Modularity and integration in ontogeny of the middle facial skeleton in two West African monkey species: collared mangabey (Cercocebus torquatus) and olive colobus (Procolobus verus)

Evteev A.A., Nanova O.G.

P. 01-18

Could studying of a single bone’s morphological variation and growth provide some additional information? For addressing this question a configuration of 13 landmarks from the middle part of the upper facial skeleton was digitized by Microscribe 3D digitizer on 25 skulls of Cercocebus torquatus and 16 skulls of Procolobus verus of different age and sex. Our results suggest that despite of strong ontogenetic integration in postnatal growth of the primate facial skeleton a study on a single bone’s growth could provide a lot of biologically meaningful information. Elongation of the snout is far more pronounced in C. torquatus and related specifically to growth of the maxilla. This process can be described by a linear growth model and seems to be closely related to the general somatic growth rather than be by itself adaptive since an elongated snout could decrease bite force generation capacity at the incisors. Premaxillary growth is to a substantial degree independent from maxillary growth. The lower part of the bone attains its species-specific shape early in ontogeny what can be considered as a preparation to strong masticatory loadings which begin in this species during the first year of life. Later growth processes of the two bones are closely related and as a result shape of the premaxilla is substantially modified. Proximal and distal parts of the nasal bones seem to show differences: the former could be apparently different among individuals of the same species while shape and size of the later much more reflect elongation of the maxilla during postnatal period.DOI: 10.15298/rusjtheriol.12.1.01

• Abzhanov A., Protas M., Grant B.R., Grant P.R. & Tabin C.J. 2004. Bmp4 and morphological variation of beaks in Darwin's finches // Science. Vol.305. P.1462-1465.
• Ackermann R.R. & Krovitz G.E. 2002. Common patterns of facial ontogeny in the hominid lineage // Anatomical Record. Vol.269. P.142-147.
• Adams D.C., Cardini A., Monteiro L.R., O'Higgins P. & Rohlf F.J. 2011. Morphometrics and phylogenetics: Principal components of shape from cranial modules are neither appropriate nor effective cladistic characters // Journal of Human Evolution. Vol.60. P.240-243.
• Alexeev V.P. 1969. [Origin of the Peoples of the Eastern Europe]. Moskva: Nauka. 328 p. [in Russian].
• Alexeev V.P. 1974. [Origin of the Peoples of the Caucasus]. Moskva: Nauka. 315 p. [in Russian].
• Bastir M., Rosas A. & O'Higgins P. 2006. Craniofacial levels and the morphological maturation of the human skull // Journal of Anatomy. Vol.209. No.5. P.637-654.
• Bjork A. 1968. The use of metallic implants in the study of facial growth in children: method and application // American Journal of Physical Anthropology. Vol.29. P.243-254.
• Bulygina E., Mitteroecker P. & Aiello L. 2006. Ontogeny of facial dimorphism and patterns of individual development within one human population // American Journal of Physical Anthropology. Vol.131. P.432-443.
• Bunak V.V. 1960. [The facial skeleton and the factors determining variation of its morphology] // Proceedings of the Institute of Ethnography, New Series. T.50. P.84-152 [in Russian].
• Cardini A. & Elton S. 2008a. Does the skull carry a phylogenetic signal? Evolution and modularity in the guenons // Biological Journal of the Linnean Society. Vol.93. P.813-834.
• Cardini A. & Elton S. 2008b. Variation in guenon skulls (I): species divergence, ecological and genetic differences // Journal of Human Evolution. Vol.54. P.615-637.
• Carey J.W. & Steegmann A.T. 1981. Human nasal protrusion, latitude, and climate // American Journal of Physical Anthropology. Vol.56. No.3. P.313-319.
• Cheverud J.M. 1982. Phenotypic, genetic, and environmental morphological integration in the cranium // Evolution. Vol.36. No.3. P.499-516.
• Churchill S.E., Shackelford L.L., Georgi J.N. & Black M.T. 2004. Morphological variation and airflow dynamics in the human nose // American Journal of Human Biology. Vol.16. P.625-638.
• Cobb S.N. & O'Higgins P. 2004. Hominins do not share a common postnatal facial ontogenetic shape trajectory // Journal of Experimental Zoology, Part B: Molecular and Developmental Evolution. Vol.302. P.302-321.
• Collard M. & O'Higgins P. 2001. Ontogeny and homoplasy in the papionin monkey face // Evolution & Development. Vol.3. No.5. P.322-331.
• Corner B.D. & Richtsmeier J.T. 1991. Morphometric analysis of craniofacial growth in Cebus apella // American Journal of Physical Anthropology. Vol.84. P.323-342.
• Creuzet S., Couly G. & Le Douarin N.M. 2005. Patterning the neural crest derivatives during development of the vertebrate head: insights from avian studies // Journal of Anatomy. Vol.207. P.447-459.
