International Journal of Primatology

, Volume 36, Issue 3, pp 513–529 | Cite as

Phylogeny, Ecology, and Morphological Evolution in the Atelid Cranium

  • Alexander Bjarnason
  • Christophe Soligo
  • Sarah Elton


Reconstructing evolutionary relationships of living and extinct primate groups requires reliable phylogenetic inference based on morphology, as DNA is rarely preserved in fossil specimens. Atelids (family Atelidae) are a monophyletic clade and one of the three major adaptive radiations of south and central American primates (platyrrhines), including the genera Alouatta, Ateles, Brachyteles, and Lagothrix, and are diverse in morphology, body and brain size, locomotion, diet, social systems, and behavioral ecology. Molecular phylogenetic relationships of the extant atelid genera are well resolved, yet morphological analyses often support alternative phylogenetic relationships to molecular data. We collected geometric morphometric data from the crania of atelid taxa for phylogenetic analysis of the cranium, cranial base, and face and tested the hypotheses that cranial data maintain a phylogenetic signal, cranial base morphology most closely reflects the atelid molecular phylogeny, and facial and overall cranial morphology are shaped by diet and have experienced greater homoplasy. All analyses supported genus monophyly, and facial morphology maintained a strong phylogenetic signal inferring the atelid molecular phylogeny and a sister relationship between Brachyteles and Lagothrix, whereas results from the cranial base and whole cranium supported AtelesLagothrix and/or AlouattaBrachyteles clades reflecting homoplasy and ecological and dietary similarities. A phylogenetic signal in the atelid face is important for future studies integrating fossil taxa and supports evidence that congruence between molecular and morphological phylogenetics in primates is module and clade specific.


Atelid Cranium Diet Ecology Morphology Phylogeny 



The original research project was devised with Charlie Lockwood and is dedicated to his memory. We wish to thank the editor-in-chief Joanna Setchell, Walter Hartwig, and an anonymous reviewer for their insightful and constructive comments that helped improve this article. A. Bjarnason received partial financial support for the research undertaken from the Department of Anthropology (University College London), the Graduate Research Fund (UCL Graduate School), the Central Research Fund (University of London), and SYNTHESYS. We thank the following institutions for access to their collections: Natural History Museum, London; Field Museum of Natural History, Chicago; Museum für Naturkunde, Berlin; Naturhistorisches Museum, Vienna; Smithsonian National Museum of Natural History, Washington, DC; Naturhistoriska Riksmuseet, Stockholm; and the Anthropological Institute & Museum of the University of Zurich. We thank Louise Tomsett, Roberto Portela Miguez, Paula Jenkins, Bill Stanley, Bettina Wimmer, Frieder Mayer, Barbara Herzig, Olavi Gronwall, Tea Jashashvili, and Marcia Ponce de Leon for access to collections, and Andrea Cardini, Brian Villmoare, Alfie Rosenberger, Chris Klingenberg, and Jim Rohlf for help and advice.


  1. Adams, D. C., Rohlf, F. J., & Slice, D. E. (2004). Geometric morphometrics: Ten years of progress following the ‘revolution’. Italian Journal of Zoology, 71, 5–16.Google Scholar
  2. Anthony, M. R. L., & Kay, R. F. (1993). Tooth form and diet in ateline and alouattine primates: Reflections on the comparative method. American Journal of Physical Anthropology, 283, 356–382.Google Scholar
  3. Aristide, L., Rosenberger, A. L., Tejedor, M. F., & Perez, S. I. (2015). Modeling lineage and phenotypic diversification in the New World monkey (Platyrrhini, Primates) radiation. Moleclar Phylogenetics and Evolution, 82, 375–385.CrossRefGoogle Scholar
  4. Bruner, E., Mantini, S., & Manzi, G. (2004). A geometric morphometric approach to airorhynchy and functional cranial morphology in Alouatta (Atelidae, Primates). Journal of Anthropological Sciences, 82, 47–66.Google Scholar
