Prenatal development of skull and brain in a mouse model of growth restriction
Abstract
Patterns of covariation result from the overlapping effect of several developmental processes. By perturbing certain specific developmental processes, experimental studies contribute to a better understanding of their particular effects on the generation of phenotype. The aim of this work was to analyze the interactions among morphological traits of the skull and the brain during late prenatal life (18.5 days postconception) in mice exposed to maternal protein undernutrition. Images from the skull and brain were obtained through micro-computed tomography and 3D landmark coordinates were digitized in order to quantify shape and size of both structures with geometric morphometric techniques. The results highlight a systemic effect of protein restriction on the size of the skull and the brain, which were both significantly reduced in the undernourished group compared to control group. Skull shape is partially explained by brain size, and patterns of shape variation were only partially coincident with previous reports for other ontogenetic stages, suggesting that allometric trajectories across pre- and postnatal ages change their directions. Within the skull, neurocranial and facial shape traits covaried strongly, while subtle covariation was found between the shape of the skull and the brain. These findings are in line with former studies in mutant mice and reveal the importance of carrying out analyses of phenotypic variation in a broad range of developmental stages. The present study contributes to the basic understanding of epigenetic relations among growing tissues and has direct implications for the field of paleoanthropology, where inferences about brain morphology are usually derived from skull remains.
Keywords: maternal protein restriction; phenotypic integration; cranial modules; micro-CT
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References
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Ackermann RR, Cheverud JM. 2000. Phenotypic covariance structure in tamarins (genus Saguinus): A comparison of variation patterns using matrix correlation and common principal component analysis. Am J Phys Anthopol 111:489-501. doi:10.1002/(SICI)1096-8644(200004)111:4<489::AID-AJPA5>3.0.CO;2-U
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Aldridge K, Kane AA, Marsh JL, Panchal J, Boyadjiev SA, Yan P, Govier D, Ahmad W, Richtsmeier JT. 2005a. Brain morphology in nonsyndromic unicoronal craniosynostosis. Anat Rec A Discov Mol Cell Evol Biol 285:690-698. doi:10.1002/ar.a.20201
Aldridge K, Kane AA, Marsh JL, Yan P, Govier D, Richtsmeier JT. 2005b. Relationship of brain and skull in pre- and postoperative sagittal synostosis. J Anat 206:373-385. doi:10.1111/j.1469-7580.2005.00397.x
Aldridge K, Marsh JL, Govier D, Richtsmeier JT. 2002. Central nervous system phenotypes in craniosynostosis. J Anat 201:31-39. doi:10.1046/j.1469-7580.2002.00074.x
Aldridge K, Reeves RH, Olson LE, Richtsmeier JT. 2007. Differential effects of trisomy on brain shape and volume in related aneuploid mouse models. Am J Med Genet A 143:1060-1070. doi:10.1002/ajmg.a.31721
Bookstein FL. 1997. Morphometric tools for landmark data: geometry and biology. Cambridge: Cambridge University Press.
Bookstein FL, Gunz P, Mitteroecker P, Pross
singer 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
Boughner JC, Wat S, Diewert VM, Young NM, Browder LW, Hallgrímsson B. 2008. Short-faced mice and developmental interactions between the brain and the face. J Anat 213:646-662. doi:10.1111/j.1469-7580.2008.00999.x
Bruner E. 2004. Geometric morphometrics and paleoneurology: brain shape evolution in the genus Homo. J Hum Evol 47:279-303. doi:10.1016/j.jhevol.2004.03.009
Cesani MF, Orben AB, Oyhenart EE, Zucchi M, Muñe MC, Pucciarelli HM. 2006. Effect of undernutrition on the cranial growth of the rat. An intergenerational study. J Anat 209:137-147. doi:10.1111/j.1469-7580.2006.00603.x
Cheverud JM. 1982. Phenotypic, genetic and environmental morphological integration in the cranium. Evolution 36:499-516.doi:10.2307/2408096
Cheverud JM. 2007. The relationship between development and evolution through heritable variation. Novartis Found Symp 284:55-65. doi:10.1002/9780470319390.ch4
Chernoff B, Magwene PM. 1999. Morphological integration: forty years later. In: Olson EC, Miller RL, editors. Morphological integration. Chicago: University of Chicago Press. p 319-353.
