Ontogenetic changes in magnitudes of integration in the macaque skull.
Macaca fascicularis
integration coefficient of variation
morphological integration
ontogeny
skull modules
Journal
American journal of physical anthropology
ISSN: 1096-8644
Titre abrégé: Am J Phys Anthropol
Pays: United States
ID NLM: 0400654
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
06
03
2020
revised:
15
06
2020
accepted:
08
07
2020
pubmed:
18
8
2020
medline:
20
3
2021
entrez:
18
8
2020
Statut:
ppublish
Résumé
Magnitudes of morphological integration may constrain or facilitate craniofacial shape variation. The aim of this study was to analyze how the magnitude of integration in the skull of Macaca fascicularis changes throughout ontogeny in relation to developmental and/or functional modules. Geometric morphometric methods were used to analyze the magnitude of integration in the macaque cranium and mandible in 80 juvenile and 40 adult M. fascicularis specimens. Integration scores in skull modules were calculated using integration coefficient of variation (ICV) of eigenvalues based on a resampling procedure. Resultant ICV scores between the skull as a whole, and developmental and/or functional modules were compared using Mann-Whitney U tests. Results showed that most skull modules were more tightly integrated than the skull as a whole, with the exception of the chondrocranium in juveniles without canines, the chondrocranium/face complex and the mandibular corpus in adults, and the mandibular ramus in all juveniles. The chondrocranium/face and face/mandibular corpus complexes were more tightly integrated in juveniles than adults, possibly reflecting the influences of early brain growth/development, and the changing functional demands of infant suckling and later masticatory loading. This is also supported by the much higher integration of the mandibular ramus in adults compared with juveniles. Magnitudes of integration in skull modules reflect developmental/functional mechanisms in M. fascicularis. However, the relationship between "evolutionary flexibility" and developmental/functional mechanisms was not direct or simple, likely because of the complex morphology, multifunctionality, and various ossification origins of the skull.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
76-88Informations de copyright
© 2020 Wiley Periodicals LLC.
Références
Ackermann, R. R. (2005). Ontogenetic integration of the hominoid face. Journal of Human Evolution, 48(2), 175-197.
Antón, S. C. (1996). Cranial adaptation to a high attrition diet in Japanese macaques. International Journal of Primatology, 17(3), 401-427.
Armbruster, W. S., Pélabon, C., Bolstad, G. H., & Hansen, T. F. (2014). Integrated phenotypes: Understanding trait covariation in plants and animals. Philosophical Transactions of the Royal Society B, 369(1649), 20130245.
Buck, L. T., De Groote, I., Hamada, Y., Hassett, B. R., Ito, T., & Stock, J. T. (2019). Evidence of different climatic adaptation strategies in humans and non-human primates. Scientific Reports, 9(1), 11025.
Buck, L. T., De Groote, I., Hamada, Y., & Stock, J. T. (2018). Humans preserve non-human primate pattern of climatic adaptation. Quaternary Science Reviews, 192, 149-166.
Cheverud, J. M. (1996). Developmental integration and the evolution of pleiotropy. American Zoologist, 36(1), 44-50.
Ciochon, R. L., Nisbett, R. A., & Corruccini, R. S. (1997). Dietary consistency and craniofacial development related to masticatory function in minipigs. Journal of Craniofacial Genetics and Developmental Biology, 17(2), 96-102.
Conaway, M. A., Schroeder, L., & von Cramon-Taubadel, N. (2018). Morphological integration of anatomical, developmental, and functional postcranial modules in the crab-eating macaque (Macaca fascicularis). American Journal of Physical Anthropology, 166(3), 661-670.
de Oliveira, F. B., Porto, A., & Marroig, G. (2009). Covariance structure in the skull of Catarrhini: A case of pattern stasis and magnitude evolution. Journal of Human Evolution, 56(4), 417-430.
Dickinson, E., Fitton, L. C., & Kupczik, K. (2018). Ontogenetic changes to muscle architectural properties within the jaw-adductor musculature of Macaca fascicularis. American Journal of Physical Anthropology, 167(2), 291-310.
