Genomic validation of the differential preservation of population history in modern human cranial anatomy

American Journal of Physical Anthropology

Volumn 162, Issue 1, 2017, Pages 170-179

  Reyes Centeno, Hugo ^a   Ghirotto, Silvia ^b   Harvati, Katerina ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF FERRARA   (Italy)

Author keywords

geometric morphometrics; population genetics; quantitative genetics; SNPs

Indexed keywords

ADULT; ANATOMY; GENE MUTATION; GENETIC DISTANCE; GENETIC VARIATION; HUMAN; MAJOR CLINICAL STUDY; MORPHOMETRICS; QUANTITATIVE GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM; TEMPORAL BONE; VALIDATION PROCESS; ANATOMY AND HISTOLOGY; CEPHALOMETRY; FEMALE; GENETICS; GENOMICS; MALE; PHYSICAL ANTHROPOLOGY; POPULATION GENETICS; PROCEDURES; REPRODUCIBILITY; SKULL; STANDARDS;

ADULT; ANTHROPOLOGY, PHYSICAL; CEPHALOMETRY; FEMALE; GENETICS, POPULATION; GENOMICS; HUMANS; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; REPRODUCIBILITY OF RESULTS; SKULL;

EID: 84994509663     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.23060     Document Type: Article

References (70)

