International Journal of Primatology

, Volume 39, Issue 2, pp 252–268 | Cite as

Multivariate Craniodental Allometry of Tarsiers

  • Rachel A. MundsEmail author
  • Rachel H. Dunn
  • Gregory E. Blomquist


Evolutionary allometry describes size and shape differences across taxa matched for developmental stage (e.g., adulthood). Allometric studies can identify subtle differences among species, and therefore help researchers interested in small-bodied, cryptic species such as tarsiers. Recent taxonomic revision has emphasized size differences among three possible tarsier genera inhabiting different island regions: Sulawesi (genus: Tarsius), Borneo (genus: Cephalopachus), and the Philippines (genus: Carlito). We examined seven craniodental measures of 102 museum specimens of adult tarsiers representing these three regions. We found that the allometric patterns within groups do not predict the observable differences among groups. Crania of the largest-bodied genus, Cephalopachus, are characterized by relatively short skulls and small orbits, with wider palates and molars than predicted by allometric increase from the smaller-bodied Tarsius. Overall, we found tarsier skulls stay the same shape as they increase in size. This may reflect shared developmental and biomechanical adaptations across tarsier groups filling an extreme leaping, faunivorous niche with hypertrophied orbits and subtle dietary differences in prey selection. These shared adaptations of tarsiers may severely limit the range of body sizes in tarsiers and impose further constraints on cranial shape. Despite their deep divergence times in the Miocene, living tarsier groups are united by a common craniodental form across a limited size range. Adaptations to extreme niches might result in a hyperconservatism of the cranium. Future primate allometric studies should explore cranial variation in other taxa to determine how adaptations to specific niches affect the size and shape of the cranium.


Carlito Cephalopachus Evolutionary allometry Miocene Tarsius 



We thank R. Thorington and L. Gordon (National Museum of Natural History) for allowing us to access the collections. We also want to thank Dr. Yao for providing the photograph of the tarsier skulls, as well as E. Westig and N. Duncan (American Museum of Natural History) for granting permission for us to use this photograph. Thank you Dr. M. Shekelle for your advice and feedback, as well as your willingness to share your data. We thank the editor of International Journal of Primatology, as well as several anonymous reviewers who provided excellent suggestions for the improvement of this article. Finally, this research would not have been accomplished if it were not for the late Dr. C. Groves, who provided not only his data but also his expertise on the subject.


