Comparative Quantitative Genetic Analysis of Cranial Capacity and Craniofacial Morphology in Two Closely Related Primate Species

  • Jessica L. JoganicEmail author
  • Katherine E. Willmore
  • Charles C. Roseman
  • Joan T. Richtsmeier
  • Jeffrey Rogers
  • James M. Cheverud
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


Evolutionary change in a character is due to a combination of the direct effects of selection on that character and the indirect effects of selection on characters that are genetically correlated with the character in question (Lande and Arnold 1983 ; Cheverud 1996 ). Therefore, selection on a single component within a correlated unit will result in coordinated evolution of the entire complex (Lande 1979 ; Cheverud 1982, 1984 ; Falconer and MacKay 1996 ). Due to the ubiquity of phenotypic correlations among traits, natural selection appears to act on many characters simultaneously. However, genetic correlations among traits can pose constraints on phenotypic evolution because these correlations are capable of altering both the rate and direction of evolution from the optimal path defi ned by natural selection (Cheverud 1984 ; Wagner and Altenberg 1996 ). If traits that are inherited together ultimately evolve together, then the challenge in explaining the correlated appearance of particular characters and understanding coordinated evolution lies in identifying genetically integrated morphological traits.


Genetic Correlation Brain Size Additive Genetic Variance Cranial Vault Selection Gradient 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Cranial capacity


Craniofacial complex


Southwest National Primate Research Center


Variance/covariance matrix



We acknowledge support from NSF grant BCS-0725068 and the Genomics of Cranial Morphology Project. We would like to thank Dr. Heather Lawson for computer programming support. This study was made possible, in part, by financial support from the National Institutes of Health Grant P40 RR003640 to the Caribbean Primate Research Center (CPRC).