• Curtis N., Kupczik K., O'Higgins P., Moazen M. & Fagan M. 2008. Predicting skull loading: applying multibody dynamics analysis to a macaque skull // The Anatomical Record. Vol.291. P.491-501.
• Davies G. & Oates J. (eds.). 1995. Colobine Monkeys: Their Ecology, Behaviour and Evolution. Cambridge: Cambridge University Press. 432 p.
• Depew M.J., Compagnucci C. & Griffin J. 2008. Suture neontology and paleontology: the bases for where, when and how boundaries between bones have been established and have evolved // Rice D.P. (ed.). Craniofacial Sutures: Development, Disease, and Treatment. Frontiers of Oral Biology, Basel. Vol.12. P.57-78.
• Depew M.J., Simpson C.A., Morasso M. & Rubenstein J.L.R. 2005. Reassessing the Dlx code: the genetic regulation of branchial arch skeletal pattern and development // Journal of Anatomy. Vol.207. P.501-561.
• Enlow D.H. 1966. A comparative study of facial growth in Homo and Macaca // American Journal of Physical Anthropology. Vol.24. P.293-308.
• Enlow D.H. 1975. Handbook of Facial Growth. Philadelphia: W.B. Saunders Company. 423 p.
• Franciscus R.G. 1995. Later Pleistocene Nasofacial Variation in Western Eurasia and Africa and Modern Human Origins. PhD Thesis, University of New Mexico. 377 p.
• Funatsu M., Sato K. & Mitani H. 2006. Effects of growth hormone on craniofacial growth // Angle Orthodontist. Vol.76. No.6. P.970-977.
• Glanville E.V. 1969. Nasal shape, prognathism and adaptation in man // American Journal of Physical Anthropology. Vol.30. P.29-38.
• Hallgrimsson B., Willmore K., Dorval C. & Cooper D.M.L. 2004. Craniofacial variability and modularity in macaques and mice // Journal of Experimental Zoology. Part B: Molecular and Developmental Evolution. Vol.302. P.207-225.
• Hammer Ш., Harper D.A.T. & Ryan P.D. 2001. PAST - Paleontological Statistics Software Package for Education and Data Analysis.
• Herring S.W. 2008. Mechanical influences on suture development and patency // Rice D.P. (ed.). Craniofacial Sutures: Development, Disease, and Treatment. Frontiers of Oral Biology, Basel. Vol.12. P.41-56.
• Holton N.E., Franciscus R.G., Marshall S.D., Southard T.E. & Nieves M.A. 2011. Nasal septal and premaxillary developmental integration: implications for facial reduction in Homo // Anatomical Record. Vol.294. P.68-78.
• Holton N.E., Franciscus R.G., Nieves M.A., Marshall S.D., Reimer S.B., Southard T.E., Keller J.C. & Maddux S.D. 2010. Sutural growth restriction and modern human facial evolution: an experimental study in a pig model // Journal of Anatomy. Vol.216. P.48-61.
• Howells W.W. 1989. Skull shapes and the map // Peabody Museum Paper. Vol.79. P.1-189.
• Hwang T.-S., Song J., Yoon H., Cho B.-P. & Kang H.-S. 2005. Morphometry of the nasal bones and piriform apertures in Koreans // Annals of Anatomy. Vol.187. P.411-414.
• Klingenberg C.P., Leamy L.J. & Cheverud J.M. 2004. Integration and modularity of quantitative trait locus effects on geometric shape in the mouse mandible // Genetics. Vol.166. P.1909-1921.
• Klingenberg C. P. 2009. Morphometric integration and modularity in configurations of landmarks: tools for evaluating a priori hypotheses // Evolution & Development. Vol.11. P.405-421.
• Klingenberg C.P. 2011. MorphoJ: an integrated software package for geometric morphometrics // Molecular Ecology Resources. Vol.11. P.353-357.
• Kopher R.A. & Mao J.J. 2003. Sutural growth modulated by the oscillatory component of micromechanical strain // Journal of Bone and Mineral Research. Vol.18. P.521-528.
• Koyabu D.B. & Endo H. 2009. Craniofacial variation and dietary adaptations of African colobines // Journal of Human Evolution. Vol.56. P.525-536.
• Lang J. & Baumeister R. 1982. On postnatal growth of the nasal cavity // Gegenbaurs Morphologisches Jahrbuch. Vol.128. P.354-393.
• Latham R.A. 1970. Maxillary development and growth: the septo-premaxillary ligament // Journal of Anatomy. Vol.107. No.3. P.471-478.
• Lieberman D.E., Ross C. & Ravosa M.J. 2000. The primate cranial base: ontogeny, function, and integration // Yearbook of Physical Anthropology. Vol.43. P.117-169.
• Martin R. 1928. Lehrbuch der Anthropologie in Systematischer Darstellung. Vol.2. Kraniologie, Osteologie. Jena: Gustav Fischer. 604 p.
• Martinez Abadias N. 2007. Evolutionary patterns of the human skull. A quantitative genetic analysis of craniofacial phenotypic variation. PhD thesis. Universitat de Barcelona. 256 p.