  1. Anemone, R. L., & Nachman, B. A. (2003). Morphometrics, functional anatomy, and the biomechanics of locomotion among tarsiers. In P. C. Wright, E. L. Simons, & S. Gursky (Eds.), Tarsiers: Past, present and future (pp. 97–120). New Brunswick: Rutgers University Press.Google Scholar
  2. Beard, K. C. (1998). A new genus of Tarsiidae (Mammalia: Primates) from the Middle Eocene of Shanxi Province, China, with notes on the historical biogeography of tarsiers. Bulletin of Carnegie Museum of Natural History, 34, 260–277.Google Scholar
  3. Beard, K. C., Qi, T., Dawson, M. R., Wang, B., & Li, C. K. (1994). A diverse new primate fauna from middle Eocene fissure-fillings in southeaster China. Nature, 368, 604–609.CrossRefPubMedGoogle Scholar
  4. Bolker, B., Phillips, P. C. (n.d.). Common principal components/back-projections analysis. cpcbp package version 0.3.3.Google Scholar
  5. Brandon-Jones, D. (1998). Pre-glacial Bornean primate impoverishment and Wallace’s line. In R. Hall & J. D. Holloway (Eds.), Biogeography and geological evolution of SE Asia (pp. 393–404). Leiden: Backhuys.Google Scholar
  6. Brown, R. M., Weghorst, J. A., Olson, K. V., Duya, M. R. M., Barley, A. J., et al (2014). Conservation genetics of the Philippine tarsier: Cryptic genetic variation restructures conservation priorities for an island archipelago primate. PLoS One, 9(8), e104340.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Burnaby, T. P. (1966). Growth-invariant discrimination functions and generalized distances. Biometrics, 22, 96–110.CrossRefGoogle Scholar
  8. Chaimanee, Y., Chavasseau, O., Beard, K. C., Kyaw, A. A., Soe, A. N., et al. (2012). Late Middle Eocene primates from the Myanmar and the initial anthropoid colonization of Africa. Proceedings of the National Academy of Sciences of the USA, 109, 10293–10297.Google Scholar
  9. Chaimanee, Y., Lebrun, R., Yamee, C., Jaeger, J. J. (2011). A new Middle Miocene tarsier from Thailand and the reconstruction of its orbital morphology using a geometric-morphometric method. Proceedings of the Royal Society of London B: Biological Sciences, rspb20102062.Google Scholar
  10. Cheverud, J. M. (1982). Relationships among ontogenetic, static, and evolutionary allometry. American Journal of Physical Anthropology, 59, 139–149.CrossRefPubMedGoogle Scholar
  11. Cheverud, J. M., & Marroig, G. (2007). Comparing covariance matrices: Random skewers method compared to the common principal components model. Genetics and Molecular Biology, 30(2), 461–469.CrossRefGoogle Scholar
  12. Crompton, R. H., & Andau, P. M. (1987). Ranging, activity rhythms, and sociality in free-ranging Tarsius bancanus: A preliminary report. International Journal of Primatology, 8(1), 43–71.CrossRefGoogle Scholar
  13. Dagosto, M., Gebo, D. L., & Dolino, C. N. (2003). The natural history of the Philippine tarsier (Tarsius syrichta). In P. C. Wright, E. L. Simons, & S. Gursky (Eds.), Tarsiers: Past, present and future (pp. 237–259). New Brunswick: Rutgers University Press.Google Scholar
  14. Driller, C., Merker, S., Perwitasari-Farajallah, D., Sinaga, W., Anggraeni, N., & Zischler, H. (2015). Stop and go-waves of tarsier dispersal mirror the genesis of Sulawesi island. PLoS One, 10(11), e0141212.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Evans, A. R., & Sanson, G. D. (1998). The effect of tooth shape on the breakdown of insects. Journal of Zoology London, 246, 391–400.CrossRefGoogle Scholar
  16. Fleagle, J. G. (1985). Size and adaptations in primates. In W. L. Jungers (Ed.), Size and scaling in primate biology (pp. 1–19). New York: Plenum Press.Google Scholar
  17. Flury, B. (1988). Common principal components and related multivariate models. New York: John Wiley & Sons.Google Scholar
  18. Ford, S. M. (1980). Callitrichids as phyletic dwarfs, and the place of the Callitrichidae in Platyrrhini. Primates, 21, 31–43.CrossRefGoogle Scholar
  19. Gelman, A., & Weakliem, D. (2009). Of beauty, sex and power: Too little attention has been paid to the statistical challenges in estimating small effects. American Scientist, 97, 310–316.CrossRefGoogle Scholar
  20. Gingerich, P. D., Smith, B. H., & Rosenberg, K. (1982). Allometric scaling in the dentition of primates and prediction of body weight from tooth size in fossils. American Journal of Physical Anthropology, 58, 81–100.CrossRefPubMedGoogle Scholar