Enlow, D. H., & Hans, M. G. (1996). Essentials of facial growth. Philadelphia, PA: WB Saunders.
Evteev, A., Cardini, A. L., Morozova, I., & O'Higgins, P. (2014). Extreme climate, rather than population history, explains mid-facial morphology of northern Asians. American Journal of Physical Anthropology, 153(3), 449-462.
Fleagle, J. G. (2013). Primate adaptation and evolution, San Diego, CA: Academic Press.
Freidline, S. E., Gunz, P., & Hublin, J. J. (2015). Ontogenetic and static allometry in the human face: Contrasting Khoisan and Inuit. American Journal of Physical Anthropology, 158(1), 116-131.
German, R. Z., Hertweck, D. W., Sirianni, J. E., & Swindler, D. R. (1994). Heterochrony and sexual dimorphism in the pigtailed macaque (Macaca nemestrina). American Journal of Physical Anthropology, 93(3), 373-380.
Gkantidis, N., & Halazonetis, D. J. (2011). Morphological integration between the cranial base and the face in children and adults. Journal of Anatomy, 218(4), 426-438.
Gonzalez, P. N., Oyhenart, E. E., & Hallgrímsson, B. (2011). Effects of environmental perturbations during postnatal development on the phenotypic integration of the skull. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 316(8), 547-561.
Goswami, A., & Polly, P. D. (2010). The influence of modularity on cranial morphological disparity in Carnivora and primates (mammalia). PLoS One, 5(3), e9517.
Goswami, A., Polly, P. D., Mock, O. B., & Sánchez-Villagra, M. R. (2012). Shape, variance and integration during craniogenesis: Contrasting marsupial and placental mammals. Journal of Evolutionary Biology, 25(5), 862-872.
Goswami, A., Smaers, J. B., Soligo, C., & Polly, P. D. (2014). The macroevolutionary consequences of phenotypic integration: From development to deep time. Philosophical Transactions of the Royal Society B, 369(1649), 20130254.
Hallgrímsson, B., Jamniczky, H., Young, N. M., Rolian, C., Parsons, T. E., Boughner, J. C., & Marcucio, R. S. (2009). Deciphering the palimpsest: Studying the relationship between morphological integration and phenotypic covariation. Evolutionary Biology, 36(4), 355-376.
Hallgrímsson, B., & Lieberman, D. E. (2008). Mouse models and the evolutionary developmental biology of the skull. Integrative and Comparative Biology, 48(3), 373-384.
Hallgrímsson, B., Willmore, K., Dorval, C., & Cooper, D. M. (2004). Craniofacial variability and modularity in macaques and mice. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 302(3), 207-225.
Hallgrímsson, B., Willmore, K., & Hall, B. K. (2002). Canalization, developmental stability, and morphological integration in primate limbs. American Journal of Physical Anthropology, 119(S35), 131-158.
Hansen, T. F., & Houle, D. (2008). Measuring and comparing evolvability and constraint in multivariate characters. Journal of Evolutionary Biology, 21(5), 1201-1219.
Kazi-Aoual, F., Hitier, S., Sabatier, R., & Lebreton, J. D. (1995). Refined approximations to permutation tests for multivariate inference. Computational Statistics & Data Analysis, 20(6), 643-656.
Klingenberg, C. P. (2008). Morphological integration and developmental modularity. Annual Review of Ecology, Evolution, and Systematics, 39, 115-132.
Klingenberg, C. P. (2014). Studying morphological integration and modularity at multiple levels: Concepts and analysis. Philosophical Transactions of the Royal Society B, 369(1649), 20130249.
Klingenberg, C. P., & Marugán-Lobón, J. (2013). Evolutionary covariation in geometric morphometric data: Analyzing integration, modularity, and allometry in a phylogenetic context. Systematic Biology, 62(4), 591-610.
Leigh, S. R. (2004). Brain growth, life history, and cognition in primate and human evolution. American Journal of Primatology, 62(3), 139-164.
Lieberman, D. (2011). The evolution of the human head, Cambridge, MA: Harvard University Press.