Cohen MM, Kreiborg S, Lammer EJ, Cordero JF, Mastroiacovo P, Erickson JD, Roeper P, MartinezFrias ML. 1992. Birth prevalence study of the Apert syndrome. Am J Med Genet 42:655-659. doi:10.1002/ajmg.1320420505
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Frey L, Hauser WA. 2003. Epidemiology of neural tube defects. Epilepsia 44(Suppl 3):4-13. doi:10.1046/j.1528-1157.44.s3.2.x
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Gonzalez PN, Perez I, Bernal V. 2011b. Ontogenetic allometry and cranial shape diversification among human populations from South America. Anat Rec 294:1864-1874. doi:10.1002/ar.21454
Gonzalez PN, Oyhenart EE, Hallgrímsson B. 2011a. Effects of environmental perturbations during postnatal development on the phenotypic integration of the skull. J Exp Zool 314B:547-561.doi:10.1002/jez.b.21430
Gonzalez PN, Hallgrímsson B, Oyhenart EE. 2011c. Developmental plasticity in covariance structure of the skull: effects of prenatal stress. J Anat 218:43-257. doi:10.1111/j.1469-7580.2010.01326.x
Gunz P, Neubauer S, Golovanova L, Doronichev V, Maureille B, Hublin JJ. 2012. A uniquely modern human pattern of endocranial development. Insights from a new cranial reconstruction of the Neandertal newborn from Mezmaiskaya. J Hum Evol 62:300-313. doi:10.1016/j.jhevol.2011.11.013
Hallgrímsson B, Hall BK. 2011. Epigenetics: the context of development. In: Hallgrímsson B, Hall BK, editors. Epigenetics: linking the genotype and phenotype in development and evolution. California: University of California Press. p 424-438.
Hallgrímsson B, Jamniczky H, Young NM, Rolian C, Parsons TE, Boughner JC, Marcucio RS. 2009. Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic covariation. Evol Biol 36:355-376. doi:10.1007/s11692-009-9076-5
Hallgrímsson B, Lieberman DE. 2008. Mouse models and the evolutionary developmental biology of the skull. Int Comp Biol 43:373-384. doi:10.1093/icb/icn076
Hallgrímsson B, Lieberman DE, Liu W, Ford-Hutchinson AF, Jirik FR. 2007. 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
Helms JA, Cordero D, Tapadia MD. 2005. New insights into craniofacial morphogenesis. Development 132:851-861. doi:10.1242/dev.01705
Hill CA, Martínez-Abadías N, Motch SM, Austin JR, Wang Y, Jabs EW, Richtsmeier JT, Aldridge K. 2013. Postnatal brain and skull growth in an Apert syndrome mouse model. Am J Med Genet A 161A:745-757. doi:10.1002/ajmg.a.35805
Klingenberg CP. 2009. Morphometric integration and modularity in configurations of landmarks: tools for evaluating a priori hypotheses. Evol Dev 11:405-421. doi:10.1111/j.1525-142X.2009.00347.x
Klingenberg CP. 2013. Visualizations in geometric morphometrics: how to read and how to make graphs showing shape changes. Hystrix 24:15-24. doi:10.4404/hystrix-24.1-7691
Klingenberg CP, McIntyre GS. 1998. Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with procrustes methods. Evolution 52:1363-1375.
Marcucio RS, Young NM, Hu D, Hallgrimsson B. 2011. Mechanisms that underlie co-variation of the brain and face. Genesis 49:177-189. doi:10.1002/dvg.20710
Marroig G, Shirai LT, Porto A, de Oliveira FB, De Conto V. 2009.The evolution of modularity in the mammalian skull II: evolutionary consequences. Evol Biol 36:136-148. doi:10.1007/s11692-009-9051-1
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:10.5061/dryad.12g3c7ht
Martínez-Abadías N, Heuzé Y, Wang Y, Jabs EW, Aldridge K, Richtsmeier JT. 2011. FGF/FGFR signaling coordinates skull development by modulating magnitude of morphological integration: evidence from Apert syndrome mouse models. PLoS One 6:e26425. doi:10.1371/journal.pone.0026425
Metscher BD. 2009. MicroCT for developmental biology: a versatile tool for high-contrast 3D imaging at histological resolutions. Dev Dyn 238:632-640. doi:10.1002/dvdy.21857
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, Bookstein FL. 2009. The ontogenetic trajectory of the phenotypic covariance matrix, with examples from craniofacial shape in rats and humans. Evolution 63:727-737. doi:10.1111/j.1558-5646.2008.00587.x
Monteiro LR. 1999. Multivariate regression models and geometric morphometrics: the search for causal factors in the analysis of shape. Syst Biol 48:192-199.