  21. Gould, S. J. (1975). On the scaling of tooth size in mammals. American Zoologist, 15, 353–362.CrossRefGoogle Scholar
  22. Groves, C. (1998). Systematics of tarsiers and lorises. Primates, 39, 13–27.CrossRefGoogle Scholar
  23. Groves, C., & Shekelle, M. (2010). The genera and species of Tarsiidae. International Journal of Primatology, 31, 1071–1082.CrossRefGoogle Scholar
  24. Gursky, S. (2007). Tarsiiformes. In C. Campbell, A. Fuentes, K. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 73–85). Oxford: Oxford University Press.Google Scholar
  25. Hadfield, J. D. (2010). MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package. Journal of Statistical Software, 33(2), 1–22.CrossRefGoogle Scholar
  26. Hennig, C. (2015). Package ‘fpc’.Google Scholar
  27. Howland, H. C., Merola, S., & Basarab, J. B. (2004). The allometry and scaling of the size of vertebrate eyes. Vision Research, 44(17), 2043–2065.CrossRefPubMedGoogle Scholar
  28. Jablonski, N. G. (2003). The evolution of the Tarsiid niche. In P. C. Wright, E. L. Simons, & S. Gursky (Eds.), Tarsiers: Past, present and future (pp. 35–49). New Brunswick: Rutgers University Press.Google Scholar
  29. Jablonski, N. G., & Crompton, R. H. (1994). Feeding behavior, mastication, and tooth wear in the Western tarsier (Tarsius bancanus). International Journal of Primatology, 5(1), 29–59.CrossRefGoogle Scholar
  30. Jungers, W. L., Falsetti, A. B., & Wall, C. E. (1995). Shape, relative size, and size-adjustments in morphometrics. Yearbook of Physical Anthropology, 38, 137–161.CrossRefGoogle Scholar
  31. Klingenberg, C. P. (1996). Multivariate allometry. In L. F. Marcus, M. Corti, A. Loy, G. J. P. Naylor, & D. E. Slice (Eds.), Advances in morphometrics (pp. 23–49). New York: Springer-Verlag.CrossRefGoogle Scholar
  32. Klingenberg, C. P. (2016). Size, shape, and form: Concepts of allometry in geometric morphometrics. Development Genes and Evolution, 226, 113–137.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Leigh, S. R., Shah, N. F., & Buchanan, L. S. (2003). Ontogeny and phylogeny in papionin primates. Journal of Human Evolution, 45, 285–316.CrossRefPubMedGoogle Scholar
  34. Marroig, G., & Cheverud, J. M. (2009). Size and shape in callimico and marmoset skulls: allometry and heterochrony in the morphological evolution of small anthropoids. In S. M. Ford, L. M. Porter, & L. C. Davis (Eds.), The marmoset/callimico radiation (pp. 331–354). New York: Springer Science+Business Media.Google Scholar
  35. McCoy, M. W., Bolker, B. M., Osenberg, C. W., Miner, B. G., & Vonesh, J. R. (2006). Size correction: Comparing morphological traits among populations and environments. Oecologia, 148, 547–554.CrossRefPubMedGoogle Scholar
  36. Merker, S., Driller, C., Perwitasari-Farajallah, D., Pamungkas, J., & Zischler, H. (2009). Elucidating geological and biological processes underlying the diversification of Sulawesi tarsiers. Proceedings of the National Academy of Sciences of the USA, 106, 8459–8464.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Merker, S., Thomas, S., Volker, E., Perwitasari-Farajallah, D., Feldmeyer, B., et al (2014). Control region length dynamics potentially drives amino acid evolution in tarsier mitochondrial genomes. Journal of Molecular Evolution, 79(1–2), 40–51.CrossRefPubMedGoogle Scholar
  38. Mitteroecker, P., Gunz, P., Windhager, S., & Schaefer, K. (2013). A brief review of shape, form, and allometry in geometric morphometrics, with applications to human facial morphology. Hystrix, 24, 59–66.Google Scholar
  39. Musser, G. G., & Dagosto, M. (1987). The identity of Tarsius pumilus, a pygmy species endemic to the montane mossy forests of central Sulawesi. American Museum Novitates, 2867, 1–53.Google Scholar
  40. Niemitz, C. (1984). The biology of tarsiers. New York: Gustav Fischer Verlag.Google Scholar
  41. Nietsch, A. (1993). Beitrage zur Biologie von Tarsius spectrum in Sulawesis-Zur morphometric, Entwicklung sowie zum Verhalten unter halbfreien und unter Freilandbedingungne. PhD thesis, Free University of Berlin.Google Scholar
  42. Ovaskainen, O., Cano, J. M., & Merilä, J. (2008). A Bayesian framework for comparative quantitative genetics. Proceedings of the Royal Society of London B: Biological Sciences, 275, 669–678.CrossRefGoogle Scholar
  43. Paradis, E. (2010). pegas: An R package for population genetics with an integrated-modular approach. Bioinformatics, 26, 419–420.CrossRefPubMedGoogle Scholar