  5. Bryant, H. N. (2001). Character polarity and the rooting of cladograms. In G. Wagner (Ed.), The character concept in evolutionary biology (pp. 319–337). San Diego: Academic Press.CrossRefGoogle Scholar
  6. Cardini, A., & Elton, S. (2008). Does the skull carry a phylogenetic signal? Evolution and modularity in the guenons. Biological Journal of the Linnean Society, 93, 813–834.CrossRefGoogle Scholar
  7. Cartelle, C., & Hartwig, W. C. (1996). A new extinct primate among the Pleistocene megafauna of Bahia, Brazil. Proceedings of the National Academy of Sciences of the USA, 93, 6405–6409.PubMedCentralPubMedCrossRefGoogle Scholar
  8. Cavalli-Sforza, L. L., & Edwards, A. W. F. (1967). Phylogenetic analysis: Models and estimation procedures. American Journal of Human Genetics, 19, 233–257.PubMedCentralPubMedGoogle Scholar
  9. Cheverud, J. M. (1982). Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution, 36, 499–516.CrossRefGoogle Scholar
  10. Cheverud, J. M. (1995). Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. The American Naturalist, 145, 63–89.CrossRefGoogle Scholar
  11. Cole, T. M. (1995). Comparative craniometry of the Atelinae (Platyrrhini, Primates): Function, development, and evolution. Ann Arbor: University Microfilms.Google Scholar
  12. Cole, T. M. I., Lele, S., & Richtsmeier, J. T. (2002). A parametic bootstrap approach to the detection of phylogenetic signals in landmark data. In N. F. P. Macleod (Ed.), Morphology, shape, and phylogenetics (pp. 194–219). London: Taylor & Francis.CrossRefGoogle Scholar
  13. Collard, M., & Wood, B. (2001). Homoplasy and the early hominid masticatory system: Inferences from analyses of extant hominoids and papionins. Journal of Human Evolution, 41, 167–194.PubMedCrossRefGoogle Scholar
  14. Collins, A. C. (2004). Atelinae phylogenetic relationships: The trichotomy revived? American Journal of Physical Anthropology, 124, 285–296.PubMedCrossRefGoogle Scholar
  15. Desper, R., & Gascuel, O. (2005). The minimum-evolution distance-based approach to phylogenetic inference. In O. Gascuel (Ed.), Mathematics of evolution and phylogeny (pp. 1–32). Oxford: Oxford University Press.Google Scholar
  16. Di Fiore, A., Chaves, P. B., Cornejo, F. M., Schmitt, C. A., Shanee, S., Cortes-Ortiz, L., Fagundes, V., Roos, C., & Pacheco, V. (2015). The rise and fall of a genus: Complete mtDNA genomes shed light on the phylogenetic position of yellow-tailed woolly monkeys, Lagothrix flavicauda, and on the evolutionary history of the family Atelidae (Primates: Platyrrhini). Molecular Phylogenetics and Evolution, 82, 495–510.PubMedCrossRefGoogle Scholar
  17. Di Fiore, A., Link, A., & Campbell, C. J. (2011). The atelines: Behavioural and socioecological diversity in a New World monkey radiation. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, S. K. Bearder, & R. M. Stumpf (Eds.), Primates in perspective (2nd ed., pp. 155–188). Oxford: Oxford University Press.Google Scholar
  18. Felsenstein, J. (1984). Distance methods for inferring phylogenies: A justification. Evolution, 38, 16–24.CrossRefGoogle Scholar
  19. Felsenstein, J. (2005). PHYLIP (Phylogeny Inference Package), Department of Genome Sciences, University of Washington, Seattle.Google Scholar
  20. Fitch, W. M., & Margoliash, E. (1967). Construction of phyogenetic trees. Science, 155, 279–284.PubMedCrossRefGoogle Scholar
  21. Fleagle, J. G. (2013). Primate adaptation and evolution (3rd ed.). San Diego: Academic Press.Google Scholar
  22. Ford, S. M. (1986). Systematics of the New World monkeys. In D. R. Swindler & J. Erwin (Eds.), Comparative primate biology, Vol. 1: Systematics, evolution, and anatomy (pp. 73–135). New York: Alan R. Liss.Google Scholar
  23. Ford, S. M., & Davis, L. C. (1992). Systematics and body size: Implications for feeding adaptations in New World monkeys. American Journal of Physical Anthropology, 88, 415–468.PubMedCrossRefGoogle Scholar