Morimoto K, Nishikuni K, Hirano S, Takemoto O, Futagi Y. 2003. Quantitative follow-up analysis by computed tomographic imaging in neonatal hydrocephalus. Pediatr Neurol 29:435-439. doi:10.1016/S0887-8994(03)00401-6
Moss ML, Young RW. 1960. A functional approach to craniology. Am J Phys Anthropol 18:281-291.
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
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Lieberman DE, Hallgrímsson B, Liu W, Parsons TE, Jamniczky H. 2008. Spatial packing, cranial base angulation, and craniofacial shape variation in the mammalian skull: testing a new model using mice. J Anat 212:720-735. doi:10.1111/j.1469-7580.2008.00900.x
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Aldridge K, Hill CA, Austin JR, Percival C, MartinezAbadias N, Neuberger T, Wang Y, Jabs EW, Richtsmeier JT. 2010. Brain phenotypes in two FGFR2 mouse models for Apert syndrome. Dev Dyn 239:987-997. doi:10.1002/dvdy.22218
Aldridge K, Kane AA, Marsh JL, Panchal J, Boyadjiev SA, Yan P, Govier D, Ahmad W, Richtsmeier JT. 2005a. Brain morphology in nonsyndromic unicoronal craniosynostosis. Anat Rec A Discov Mol Cell Evol Biol 285:690-698. doi:10.1002/ar.a.20201
Aldridge K, Kane AA, Marsh JL, Yan P, Govier D, Richtsmeier JT. 2005b. Relationship of brain and skull in pre- and postoperative sagittal synostosis. J Anat 206:373-385. doi:10.1111/j.1469-7580.2005.00397.x
Aldridge K, Marsh JL, Govier D, Richtsmeier JT. 2002. Central nervous system phenotypes in craniosynostosis. J Anat 201:31-39. doi:10.1046/j.1469-7580.2002.00074.x
Aldridge K, Reeves RH, Olson LE, Richtsmeier JT. 2007. Differential effects of trisomy on brain shape and volume in related aneuploid mouse models. Am J Med Genet A 143:1060-1070. doi:10.1002/ajmg.a.31721
Bookstein FL. 1997. Morphometric tools for landmark data: geometry and biology. Cambridge: Cambridge University Press.
Bookstein FL, Gunz P, Mitteroecker P, Pross
singer 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
Boughner JC, Wat S, Diewert VM, Young NM, Browder LW, Hallgrímsson B. 2008. Short-faced mice and developmental interactions between the brain and the face. J Anat 213:646-662. doi:10.1111/j.1469-7580.2008.00999.x
Bruner E. 2004. Geometric morphometrics and paleoneurology: brain shape evolution in the genus Homo. J Hum Evol 47:279-303. doi:10.1016/j.jhevol.2004.03.009
Cesani MF, Orben AB, Oyhenart EE, Zucchi M, Muñe MC, Pucciarelli HM. 2006. Effect of undernutrition on the cranial growth of the rat. An intergenerational study. J Anat 209:137-147. doi:10.1111/j.1469-7580.2006.00603.x
Cheverud JM. 1982. Phenotypic, genetic and environmental morphological integration in the cranium. Evolution 36:499-516.doi:10.2307/2408096
Cheverud JM. 2007. The relationship between development and evolution through heritable variation. Novartis Found Symp 284:55-65. doi:10.1002/9780470319390.ch4
Chernoff B, Magwene PM. 1999. Morphological integration: forty years later. In: Olson EC, Miller RL, editors. Morphological integration. Chicago: University of Chicago Press. p 319-353.
Cohen MM, Kreiborg S, Lammer EJ, Cordero JF, Mastroiacovo P, Erickson JD, Roeper P, MartinezFrias ML. 1992. Birth prevalence study of the Apert syndrome. Am J Med Genet 42:655-659. doi:10.1002/ajmg.1320420505
Dambska M, Schmidt-Sidor B, Maslinska D, Laure-Kamionowska M, Kosno-Kruszewska E, Deregowski K. 2003. Anomalies of cerebral structures in acranial neonates. Clin Neuropathol 22:291-295.