  1. Ackermann RR (2005) Ontogenetic integration of the hominin face. J Hum Evol 48:175–197PubMedCrossRefGoogle Scholar
  2. Ackermann RR, Cheverud JM (2002) Discerning evolutionary processes in patterns of tamarin (genus Saguinus) craniofacial variation. Am J Phys Anthropol 117:260–271PubMedCrossRefGoogle Scholar
  3. Ackermann RR, Rogers J, Cheverud JM (2006) Identifying the morphological signatures of hybridization in primate and human evolution. J Hum Evol 51:632–645PubMedCrossRefGoogle Scholar
  4. Aiello LC, Wheeler P (1995) The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr Anthropol 36:199–221CrossRefGoogle Scholar
  5. Almasy L, Blangero J (1998) Multipoint quantitative-trait linkage analysis in general pedigrees. Am J Hum Genet 62:1198–1211PubMedCrossRefGoogle Scholar
  6. Blackith RE, Reyment RA (1971) Multivariate morphometrics. Academic, New YorkGoogle Scholar
  7. Blangero J, Williams JT, Almasy L (2001) Variance component methods for detecting complex trait loci. Adv Genet 42:151–181PubMedCrossRefGoogle Scholar
  8. Boughner JC, Wat S, Diewer VM, Young NM, Browder LW, Hallgrímsson B (2008) Short-faced mice and developmental interactions between the brain and the face. J Anat 213:646–662PubMedCrossRefGoogle Scholar
  9. Bruner E (2007) Cranial shape and size variation in human evolution: structural and functional perspectives. Childs Nerv Syst 23:1357–1365PubMedCrossRefGoogle Scholar
  10. Cheverud JM (1981) Epiphyseal union and dental eruption in Macaca mulatta. Am J Phys Anthropol 56:157–167PubMedCrossRefGoogle Scholar
  11. Cheverud JM (1982) Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution 36:499–516CrossRefGoogle Scholar
  12. Cheverud JM (1984) Quantitative genetics and developmental constraints on evolution by selection. J Theor Biol 110:155–171PubMedCrossRefGoogle Scholar
  13. Cheverud JM (1988) A comparison of genetic and phenotypic correlations. Evolution 42:958–968CrossRefGoogle Scholar
  14. Cheverud JM (1995) Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. Am Nat 145:63–89CrossRefGoogle Scholar
  15. Cheverud JM (1996) Developmental integration and the evolution of pleiotrophy. Am Zool 36:44–50Google Scholar
  16. Cheverud JM, Buikstra JE (1981a) Quantitative genetics of skeletal nonmetric traits in the rhesus macaques on Cayo Santiago: I. single trait heritabilities. Am J Phys Anthropol 54:43–49PubMedCrossRefGoogle Scholar
  17. Cheverud JM, Buikstra JE (1981b) Quantitative genetics of skeletal nonmetric traits in the rhesus macaques on Cayo Santiago: II. phenotypic, genetic, and environmental correlations between traits. Am J Phys Anthropol 54:51–58PubMedCrossRefGoogle Scholar
  18. Cheverud JM, Falk D, Vannier M, Konigsberg L, Helmkamp RC, Hildebolt C (1990) Heritability of brain size and surface features in rhesus macaques (Macaca mulatta). J Hered 81:51–57PubMedGoogle Scholar
  19. de Oliveira FB, Porto A, Marroig G (2009) Covariance structure in the skull of Catarrhini: a case of pattern stasis and magnitude evolution. J Hum Evol 56:417–430PubMedCrossRefGoogle Scholar
  20. Falconer DS, Mackay TFC (1996) Quantitative genetics. Pearson Education Limited, Harlow, EnglandGoogle Scholar
  21. Fish JL, Lockwood CA (2003) Dietary constraints on encephalization in primates. Am J Phys Anthropol 120:171–181PubMedCrossRefGoogle Scholar
  22. Hershkovitz P (1977) Living new world primates (Platyrrhini) 1: with an introduction to primates. University of Chicago Press, ChicagoGoogle Scholar
  23. Konigsberg L, Cheverud J (1992) Uncertain paternity in primate quantitative genetic studies. Am J Primatol 27:133–144CrossRefGoogle Scholar
  24. Lande R (1979) Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution 33:402–416CrossRefGoogle Scholar
  25. Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226CrossRefGoogle Scholar
  26. Lieberman DE, Hallgrímsson B, Liu W, Parsons TE, Jamniczky HA (2008) Spatial packing, cranial base angulation, and craniofacial shape variation in the mammalian skull: testing a new model using mice. J Anat 212:720–735PubMedCrossRefGoogle Scholar
  27. Lovsfold D (1988) Quantitative genetics of morphological differentiation in Peromyscus: II. analysis of selection and drift. Evolution 42:54–67CrossRefGoogle Scholar
  28. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland, MAGoogle Scholar
  29. Manly BFJ (1986) Multivariate statistical methods: a primer. Chapman & Hall, New YorkGoogle Scholar
  30. Marroig G, Cheverud JM (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 55:2576–2600PubMedGoogle Scholar
  31. Marroig G, De Vivo M, Cheverud JM (2004) Cranial evolution in sakis (Pithecia, Platyrrhini) II: evolutionary processes and morphological integration. J Evol Biol 17:144–155PubMedCrossRefGoogle Scholar
  32. McNab BK, Eisenberg JF (1989) Brain size and its relation to the rate of metabolism in mammals. Am Nat 133:157–167CrossRefGoogle Scholar
  33. Mousseau TA, Roff DA (1987) Natural selection and the heritability of fitness components. Heredity 59:181–197PubMedCrossRefGoogle Scholar
  34. Persing JA, Morgan EP, Cronin AJ, Wolcott WP (1991) Skull base expansion: craniofacial effects. Plast Reconstr Surg 87:1028–1033PubMedCrossRefGoogle Scholar
  35. Rawlins RG, Kessler MJ (1986) The history of the Cayo Santiago colony. In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques: history, behavior and biology. State University of New York Press, Albany, NY, pp 13–46Google Scholar
  36. Richtsmeier JT, Aldridge K, DeLeon VB, Panchal J, Kane AA, Marsh JL, Yan P, Cole TM III (2006) Phenotypic integration of neurocranium and brain. J Exp Zool (Mol Dev Evol) 306B:360–378CrossRefGoogle Scholar
  37. Roff DA (1995) The estimation of genetic correlations from phenotypic correlations: a test of Cheverud’s conjecture. Heredity 74:481–490CrossRefGoogle Scholar
  38. Rogers J, Kochunov P, Lancaster J, Shelledy W, Glahn D, Blangero J, Fox P (2007) Heritability of brain volume, surface area and shape: an MRI study in an extended pedigree of baboons. Hum Brain Mapp 28:576–583PubMedCrossRefGoogle Scholar
  39. Ross C (1996) Adaptive explanation for the origins of Anthropoidea (Primates). Am J Primatol 40:205–230CrossRefGoogle Scholar
  40. Schumacher GH (1997) Principles of skeletal growth. In: Dixon AD, Hoyte DAN, Ronning O (eds) Fundamentals of craniofacial growth. CRC Press LLC, Boca Raton, FL, pp 1–22Google Scholar
  41. Steiper ME, Young NM (2006) Primate molecular divergence dates. Mol Phylogenet Evol 41:384–394PubMedCrossRefGoogle Scholar
  42. Stephan H, Baron G, Frahm HD (1988) Comparative size of brain and brain components. In: Steklis HD, Erwin J (eds) Comparative primate biology, vol 4, Neurosciences. Alan R. Liss, New York, pp 1–38Google Scholar
  43. Taylor AB, van Schaik CP (2007) Variation in brain size and ecology in Pongo. J Hum Evol 52:59–71PubMedCrossRefGoogle Scholar
  44. Wagner GP, Altenberg L (1996) Complex adaptations and the evolution of evolvability. Evolution 50:967–976CrossRefGoogle Scholar
  45. Xing J, Wang H, Han K, Ray DA, Huang CH, Chemnick LG, Stewart C, Disotell TR, Ryder OA, Batzer MA (2005) A mobile element based phylogeny of Old World monkeys. Mol Phylogenet Evol 37:872–880PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Jessica L. Joganic
    • 1
    Email author
  • Katherine E. Willmore
    • 2
  • Charles C. Roseman
    • 3
  • Joan T. Richtsmeier
    • 2
  • Jeffrey Rogers
    • 4
    • 5
  • James M. Cheverud
    • 6
    • 1
  1. 1.Department of AnthropologyWashington UniversitySaint LouisUSA
  2. 2.Department of AnthropologyPennsylvania State UniversityUniversity ParkUSA
  3. 3.Department of AnthropologyUniversity of IllinoisUrbanaUSA
  4. 4.Southwest National Primate Research CenterSan AntonioUSA
  5. 5.Department of Molecular and Human GeneticsHuman Genome Sequencing Center, Baylor College of MedicineHoustonUSA
  6. 6.Department of Anatomy and NeurobiologyWashington UniversitySaint LouisUSA

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