Lieberman, D. E., Pearson, O. M., & Mowbray, K. M. (2000). Basicranial influence on overall cranial shape. Journal of Human Evolution, 38(2), 291-315.
Lieberman, D. E., Ross, C. F., & Ravosa, M. J. (2000). The primate cranial base: Ontogeny, function, and integration. American Journal of Physical Anthropology, 113(S31), 117-169.
Maddux, S. D., Butaric, L. N., Yokley, T. R., & Franciscus, R. G. (2017). Ecogeographic variation across morphofunctional units of the human nose. American Journal of Physical Anthropology, 162(1), 103-119.
Maddux, S. D., Yokley, T. R., Svoma, B. M., & Franciscus, R. G. (2016). Absolute humidity and the human nose: A reanalysis of climate zones and their influence on nasal form and function. American Journal of Physical Anthropology, 161(2), 309-320.
Marroig, G., Shirai, L. T., Porto, A., de Oliveira, F. B., & De Conto, V. (2009). The evolution of modularity in the mammalian skull II: Evolutionary consequences. Evolutionary Biology, 36(1), 136-148.
Melo, D., Garcia, G., Hubbe, A., Assis, A. P., & Marroig, G. (2015). EvolQG-An R package for evolutionary quantitative genetics. F1000Research, 4(925),
Mitteroecker, P., & Bookstein, F. (2009). The ontogenetic trajectory of the phenotypic covariance matrix, with examples from craniofacial shape in rats and humans. Evolution, 63(3), 727-737.
Moss, M. L., & Rankow, R. M. (1968). The role of the functional matrix in mandibular growth. Angle Orthodontist, 38(2), 95-103.
Mouri, T. (1994). Postnatal growth and sexual dimorphism in the skull of the Japanese macaque (Macaca fuscata). Anthropological Science, 102(Supplement), 43-56.
Mouri, T. (1996). Multivariate cranial ontogenetic allometries in crab-eating, rhesus and Japanese macaques. Anthropological Science, 104(4), 281-303.
Neaux, D. (2017). Morphological integration of the cranium in Homo, Pan, and Hylobates and the evolution of hominoid facial structures. American Journal of Physical Anthropology, 162(4), 732-746.
Neaux, D., Guy, F., Gilissen, E., Coudyzer, W., & Ducrocq, S. (2013). Covariation between midline cranial base, lateral basicranium, and face in modern humans and chimpanzees: A 3D geometric morphometric analysis. Anatomical Record, 296(4), 568-579.
Neaux, D., Sansalone, G., Ledogar, J. A., Ledogar, S. H., Luk, T. H., & Wroe, S. (2018). Basicranium and face: Assessing the impact of morphological integration on primate evolution. Journal of Human Evolution, 118, 43-55.
Neaux, D., Wroe, S., Ledogar, J. A., Heins Ledogar, S., & Sansalone, G. (2019). Morphological integration affects the evolution of midline cranial base, lateral basicranium, and face across primates. American Journal of Physical Anthropology, 170(1), 37-47.
Neubauer, S., Gunz, P., & Hublin, J. J. (2009). The pattern of endocranial ontogenetic shape changes in humans. Journal of Anatomy, 215(3), 240-255.
Nicholson, E., & Harvati, K. (2006). Quantitative analysis of human mandibular shape using three-dimensional geometric morphometrics. American Journal of Physical Anthropology, 131(3), 368-383.
Noback, M. L., Harvati, K., & Spoor, F. (2011). Climate-related variation of the human nasal cavity. American Journal of Physical Anthropology, 145(4), 599-614.
Olson, E. C., & Miller, R. L. (1958). Morphological integration, Chicago, IL: University of Chicago Press.
Pavlicev, M., Cheverud, J. M., & Wagner, G. P. (2009). Measuring morphological integration using eigenvalue variance. Evolutionary Biology, 36(1), 157-170.
Polanski, J. M. (2011). Morphological integration of the modern human mandible during ontogeny. International Journal of Evolutionary Biology, 2011, 1-11.