Davies BR, Duran M. 2003. Malformations of the cranium, vertebral column, and related central nervous system: morphologic heterogeneity may indicate biological diversity. Birth Defects Res A Clin Mol Teratol 67:563-571. doi:10.1002/bdra.10080
Drake AG, Klingenberg CP. 2008. The pace of morphological change: historical transformation of skull shape in St Bernard dogs. Proc R Soc B 275:71-76. doi:10.1098/rspb.2007.1169
Enlow DH, Hans HM. 1998. Crecimiento facial. México DF: Mc-Graw Hill Interamericana.
Frey L, Hauser WA. 2003. Epidemiology of neural tube defects. Epilepsia 44(Suppl 3):4-13. doi:10.1046/j.1528-1157.44.s3.2.x
Gkantidis N, Halazonetis DJ. 2011. Morphological integration between the cranial base and theface in children and adults. J Anat 218:426-438. doi:10.1111/j.1469-7580.2011.01346.x
Gonzalez PN, Perez I, Bernal V. 2011b. Ontogenetic allometry and cranial shape diversification among human populations from South America. Anat Rec 294:1864-1874. doi:10.1002/ar.21454
Gonzalez PN, Oyhenart EE, Hallgrímsson B. 2011a. Effects of environmental perturbations during postnatal development on the phenotypic integration of the skull. J Exp Zool 314B:547-561.doi:10.1002/jez.b.21430
Gonzalez PN, Hallgrímsson B, Oyhenart EE. 2011c. Developmental plasticity in covariance structure of the skull: effects of prenatal stress. J Anat 218:43-257. doi:10.1111/j.1469-7580.2010.01326.x
Gunz P, Neubauer S, Golovanova L, Doronichev V, Maureille B, Hublin JJ. 2012. A uniquely modern human pattern of endocranial development. Insights from a new cranial reconstruction of the Neandertal newborn from Mezmaiskaya. J Hum Evol 62:300-313. doi:10.1016/j.jhevol.2011.11.013
Hallgrímsson B, Hall BK. 2011. Epigenetics: the context of development. In: Hallgrímsson B, Hall BK, editors. Epigenetics: linking the genotype and phenotype in development and evolution. California: University of California Press. p 424-438.
Hallgrímsson B, Jamniczky H, Young NM, Rolian C, Parsons TE, Boughner JC, Marcucio RS. 2009. Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic covariation. Evol Biol 36:355-376. doi:10.1007/s11692-009-9076-5
Hallgrímsson B, Lieberman DE. 2008. Mouse models and the evolutionary developmental biology of the skull. Int Comp Biol 43:373-384. doi:10.1093/icb/icn076
Hallgrímsson B, Lieberman DE, Liu W, Ford-Hutchinson AF, Jirik FR. 2007. 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
Helms JA, Cordero D, Tapadia MD. 2005. New insights into craniofacial morphogenesis. Development 132:851-861. doi:10.1242/dev.01705
Hill CA, Martínez-Abadías N, Motch SM, Austin JR, Wang Y, Jabs EW, Richtsmeier JT, Aldridge K. 2013. Postnatal brain and skull growth in an Apert syndrome mouse model. Am J Med Genet A 161A:745-757. doi:10.1002/ajmg.a.35805
Klingenberg CP. 2009. Morphometric integration and modularity in configurations of landmarks: tools for evaluating a priori hypotheses. Evol Dev 11:405-421. doi:10.1111/j.1525-142X.2009.00347.x
Klingenberg CP. 2013. Visualizations in geometric morphometrics: how to read and how to make graphs showing shape changes. Hystrix 24:15-24. doi:10.4404/hystrix-24.1-7691
Klingenberg CP, McIntyre GS. 1998. Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with procrustes methods. Evolution 52:1363-1375.