1. Betti, L., Balloux, F., Amos, W., Hanihara, T., & Manica, A. (2009). Distance from Africa, not climate, explains within-population phenotypic diversity in humans. Proc Biol Sci, 276, 809–814.
2. Betti, L., Balloux, F., Hanihara, T., & Manica, A. (2010). The relative role of drift and selection in shaping the human skull. Am J Phys Anthrop, 141, 76–82.
3. Buikstra, J. E., & Ubelaker, D. H. (1994). Standards for data collection from human skeletal remains. Fayetteville: Arkansas Archaeological Survery.
4. Cardini, A., & Elton, S. (2008). Does the skull carry a phylogenetic signal? Evolution and modularity in the guenons. Biol J Linn Soc, 93, 813–834.
5. Carson, E. A. (2006). Maximum likelihood estimation of human craniometric heritabilities. Am J Phys Anthrop, 131, 169–180.
6. Chakraborty, R., & Danker-Hopfe, H. (1991). Analysis of population structure: A comparative study of different estimators of Wright's fixation indices. In Govindaraju V, Raghavan VV, and Rao CR, (Eds). Handbook of statistics. Oxford: North-Holland. (pp. 203–254).
7. Collard, M., & Wood, B. (2000). How reliable are human phylogenetic hypotheses? Proc Natl Acad Sci USA, 97, 5003–5006.
8. Colonna, V., Boattini, A., Guardiano, C., Dall'ara, I., Pettener, D., Longobardi, G., & Barbujani, G. (2010). Long-range comparison between genes and languages based on syntactic distances. Hum Hered, 70, 245–254.
9. Dahm, M. C., Shepherd, R. K., & Clark, G. M. (1993). The postnatal growth of the temporal bone and its implications for cochlear implantation in children. Acta Otolaryngol, 113, 4–39.
10. Dow, M. M., & Cheverud, J. M. (1985). Comparison of distance matrices in studies of population structure and genetic microdifferentiation: Quadratic assignment. Am J Phys Anthrop, 68, 367–373.
11. Edwards, S. V. (2009). Is a new and general theory of molecular systematics emerging? Evolution, 63, 1–19.
12. Goldstein, D. B., Ruiz Linares, A., Cavalli-Sforza, L. L., & Feldman, M. W. (1995). An evaluation of genetic distances for use with microsatellite loci. Genetics, 139, 463–471.
13. Gower, J. (1975). Generalized procrustes analysis. Psychometrika, 40, 33–51.
14. Harpending, H. C., & Ward, R. H. (1982). Chemical systematics and human populations. In: Nitecki M, editor. Biochemical aspects of evolutionary biology. Chicago: University of Chicago Press. pp 213–256.
15. Harvati, K. (2001). The Neanderthal problem: 3-D geometric morphometric models of cranial shape variation within and among species. Unpublished Ph.D. Dissertation, Department Anthropology, City University of New York.
16. Harvati, K. (2003). Quantitative analysis of neanderthal temporal bone morphology using three-dimensional geometric morphometrics. Am J Phys Anthrop, 120, 323–338.
17. Harvati, K., & Weaver, T. (2006a). Human cranial anatomy and the differential preservation of population history and climate signatures. Anat Rec A Discov Mol Cell Evol Biol, 288, 1225–1233.
18. Harvati, K., & Weaver, T. (2006b). Reliability of cranial morphology in reconstructing Neanderthal phylogeny. In: K Harvati, & T Harrison (Eds.), Neanderthals revisited: New approaches and perspectives. Dordrecht: Springer. pp 239–254.
19. Hill, C. A. (2011). Ontogenetic change in temporal bone pneumatization in humans. Anat Rec, 294, 1103–1115.
20. Hlusko, L. J. (2004). Integrating the genotype and phenotype in hominid paleontology. Proc Natl Acad Sci USA, 101, 2653–2657.
21. ST. Nat Rev Genet, 10, 639–650.
22. Hubbe, M., Hanihara, T., & Harvati, K. (2009). Climate signatures in the morphological differentiation of worldwide modern human populations. Anat Rec, 292, 1720–1733.
23. Hubbe, M., Neves, W. A., & Harvati, K. (2010). Testing evolutionary and dispersion scenarios for the settlement of the new World. PLoS One, 5, e11105.
24. Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Mol Ecol Resour, 11, 353–357.
25. Klingenberg, C. P., & Monteiro, L. R. (2005). Distances and directions in multidimensional shape spaces: Implications for morphometric applications. Syst Biol, 54, 678–688.
26. ST comparisons: Evolutionary and ecological insights from genomic heterogeneity. Nat Rev Genet, 14, 179–190.
27. Lockwood, C. A., Kimbel, W. H., & Lynch, J. M. (2004). Morphometrics and hominoid phylogeny: Support for a chimpanzee–human clade and differentiation among great ape subspecies. Proc Natl Acad Sci USA, 101, 4356–4360.
28. Lockwood, C. A., Lynch, J. M., & Kimbel, W. H. (2002). Quantifying temporal bone morphology of great apes and humans: An approach using geometric morphometrics. J Anat, 201, 447–464.
29. Manica, A., Amos, W., Balloux, F., & Hanihara, T. (2007). The effect of ancient population bottlenecks on human phenotypic variation. Nature, 448, 346–348.
30. Mantel, N. (1967). The detection of disease clustering and a generalized regression approach. Cancer Res, 27, 209–220.
31. Mardia, K. V., Bookstein, F. L., & Moreton, I. J. (2000). Statistical assessment of bilateral symmetry of shapes. Biometrika, 87, 285–300.
32. Martínez-Abadías, N., Esparza, M., Sjøvold, T., González-José, R., Santos, M., & Hernández, M. (2009). Heritability of human cranial dimensions: Comparing the evolvability of different cranial regions. J Anat, 214, 19–35.
33. Martínez-Abadías, N., Esparza, M., Sjøvold, T., González-José, R., Santos, M., Hernández, M., & Klingenberg, C. P. (2012). Pervasive genetic integration directs the evolution of human skull shape. Evolution, 66, 1010–1023.
34. Nemzek, W. R., Brodie, H. A., Chong, B. W., Babcook, C. J., Hecht, S. T., Salamat, S., … Seibert, J. A. (1996). Imaging findings of the developing temporal bone in fetal specimens. Am J Neuroradiol, 17, 1467–1477.