  24. Goodall, C. (1991). Procrustes methods in the statistical analysis of shape. Journal of the Royal Statistica Society B (Statistical Methodology), 53, 285–339.Google Scholar
  25. Goswami, A. (2006). Cranial modularity shifts during mammalian evolution. The American Naturalist, 168, 270–280.PubMedCrossRefGoogle Scholar
  26. Gower, J. C. (1975). Generalized procrustes analysis. Psychometrika, 40, 33–51.CrossRefGoogle Scholar
  27. Groves, C. (2001). Primate taxonomy. Washington, DC: Smithsonian Institution Press.Google Scholar
  28. Halenar, L.B. (2011a). Reconstructing the Locomotor Repertoire of Protopithecus brasiliensis. I. Body Size. The Anatomical Record, 294, 2024–2047.Google Scholar
  29. Halenar, L.B. (2011b). Reconstructing the locomotor repertoire of Protopithecus brasiliensis. II. Forelimb morphology. The Anatomical Record, 294, 2048–2063.Google Scholar
  30. Halenar, L. B., & Rosenberger, A. L. (2013). A closer look at the “Protopithecus” fossil assemblages: New genus and species from Bahia, Brazil. Journal of Human Evolution, 65, 374–390.PubMedCrossRefGoogle Scholar
  31. Hall, B. K. (2007). Homoplasy and homology: Dichotomy or continuum? Journal of Human Evolution, 52, 473–479.PubMedCrossRefGoogle Scholar
  32. Hallgrimsson, B., Willmore, K., Dorval, C., & Cooper, D. M. L. (2004). Craniofacial variability and modularity in macaques and mice. Journal of Experimental Zoology B: Molecular and Developmental Evolution, 302, 207–225.PubMedCrossRefGoogle Scholar
  33. Hartwig, W. C. (1993). Comparative morphology, ontogeny and phylogeny of the New World Monkeys (Platyrrhini). Ann Arbor: University Microfilms.Google Scholar
  34. Hartwig, W. C. (1995). Effect of life history on the squirrel monkey (Platyrrhini, Saimiri) cranium. American Journal of Physical Anthropology, 97, 435–449.Google Scholar
  35. Hartwig, W. C. (2005). Implications of molecular and morphological data for understanding ateline phylogeny. International Journal of Primatology, 26, 999–1015.CrossRefGoogle Scholar
  36. Hartwig, W. C., & Cartelle, C. (1996). A complete skeleton of the giant South American primate Protopithecus. Nature, 381, 307–311.PubMedCrossRefGoogle Scholar
  37. Hartwig, W. C., Rosenberger, A. L., Garber, P. A., & Norconk, M. A. (1996). On Atelines. In M. A. Norconk, A. L. Rosenberger, & P. A. Garber (Eds.), Adaptive radiations of neotropical primates (pp. 427–431). New York: Plenum Press.CrossRefGoogle Scholar
  38. Hartwig, W. C., Rosenberger, A. L., Norconk, M. A., & Owl, M. Y. (2011). Relative brain size, gut size, and evolution in New World monkeys. The Anatomical Record, 294, 2207–2221.PubMedCrossRefGoogle Scholar
  39. Harvati, K., & Weaver, T. D. (2006a). Reliability of cranial morphology in reconstructing neanderthal phylogeny. In K. Harvati & T. L. Harrison (Eds.), Neanderthals revisited: New approaches and perspectives (pp. 239–254). Dordrecht, the Netherlands: Springer Science+Business Media.Google Scholar
  40. Harvati, K., & Weaver, T. (2006b). Human cranial anatomy and the differential preservation of population history and climate signatures. The Anatomical Record, 288, 1225–1233.PubMedCrossRefGoogle Scholar
  41. Horovitz, I., & MacPhee, R. D. (1999). The quaternary cuban platyrrhine Paralouatta vaonai and the origin of Antillean monkeys. Journal of Human Evolution, 36, 33–68.PubMedCrossRefGoogle Scholar
  42. Horovitz, I., & Meyer, A. (1997). Evolutionary trends in the ecology of New World monkeys inferred from a combined phylogenetic analysis of nuclear, mitochondrial, and morphological data. In T. J. Givnish & K. J. Sytsma (Eds.), Molecular evolution and adaptive radiation (pp. 189–224). New York: Cambridge University Press.Google Scholar
  43. Horovitz, I., Zardoya, R., & Meyer, A. (1998). Platyrrhine systematics: A simultaneous analysis of molecular and morphological Data. American Journal of Physical Anthropology, 106, 261–281.PubMedCrossRefGoogle Scholar