• McGraw W.S., Vick A.E. & Daegling D.J. 2011. Sex and age differences in the diet and ingestive behaviors of sooty mangabeys (Cercocebus atys) in the Tai Forest, Ivory Coast // American Journal of Physical Anthropology. Vol.144. P.140-153.
• Mogra R., Schluter P.J., Ogle R.F., O'Connel J., Fortus L. & Hyett J.A. 2010. A prospective cross-sectional study to define racial variation in fetal nasal bone length through ultrasound assessment at 18-20 weeks' gestation // Australian and New Zealand Journal of Obstetrics and Gynaecology. Vol.50. P.528-533.
• Mooney M.P. & Siegel M.I. 1986. Developmental relationship between premaxillary-maxillary suture patency and anterior nasal spine morphology // Cleft Palate Journal. Vol.23. P.101-107.
• Morimoto N., Ogihara N., Katayama K. & Shiota K. 2008. Three-dimensional ontogenetic shape changes in the human cranium during the fetal period // Journal of Anatomy. Vol.212. P.627-635.
• Moss M.L. & Young R.W. 1960. A functional approach to craniology // American Journal of Physical Anthropology. Vol.18. P.281-292.
• O'Higgins P., Chadfield P. & Jones N. 2001. Facial growth and the ontogeny of morphological variation within and between the primates Cebus apella and Cercocebus torquatus // Journal of Zoology, London. Vol.254. P.337-357.
• O'Higgins P. & Collard M. 2002. Sexual dimorphism and facial growth in papionin monkeys // Journal of Zoology, London. Vol.257. P.255-272.
• 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 // Journal of Anatomy. Vol.193. P.251-272.
• Oxnard C. & O'Higgins P. 2009. Biology clearly needs morphometrics. Does morphometrics need biology? // Biological Theory: Integrating Development, Evolution and Cognition. Vol.4. No.1. P.84-97.
• Ponce de Leon M. & Zollikofer C. 2001. Neanderthal cranial ontogeny and its implications for late hominid diversity // Nature. Vol.412. P.534-538.
• Rice D.P. 2008. Developmental anatomy of craniofacial sutures // Rice D.P. (ed.). Craniofacial Sutures: Development, Disease, and Treatment. Frontiers of Oral Biology, Basel. Vol.12. P.1-21.
• Richmond B.G., Wright B.W., Grosse I., Dechow P.C., Ross C.F., Spencer M.A. & Strait D.S. 2005. Finite element analysis in functional morphology // Anatomical Record. Vol.283A. P.259-274.
• Richtsmeier J.T., Corner B.D., Grausz H.M., Cheverud J.M. & Dahaney S.E. 1993. The role of post natal growth in the production of facial morphology // Systematic Biology. Vol.42. P.307-330.
• Roseman C.C. & Weaver T.D. 2004. Multivariate apportionment of global human craniometric diversity // American Journal of Physical Anthropology. Vol.125. P.257-263.
• Schultz A.H. 1963. Age changes, sex differences and variability as factor in the classification of primates // Washburn S.L. (ed.). Classification and Human Evolution. Chicago. P.85-115.
• Smith H.F., Terhune C.E. & Lockwood C.A. 2007. Genetic, geographic and environmental correlates of human temporal bone variation // American Journal of Physical Anthropology. Vol.134. P.312-322.
• Sonek J.D., Mckenna D., Webb D., Croom C. & Nicolaides K. 2003. Nasal bone length throughout gestation: normal ranges based on 3537 fetal ultrasound measurements // Ultrasound in Obstetrics & Gynecology. Vol.21. No.2. P.152-155.
• Sperber G.H. 2001. Craniofacial Development. Hamilton, BC: Decker Inc. 220 p.
• Sysak N.S. 1960. [Data on the age morphology of the human skull] // Proceedings of the Institute of Ethnography, New Series. T.50. P.29-41 [in Russian].
• Thomson A. & Buxton L.H.D. 1923. Man's nasal index in relation to certain climatic conditions // Journal of the Royal Anthropological Institute. Vol.53. P.92-122.
• Vidarsdуttir U.S., O'Higgins P. & Stringer C. 2002. A geometric morphometric study of regional differences in the ontogeny of the modern human facial skeleton // Journal of Anatomy.Vol.201. No.1. P.211-229.
• Wagner G.P. & Altenberg L. 1996. Complex adaptations and the evolution of evolvability // Evolution. Vol.50. P.967-976.
• Woo T.L. & Morant G.M. A biomechanical study of the flatness of the facial skeleton in man // Biometrika. Vol.26. P.196-250.
• Wu P., Jiang T.-X., Suksaweang S., Widelitz R.B. & Chuong C.-M. 2004. Molecular shaping of the beak // Science. Vol.305. P.1465-1466.
• Yokley T.R. 2009. Ecogeographic variation in human nasal passages // American Journal of Physical Anthropology. Vol.138. No.1. P.11-22.