Marcucio RS, Young NM, Hu D, Hallgrimsson B. 2011. Mechanisms that underlie co-variation of the brain and face. Genesis 49:177-189. doi:10.1002/dvg.20710
Marroig G, Shirai LT, Porto A, de Oliveira FB, De Conto V. 2009.The evolution of modularity in the mammalian skull II: evolutionary consequences. Evol Biol 36:136-148. doi:10.1007/s11692-009-9051-1
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:10.5061/dryad.12g3c7ht
Martínez-Abadías N, Heuzé Y, Wang Y, Jabs EW, Aldridge K, Richtsmeier JT. 2011. FGF/FGFR signaling coordinates skull development by modulating magnitude of morphological integration: evidence from Apert syndrome mouse models. PLoS One 6:e26425. doi:10.1371/journal.pone.0026425
Metscher BD. 2009. MicroCT for developmental biology: a versatile tool for high-contrast 3D imaging at histological resolutions. Dev Dyn 238:632-640. doi:10.1002/dvdy.21857
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, Bookstein FL. 2009. The ontogenetic trajectory of the phenotypic covariance matrix, with examples from craniofacial shape in rats and humans. Evolution 63:727-737. doi:10.1111/j.1558-5646.2008.00587.x
Monteiro LR. 1999. Multivariate regression models and geometric morphometrics: the search for causal factors in the analysis of shape. Syst Biol 48:192-199.
Morimoto K, Nishikuni K, Hirano S, Takemoto O, Futagi Y. 2003. Quantitative follow-up analysis by computed tomographic imaging in neonatal hydrocephalus. Pediatr Neurol 29:435-439. doi:10.1016/S0887-8994(03)00401-6
Moss ML, Young RW. 1960. A functional approach to craniology. Am J Phys Anthropol 18:281-291.
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
Nieman BJ, Blank MC, Roman BB, Henkelman RM, Millen KJ. 2012. If the skull fits: magnetic resonance imaging and microcomputed tomography for combined analysis of brain and skull phenotypes in the mouse. Physiol Genomics 44:992-1002. doi:10.1152/physiolgenomics.00093.2012
La Merrill M, Harper R, Birnbaum LS, Cardiff RD, Threadgill DW. 2010. Maternal dioxin exposure combined with a diet high in fat increases mammary cancer incidence in mice. Environ Health Perspect 118:596-601. doi:10.1289/ehp.0901047
Lieberman DE, Hallgrímsson B, Liu W, Parsons TE, Jamniczky H. 2008. Spatial packing, cranial base angulation, and craniofacial shape variation in the mammalian skull: testing a new model using mice. J Anat 212:720-735. doi:10.1111/j.1469-7580.2008.00900.x
Opperman LA. 2000. Cranial sutures as intramembranous bone growth sites. Dev Dyn 219:472-485. doi:10.1002/1097-0177(2000)9999:9999<::AIDDVDY1073>3.0.CO;2-F
Oyhenart EE, Sobrero MS, Pucciarelli HM.1994. Heredity, nutrition and craniofacial differentiation in weanling rats: A multivariate analysis. Am J Hum Biol 6:277-282. doi:10.1002/ajhb.1310060302
Polanski JM,Franciscus RG. 2006. Patterns of craniofacial integration in extant Homo, Pan, and Gorilla. Am J Phys Anthropol 131:38-49. doi:10.1002/ajpa.2042
Pucciarelli HM. 1991. Nutrición y morfogénesis craneofacial. Una contribución de la Antropología Biológica Experimental. Rev Arg Antrop Biol 10:7-19.
Pucciarelli HM, Goya RG, 1983. Effects of post-weaning malnutrition on the weight of the head components in rats. Acta Anat 115:231-237.
Pucciarelli HM, Oyhenart EE. 1987. Effects of maternal food restriction during lactation on craniofacial growth in weanling rats. Am J Phys Anthropol 72:67-75. doi:10.1002/ajpa.1330720109
Radiloff DR, Rinella ES, Threadgill DW. 2009. Modeling cancer patient populations in mice: complex genetic and environmental factors. Drug Discov Today Dis Models 4:83-88.
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 306B:360-378. doi:10.1002/jez.b
Richtsmeier JT, Flaherty K. 2013. Hand in glove: brain and skull in development and dysmorphogenesis. Acta Neuropathol. 125:469-489. doi:10.1007/s00401-013-1104-y
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2016-03-14
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Barbeito-Andrés, J., Gonzalez, P. N., & Hallgrímsson, B. (2016). Prenatal development of skull and brain in a mouse model of growth restriction. Revista Argentina De Antropología Biológica, 18(1). Retrieved from https://revistas.unlp.edu.ar/raab/article/view/2225
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