  44. Isler, K., Kirk, E. C., Miller, J. M. A., Albrecht, G. A., Gelvin, B. R., & Martin, R. D. (2008). Endocranial volume of primate species: Scaling analyses using a comprehensive and reliable dataset. Journal of Human Evolution, 55, 967–978.PubMedCrossRefGoogle Scholar
  45. Jameson Kielsing, N. M., Yi, S. V., Xu, K., Gianluca Sperone, F., & Wildman, D. E. (2015). The tempo and mode of New World monkey evolution and biogeography in the context of phylogenomic analysis. Molecular Phylogenetics and Evolution, 82, 386–399.CrossRefGoogle Scholar
  46. Jenner, R. A. (2004). Accepting partnership by submission? Morphological phylogenetics in a molecular millenium. Systematic Biology, 53, 333–359.Google Scholar
  47. Jones, A. L. (2008). The evolution of brachiation in ateline primates, ancestral character states and history. American Journal of Physical Anthropology, 137, 123–144.PubMedCrossRefGoogle Scholar
  48. Kay, R. F. (1990). The phyletic relationships of extant and fossil Pitheciinae (Platyrrhini, Anthropoidea). Journal of Human Evolution, 19, 175–208.CrossRefGoogle Scholar
  49. Kay, R. F. (2015). Biogeography in deep time- What do phylogenetics, geology, and paleoclimate tell us about early platyrrhine evolution? Journal of Human Evolution, 82, 358–374.Google Scholar
  50. Kay, R. F., Fleagle, J. G., Mitchell, T. R. T., Colbert, M., Brown, T., & Powers, D. W. (2008). The anatomy of Dolichocebus gaimanensis, a stem platyrrhine monkey from Argentina. Journal of Human Evolution, 54, 323–382.PubMedCrossRefGoogle Scholar
  51. Kinzey, W. G. (1997). New World primates: Ecology, evolution, and behavior. New York: Aldine de Gruyter.Google Scholar
  52. Kitching, I. J., Forey, P. L., Humphries, C. J., & Williams, D. M. (1998). Cladistics: The Theory and Practice of Parsimony. Oxford, Oxford University Press.Google Scholar
  53. Klingenberg, C. P. (2008). Morphological integration and developmental modularity. Annual Review of Ecology, Evolution and Systematics, 39, 115–132.CrossRefGoogle Scholar
  54. Klingenberg, C. P. (2010). Evolution and development of shape: Integrating quantitative approaches. Nature Reviews Genetics, 11, 623–635.PubMedGoogle Scholar
  55. Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353–357.PubMedCrossRefGoogle Scholar
  56. Kuhner, M. K., & Felsenstein, J. (1994). A simulation comparison of phylogeny algorithms under equal and unequal evolutionary rates. Molecular Biology and Evolution, 11, 459–468.PubMedGoogle Scholar
  57. Lieberman, D. E. (1997). Making behavioural and phylogenetic inferences from hominid fossils: Considering the developmental influence of mechanical forces. Annual Review of Anthropology, 26, 185–210.CrossRefGoogle Scholar
  58. Lieberman, D. E., Pearson, O. M., & Mowbray, K. M. (2000a). Basicranial influence on overall cranial shape. Journal of Human Evolution, 38, 291–315.PubMedCrossRefGoogle Scholar
  59. Lieberman, D. E., Ross, C. F., & Ravosa, M. (2000b). The primate cranial base: Ontogeny, function and integration. Yearbook of Physical Anthropology, 43, 117–169.CrossRefGoogle Scholar
  60. Lieberman, D. E., Wood, B. A., & Pilbeam, D. R. (1996). Homoplasy and early Homo: An analysis of the evolutionary relationships of H. habilis sensu stricto and H. rudolfensis. Journal of Human Evolution, 30, 97–120.CrossRefGoogle Scholar
  61. Lockwood, C. A. (1999). Homoplasy and adaptation in the atelid postcranium. American Journal of Physical Anthropology, 108, 459–482.PubMedCrossRefGoogle Scholar
  62. Lockwood, C. A., & Fleagle, J. G. (1999). The recognition and evaluation of homoplasy in primate and human evolution. Yearbook of Physical Anthropology, 42, 189–232.CrossRefGoogle Scholar
  63. 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. Proceedings of the National Academy of Sciences of the USA, 101, 4356–4360.PubMedCentralPubMedCrossRefGoogle Scholar
  64. Lockwood, C. A. (2007). Adaptation and functional integration In primate phylogenetics. Journal of Human Evolution, 52, 490–503.Google Scholar