35. Pinhasi, R., & von Cramon-Taubadel, N. (2009). Craniometric data supports demic diffusion model for the spread of agriculture into Europe. PLoS One, 4, e6747.
36. Relethford, J. H. (1991). Genetic drift and anthropometric variation in Ireland. Hum Biol, 63, 155–165.
37. Relethford, J. H. (2004a). Boas and beyond: Migration and craniometric variation. Am J Hum Biol, 16, 379–386.
38. Relethford, J. H. (2004b). Global patterns of isolation by distance based on genetic and morphological data. Hum Biol, 76, 499–513.
39. Relethford, J. H., & Blangero, J. (1990). Detection of differential gene flow from patterns of quantitative variation. Hum Biol, 62, 5–25.
40. Relethford, J. H., Crawford, M. H., & Blangero, J. (1997). Genetic drift and gene flow in post-famine Ireland. Hum Biol, 69, 443–465.
41. Relethford, J. H., & Harpending, H. C. (1994). Craniometric variation, genetic theory, and modern human origins. Am J Phys Anthrop, 95, 249–270.
42. Relethford, J. H., & Lees, F. C. (1982). The use of quantitative traits in the study of human population structure. Am J Phys Anthrop, 25, 113–132.
43. Reyes-Centeno, H., Ghirotto, S., Détroit, F., Grimaud-Hervé, D., Barbujani, G., & Harvati, K. (2013). Testing the “Negrito” hypothesis: Modern human phenotypic and genetic diversity in Asia. Proceedings of the European Society for the study of Human Evolution. Vienna. p 182.
44. Reyes-Centeno, H., Ghirotto, S., Détroit, F., Grimaud-Hervé, D., Barbujani, G., & Harvati, K. (2014). Genomic and cranial phenotype data support multiple modern human dispersals from Africa and a southern route into Asia. Proc Natl Acad Sci USA, 111, 7248–7253.
45. Reyes-Centeno, H., Hubbe, M., Hanihara, T., Stringer, C., & Harvati, K. (2015). Testing modern human out-of-Africa dispersal models and implications for modern human origins. J Hum Evol, 87, 95–106.
46. Rogers, A. R. (2014). How population growth affects linkage disequilibrium. Genetics, 197, 1329–1341.
47. Rohlf, F. J., & Slice, D. (1990). Extensions of the procrustes method for the optimal superimposition of landmarks. Syst Biol, 39, 40–59.
48. Roseman, C. C. (2004). Detecting interregionally diversifying natural selection on modern human cranial form by using matched molecular and morphometric data. Proc Natl Acad Sci USA, 101, 12824–12829.
49. Roseman, C. C., & Weaver, T. D. (2007). Molecules versus morphology? not for the human cranium. Bioessays, 29, 1185–1188.
50. Šešelj, M., Duren, D. L., & Sherwood, R. J. (2015). Heritability of the human craniofacial complex. Anatomical Record, 298, 1535–1547.
51. 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. J Hum Evol, 62, 155–164.
52. Slatkin, M. (1995). A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139, 457–462.
53. Slice, D. E. (1994). −1999. Morpheus et al., software for morphometric research. Stonybrook, New York: Department of Ecology and Evolution, State University of New York.
54. Smith, H. F. (2009). Which cranial regions reflect molecular distances reliably in humans? Evidence from three-dimensional morphology. Am J Hum Biol, 21, 36–47.
55. Smith, H. F., Ritzman, T., Otárola-Castillo, E., & Terhune, C. E. (2013). A 3-D geometric morphometric study of intraspecific variation in the ontogeny of the temporal bone in modern Homo sapiens. J Hum Evol, 65, 479–489.
56. Smith, H. F., Terhune, C. E., & Lockwood, C. A. (2007). Genetic, geographic, and environmental correlates of human temporal bone variation. Am J Phys Anthrop, 134, 312–322.
57. Smouse, P. E., Long, J. C., & Sokal, R. R. (1986). Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Biol, 35, 627–632.
58. Spitze, K. (1993). Population structure in Daphnia obtusa: Quantitative genetic and allozymic variation. Genetics, 135, 367–374.
59. Tassi, F., Ghirotto, S., Mezzavilla, M., Vilaça, S. T., De Santi, L., & Barbujani, G. (2015). Early modern human dispersal from Africa: Genomic evidence for multiple waves of migration. Invest Gene, 6, 1–16.
60. Tattersall, I., & Schwartz, J. H. (2008). The morphological distinctiveness of Homo sapiens and its recognition in the fossil record: Clarifying the problem. Evol Anthropol, 17, 49–54.
61. Tenesa, A., Navarro, P., Hayes, B. J., Duffy, D. L., Clarke, G. M., Goddard, M. E., & Visscher, P. M. (2007). Recent human effective population size estimated from linkage disequilibrium. Genome Res, 17, 520–526.
62. von Cramon-Taubadel, N. (2009a). Congruence of individual cranial bone morphology and neutral molecular affinity patterns in modern humans. Am J Phys Anthrop, 140, 205–215.
63. von Cramon-Taubadel, N. (2009b). Revisiting the homoiology hypothesis: The impact of phenotypic plasticity on the reconstruction of human population history from craniometric data. J Hum Evol, 57, 179–190.
64. von Cramon-Taubadel, N. (2011). The relative efficacy of functional and developmental cranial modules for reconstructing global human population history. Am J Phys Anthrop, 146, 83–93.
65. von Cramon-Taubadel, N., & Lycett, S. J. (2008). Brief communication: Human cranial variation fits iterative founder effect model with African origin. Am J Phys Anthrop, 136, 108–113.
66. von Cramon-Taubadel, N., & Pinhasi, R. (2011). Craniometric data support a mosaic model of demic and cultural neolithic diffusion to outlying regions of Europe. Proc Biol Sci, 278, 2874–2880.
67. von Cramon-Taubadel, N., & Smith, H. F. (2012). The relative congruence of cranial and genetic estimates of hominoid taxon relationships: Implications for the reconstruction of hominin phylogeny. J Hum Evol, 62, 640–653.
68. Weir, B. S., & Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 1358–1370.
69. White, T. D., & Folkens, P. A. (2005). The human bone manual. San Diego: Academic Press.
70. Wright, S. (1951). The genetical structure of populations. Ann Eugen, 15, 323–354.