman DE, Liu W, Hutchinson AF, Jirik FR. 2007b. Epigenetic interactions and the structure of phenotypic variation in the cranium. Evol Dev 9:76-91. doi:10.1111/j.1525-142X.2006.00139.x
Herring SW, Teng S. 2000. Strain in the braincase and its sutures during function. Am J Phys Anthropol 112:575-593. doi:10.1002/1096-8644(200008)112:4<575::AIDAJPA10>3.0.CO;2-0
Howells WW. 1973. Cranial variation in man. Papers of the Peabody Museum of Archaeology and Ethnology. Cambridge: Harvard University Press.
Kent JT. 1994. The complex Bingham distribution and shape analysis. J Roy Statist Soc B 56:285-299.
Klingenberg CP. 1998. Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biol Rev 73:79-123. doi:10.1017/S000632319800512X
Klingenberg CP. 2011. MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353-357. doi:10.1111/j.1755-0998.2010.02924.x
Kuykendall KL. 1996. Dental development in chimpanzees (Pan troglodytes): the timing of tooth calcification stages. Am J Phys Anthropol 99:135-157. doi:10.1002/(SICI)1096-8644(199601)99:1<135::AIDAJPA8>3.0.CO;2-#
Leigh SR, Shea BT. 1996. Ontogeny of body size variation in African apes. Am J Phys Anthropol 99:43-65. doi:10.1002/(SICI)1096-8644(199601)99:1<43::AIDAJPA3>3.0.CO;2-0
LeMay M. 1976. Morphological cerebral asymmetries of modern man, fossil man, and nonhuman primate. Ann New York Acad Sc 280:349-366. doi:10.1111/j.1749-6632.1976.tb25499.x
Lestrel PE, Bodt A, Swindler DR. 1993. Longitudinal study of cranial base shape changes in Macaca nemestrina. Am J Phys Anthropol 91:117-129. doi:10.1002/ajpa.1330910108
Lieberman DE, McCarthy RC. 1999. The ontogeny of cranial base angulation in humans and chimpanzees and its implications for reconstructing pharyngeal dimensions. J Hum Evol 36:487-517. doi:10.1006/jhev.1998.0287
Lieberman DE, Carlo J, Ponce de León M, Zollikofer CPE. 2007. A geometric morphometric analysis of heterochrony in the cranium of chimpanzees and bonobos. J Hum Evol 52:647-662. doi:10.1016/j.jhevol.2006.12.005
Lieberman DE, McBratney BM, Krovitz GE. 2002. The evolution and development of craniofacial form in Homo sapiens. Proc Natl Acad Sci USA 99:1134-1139. doi:10.1073/pnas.022440799
Lieberman DE, Krovitz GE, McBratney-Owen B. 2004. Testing hypotheses about tinkering in the fossil record: the case of the human skull. J Exp Zool B Mol Dev Evol 302:284-301. doi:10.1002/jez.b.21004
Lieberman DE, Ross CF, Ravosa MJ. 2000. The primate cranial base: ontogeny, function, and integration. Yrbk Phys Anthropol 43:117-169. doi:10.1002/1096-8644(2000)43:31+<117::AID-AJPA5>3.3.CO;2-9
Martínez-Abadías N, Esparza M, Sjøvold T, González-José R, Santos M, Hernández M, Klingenberg CP. 2012. Pervasive genetic integration directs the evolution of human skull shape. Evolution 66:10-23. doi:10.1111/j.1558-5646.2011.01496.x
McCarthy RC. 2001. Anthropoid cranial base architecture and scaling relationships. J Hum Evol 40:41-66. doi:10.1006/jhev.2000.0446
McHenry HM, Coffing K. 2000. Australopithecus to Homo: transformations in body and mind. Ann Rev Anthropol 29:125-146. doi:10.1146/annurev.anthro.29.1.125
Mitteroecker P, Bookstein F. 2008. The evolutionary role of modularity and integration in the hominoid cranium. Evolution 62:943-958. doi:10.1111/j.1558-5646.2008.00321.x
Mitteroecker P, Gunz P, Bernhard M, Schaefer K, Bookstein FL. 2004. Comparison of cranial ontogenetic trajectories among great apes and humans. J Hum Evol 46:679-698. doi:10.1016/j.jhevol.2004.03.006
Moss ML, Young RW. 1960. A functional approach to craniology. Am J Phys Anthropol 18:281-291. doi:10.1002/ajpa.1330180406
Neubauer S, Gunz P, Hublin JJ. 2010. Endocranial shape changes during growth in chimpanzees and humans: a morphometric analysis of unique and shared aspects. J Hum Evol 59:555-566. doi:10.1016/j.jhevol.2010.06.011
O’Higgins P, Jones N. 1998. Facial growth in Cercocebus torquatus. An application of three-dimensional geometric morphometric techniques to the study of morphological variation. J Anat 193:251-272. doi:10.1046/j.1469-7580.1998.19320251.x
Penin X, Berge C, Baylac M. 2002. Ontogenetic study of the skull in modern humans and the common chimpanzees: neotenic hypothesis reconsidered with a tridimensional Procrustes analysis. Am J Phys Anthropol 118:50-62.
Richtsmeier JT, Aldridge K, DeLeon VB, Panchal J, Kane AA, Marsh JL, Yan P, Cole TM. 2006. Phenotypic integration of neurocranium and brain. J Exp Zool Part B 306:360-378. doi:10.1002/ajpa.10044
Rohlf F J, Corti M. 2000. Use of two-block partial leastsquares to study covariation in shape. Syst Biol 49:740-753. doi:10.1080/106351500750049806
Rohlf F, Slice DE. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst Zool 39:40-59. doi:10.2307/2992207
Schaefer K, Mitteroecker P, Gunz P, Bernhard M, Bookstein FL. 2004. Craniofacial sexual dimorphism patterns and allometry among extant hominids. Ann Anat 186:471-478. doi:10.1016/S0940-9602(04)80086-4
Smith HB. 1989. Dental development as a measure of life history in primates. Evolution 43:683-688. doi:10.2307/2409073
Vrba ES. 1998. Multiphasic growth models and the evolution of prolonged growth exemplified by human brain evolution. J Theor Biol 190:227-239. doi:10.1006/jtbi.1997.0549
Zafar H, Nordh E, Eriksson PO. 2000. Temporal coordination between mandibular and head-neck movements during jaw opening-closing tasks in man. Arch Oral Biol 45:675-682. doi:10.1016/S0003-9969(00)00032-7
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