  65. Marroig, G., & Cheverud, J. (2001). A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology and ontogeny during cranial evolution of New World monkeys. Evolution, 55, 2576–2600.PubMedCrossRefGoogle Scholar
  66. Marroig, G., & Cheverud, J. (2004). Did natural selection or genetic drift produce the cranial diversification of Neotropical monkeys? The American Naturalist, 163, 417–428.PubMedCrossRefGoogle Scholar
  67. Marroig, G., & Cheverud, J. (2005). Size as a line of least evolutionary resistace: Diet and adaptive morphological radiation in New World monkeys. Evolution, 59, 1128–1142.PubMedCrossRefGoogle Scholar
  68. 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. Journal of Evolutionary Biology, 36, 136–148.CrossRefGoogle Scholar
  69. Matthews, L. J., & Rosenberger, A. L. (2008). Taxon combinations, parsimony analysis (PAUP*), and the taxonomy of the yellow-tailed woolly monkey, Lagothrix flavicauda. American Journal of Physical Anthropology, 137, 245–255.PubMedCrossRefGoogle Scholar
  70. Mihaescu, R., Levy, D., & Pachter, L. (2009). Why neighbor-joining works. Algorithmica, 54, 1–24.CrossRefGoogle Scholar
  71. Mitteroecker, P., & Gunz, P. (2009). Advances in geometric morphometrics. Journal of Evolutionary Biology, 36, 235–247.CrossRefGoogle Scholar
  72. Nei, M., & Kumar, S. (2000). Molecular evolution and phylogenetics. Oxford: Oxford University Press.Google Scholar
  73. Nixon, K. C., & Carpenter, J. M. (1993). On outgroups. Cladistics, 9, 413–426.CrossRefGoogle Scholar
  74. Norconk, M. A., Wright, B. W., Conklin-Brittain, N. L., & Vinyard, C. J. (2009). Mechanical and nutritional properties of food as factors in platyrrhine dietary adaptations. In P. A. Garber, A. Estrada, J. C. Bicca-Marques, E. W. Heymann, & K. B. Strier (Eds.), South American primates comparative perspectives in the study of behaviour, ecology, and conservation (pp. 279–319). New York: Springer Science + Business Media.Google Scholar
  75. Olson, T. R. (1981). Basicrania and evolution of the pliocene hominids. In C. B. Stringer (Ed.), Aspects of human evolution (pp. 99–128). London: Taylor & Francis.Google Scholar
  76. Orlosky, F. (1973). Comparative dental morphology of extant and extinct Cebidae. Ann Arbor: University Microfilms.Google Scholar
  77. Perez, S. I., Klaczko, J., Rocatti, G., & Dos Reis, S. F. (2011). Patterns of cranial shape diversification during the branching process of New World monkeys (Primates: Platyrrhini). Journal of Evolutionary Biology, 24, 1826–1835.PubMedCrossRefGoogle Scholar
  78. Philippe, H., Telford, M. J. (2006). Large-scale sequencing and the new animal phylogeny. Trends in Ecology and Evolution, 21, 614–620.Google Scholar
  79. 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. Journal of Evolutionary Biology, 36, 118–135.CrossRefGoogle Scholar
  80. Rivero, M., & Arredondo, O. (1991). Paralouatta varonai, a new Quaternary platyrrhine from Cuba. Journal of Human Evolution, 21, 1–11.CrossRefGoogle Scholar
  81. Rohlf, F. J. (2000a). On the use of shapes spaces to compare morphometric methods. Hystrix, 11, 1–17.Google Scholar
  82. Rohlf, F. J. (2000b). Statistical power comparisons among alternative morphometric methods. American Journal of Physical Anthropology, 111, 463–478.PubMedCrossRefGoogle Scholar
  83. Rohlf, F. J. (2003). Bias and error in estimates of mean shape in geometric morphometrics. Journal of Human Evolution, 44, 665–683.PubMedCrossRefGoogle Scholar
  84. Rohlf, F. J., & Marcus, L. F. (1993). A revolution in morphometrics. Trends in Ecology and Evolution, 8, 129–132.CrossRefGoogle Scholar
  85. Rohlf, F. J., & Slice, D. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39, 40–59.CrossRefGoogle Scholar
  86. Roseman, C.C., Willmore, K.E., Rogers, J., Hildebolt, C., Sadler, B.E., Richtsmeier, J.T., & Cheverud, J.M. (2010). Genetic and environmental contributions to variation in baboon cranial morphology. American Journal of Physical Anthropology, 143, 1–12.Google Scholar