Porto, A., de Oliveira, F. B., Shirai, L. T., De Conto, V., & Marroig, G. (2009). The evolution of modularity in the mammalian skull I: Morphological integration patterns and magnitudes. Evolutionary Biology, 36(1), 118-135.
Profico, A., Piras, P., Buzi, C., Di Vincenzo, F., Lattarini, F., Melchionna, M., … Manzi, G. (2017). The evolution of cranial base and face in Cercopithecoidea and Hominoidea: Modularity and morphological integration. American Journal of Primatology, 79(12), e22721.
R Core Team. (2013). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from http://www.R-project.org/
Ravosa, M. J. (1991). The ontogeny of cranial sexual dimorphism in two Old World monkeys: Macaca fascicularis (Cercopithecinae) and Nasalis larvatus (Colobinae). International Journal of Primatology, 12(4), 403-426.
Rolian, C. (2014). Genes, development, and evolvability in primate evolution. Evolutionary Anthropology, 23(3), 93-104.
Scheuer, L., & Black, S. (2000). Developmental juvenile osteology, Oxford, UK: Elsevier.
Scott, N. A., Strauss, A., Hublin, J. J., Gunz, P., & Neubauer, S. (2018). Covariation of the endocranium and splanchnocranium during great ape ontogeny. PLoS One, 13(12), e0208999.
Shirai, L. T., & Marroig, G. (2010). Skull modularity in neotropical marsupials and monkeys: Size variation and evolutionary constraint and flexibility. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 314(8), 663-683.
Singh, N. (2014). Ontogenetic study of allometric variation in Homo and Pan mandibles. Anatomical Record, 297(2), 261-272.
Singh, N., Harvati, K., Hublin, J. J., & Klingenberg, C. P. (2012). Morphological evolution through integration: A quantitative study of cranial integration in Homo, Pan, Gorilla and Pongo. Journal of Human Evolution, 62(1), 155-164.
Smith, H. F., & von Cramon-Taubadel, N. (2015). The relative correspondence of cranial and genetic distances in papionin taxa and the impact of allometric adjustments. Journal of Human Evolution, 85, 46-64.
von Cramon-Taubadel, N. (2011). Global human mandibular variation reflects differences in agricultural and hunter-gatherer subsistence strategies. Proceedings of the National Academy of Sciences of the United States of America, 108(49), 19546-19551.
von Cramon-Taubadel, N., Frazier, B. C., & Lahr, M. M. (2007). The problem of assessing landmark error in geometric morphometrics: Theory, methods, and modifications. American Journal of Physical Anthropology, 134(1), 24-35.
Wang, Q., Dechow, P. C., & Hens, S. M. (2007). Ontogeny and diachronic changes in sexual dimorphism in the craniofacial skeleton of rhesus macaques from Cayo Santiago, Puerto Rico. Journal of Human Evolution, 53(4), 350-361.
Wiley, D. F., Amenta, N., Alcantara, D. A., Ghosh, D., Kil, Y. J., Delson, E., … Hamann, B. (2005). Evolutionary morphing. American Journal of Physical Anthropology, 55, 431-438.
Willmore, K. E., Leamy, L., & Hallgrímsson, B. (2006). Effects of developmental and functional interactions on mouse cranial variability through late ontogeny. Evolution & Development, 8(6), 550-567.
Young, N. M., Wagner, G. P., & Hallgrímsson, B. (2010). Development and the evolvability of human limbs. Proceedings of the National Academy of Sciences of the United States of America, 107(8), 3400-3405.
Zelditch, M. L. (1988). Ontogenetic variation in patterns of phenotypic integration in the laboratory rat. Evolution, 42(1), 28-41.
Zelditch, M. L., Bookstein, F. L., & Lundrigan, B. L. (1992). Ontogeny of integrated skull growth in the cotton rat Sigmodon fulviventer. Evolution, 46(4), 1164-1180.
Zelditch, M. L., & Carmichael, A. C. (1989). Growth and intensity of integration through postnatal growth in the skull of Sigmodon fulviventer. Journal of Mammalogy, 70(3), 477-484.