  87. Rosenberger, A. L. (1983). Tale of tails: Parallelusm and prehensility. American Journal of Physical Anthropology, 60, 103–107.PubMedCrossRefGoogle Scholar
  88. Rosenberger, A. L. (1984). Fossil New World monkeys dispute the molecular clock. Journal of Human Evolution, 13, 737–742.CrossRefGoogle Scholar
  89. Rosenberger, A. L. (1992). Evolution of feeding niches in New World monkeys. American Journal of Physical Anthropology, 88, 525–562.PubMedCrossRefGoogle Scholar
  90. Rosenberger, A. L., Halenar, L., & Cooke, S. (2011). The making of platyrrhine semifolivores: Models for the evolution of folivory in primates. The Anatomical Record, 294, 2112–2130.PubMedCrossRefGoogle Scholar
  91. Rosenberger, A. L., Halenar, L., Cooke, S., & Hartwig, W. C. (2008). Morphology and evolution of the spider monkey, genus Ateles. In C. J. Campbell (Ed.), Spider monkeys: Behaviour, ecology and evolution of the genus Ateles (pp. 19–49). Cambridge, U.K.: Cambridge University Press.Google Scholar
  92. Rosenberger, A. L., & Strier, K. B. (1989). Adaptive radiation of the ateline primates. Journal of Human Evolution, 18, 717–750.CrossRefGoogle Scholar
  93. Rosenberger, A. L., Tejedor, M. F., Cooke, S., Halenar, L., & Pekkar, S. (2009). Platyrrhine ecophylogenetics, past and present. In P. A. Garber, A. Estrada, J. C. Bicca-Marques, E. W. Heymann, & K. B. Strier (Eds.), South American primates: Comparative perspectives in the study of behaviour, ecology and conservation (pp. 69–113). Developments in Primatology: Progress and Prospects. New York: Springer Science + Business Media.Google Scholar
  94. Ruiz-Garcia, M., Pinedo-Castro, M., & Shostell, J. M. (2015). How many genera and species of woolly monkeys (Atelidae, Platyrrhine, Primates) are there? The first molecular analysis of Lagothrix flavicauda, an endemic Peruvian primate species. Molecular Phylogenetics and Evolution, 79, 179–198.CrossRefGoogle Scholar
  95. Saitou, N., & Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425.PubMedGoogle Scholar
  96. Schuh, R.T., & Brower, A.V.Z. (2009). Biological Systematics: Principles and Applications. (2nd ed.) New York: Cornell University Press.Google Scholar
  97. 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, 134, 312–322.PubMedCrossRefGoogle Scholar
  98. Strait, D. S., Grine, F. E., & Moniz, M. A. (1997). A reappraisal of early hominid phylogeny. Journal of Human Evolution, 32, 17–82.PubMedCrossRefGoogle Scholar
  99. Strier, K. B. (1992). Atelinae adaptations: Behavioural strategies and ecological constraints. American Journal of Physical Anthropology, 88, 515–524.PubMedCrossRefGoogle Scholar
  100. von Cramon-Taubadel, N. (2014). The microevolution of modern human cranial variation: Implications for hominin and primate evolution. Annals of Human Biology, 41, 323–335.CrossRefGoogle Scholar
  101. 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. Journal of Human Evolution, 62, 640–653.Google Scholar
  102. Wake, D. B., Wake, M. H., & Specht, C. D. (2011). Homoplasy: From detecting pattern to determining process and mechanism of evolution. Science, 331, 1032–1035.PubMedCrossRefGoogle Scholar
  103. Wiens, J. J. (2004). The role of morphological data in phylogeny reconstruction. Systematic Biology, 53, 653–661.Google Scholar
  104. Wood, B. A., & Lieberman, D. E. (2001). Craniodental variation in Paranthropus boisei: A developmental and functional perspective. American Journal of Physical Anthropology, 116, 13–25.PubMedCrossRefGoogle Scholar
  105. Yang, Z. (2006). Computational molecular evolution. Oxford: Oxford University Press.CrossRefGoogle Scholar
  106. Zelditch, M. L., Swiderski, D. L., Sheets, H. D., & Fink, W. L. (2004). Geometric morphometrics for biologists: A primer. London: Elsevier Academic Press.Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Alexander Bjarnason
    • 1
  • Christophe Soligo
    • 1
  • Sarah Elton
    • 2
  1. 1.Department of AnthropologyUniversity College LondonLondonUK
  2. 2.Department of AnthropologyDurham UniversityDurhamUK

Personalised recommendations