  44. Phillips, P. C., & Arnold, S. J. (1999). Hierarchical comparison of genetics variance-covariance matrices. I. Using the Flury hierarchy. Evolution, 53(5), 1506–1515.CrossRefPubMedGoogle Scholar
  45. R Development Core Team (2013). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  46. Roff, D. A., Prokkola, J. M., Krams, I., & Rantala, M. J. (2012). There is more than one way to skin a G matrix. Journal of Evolutionary Biology, 25(6), 1113–1126.CrossRefPubMedGoogle Scholar
  47. Rosenberger, A. L. (2010). The skull of Tarsius: Functional morphology, eyeballs, and the nonpursuit of predatory lifestyle. International Journal of Primatology, 31, 1031–1054.CrossRefGoogle Scholar
  48. Rosenberger, A. L., & Preuschoft, H. (2012). Evolutionary morphology, cranial biomechanics and the origins of tarsiers and anthropoids. Palaeobiodiversity and Palaeoenvironments, 92(4), 507–525.CrossRefGoogle Scholar
  49. Rosenberger, A. L., Smith, T. D., DeLeon, V. B., Burrows, A. M., Schenck, R., & Halenar, L. B. (2016). Eye size and set in small-bodied fossil primates: A three-dimensional method. The Anatomical Record, 299, 1671–1689.CrossRefPubMedGoogle Scholar
  50. Rossie, J. B., Xijun, N., & Beard, K. C. (2006). Cranial remains of an Eocene tarsier. Proceedings of the National Academy of Sciences of the USA, 103(12), 4381–4385.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Rychlik, L., Ramalhinho, G., & Polly, P. D. (2006). Response to environmental factors and competition: Skull, mandible and tooth shapes in Polish water shrews (Neomys, Soricidae, Mammalia). Journal of Zoological Systematics and Evolutionary Research, 44(4), 339–351.CrossRefGoogle Scholar
  52. Schluter, D. (1996). Adaptive radiation along genetic lines of least resistance. Evolution, 50(5), 1766–1774.CrossRefPubMedGoogle Scholar
  53. Sebastiao, H., & Marroig, G. (2013). Size and shape in cranial evolution of 2 marsupial genera: Didelphis and Philander (Didelphimorphia, Didelphidae). Journal of Mammalogy, 94(6), 1424–1437.CrossRefGoogle Scholar
  54. Shekelle, M., Groves, C., Gursky, S., Neri-Arboleda, I., & Nietsch, A. (2008). A method for multivariate analysis and classification of tarsier tail tufts. In M. Shekelle, I. Maryanto, C. P. Groves, H. Schulze & H. Fitch-Snyder (Eds.), Primates of the oriental night (pp. 71–84). Cibinong: Indonesian Institute of Sciences.Google Scholar
  55. Shekelle, M., Meier, R., Wahyu, W. I., & Ting, N. (2010). Molecular phylogenetics and chronometrics of Tarsiidae based on 12S mtDNA haplotypes: Evidence for Miocene origins of crown tarsiers and numerous species within the Sulawesian Clade. International Journal of Primatology, 31, 1083–1106.CrossRefGoogle Scholar
  56. Simons, E. L. (2003). The evolution of the Tarsiid niche. In P. C. Wright, E. L. Simons, & S. Gursky (Eds.), Tarsiers: Past, present and future (pp. 9–34). New Brunswick: Rutgers University Press.Google Scholar
  57. Singleton, M. (2002). Patterns of cranial shape variation in the Papionini (Primates: Cercopithecinae). Journal of Human Evolution, 42(5), 547–578.CrossRefPubMedGoogle Scholar
  58. Strait, S. G. (1993). Differences in occlusal morphology and molar size in frugivores and faunivores. Journal of Human Evolution, 25(6), 471–484.CrossRefGoogle Scholar
  59. Vinyard, C. J., Wall, C. E., Williams, S. H., Mork, A. L., Armfield, B. A., et al (2009). The evolutionary morphology of tree gouging in marmosets. In S. M. Ford, L. M. Porter, & L. C. Davis (Eds.), The marmoset/callimico radiation (pp. 395–409). New York: Springer Science+Business Media.Google Scholar
  60. Ward Jr., J. H. (1963). Hierarchical grouping to optimize an objective function. Journal of the American Statistical Association, 58(301), 236–244.CrossRefGoogle Scholar
  61. West, G. B., Brown, J. H., & Enquist, B. J. (1997). A general model for the origin of allometric scaling laws in biology. Science, 276, 122–126.CrossRefPubMedGoogle Scholar
  62. Wilson, L. A. B. (2013). Allometric disparity in rodent evolution. Ecology and Evolution, 3(4), 971–984.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Zelditch, M. L., Lundrigan, B. L., & Garland, T. (2004). Developmental regulation of skull morphology. I. Ontogenetic dynamics of variance. Evolution & Development, 6(3), 194–206.Google Scholar
  64. Zijlstra, J. S., Lawerence, J. F., & Wessels, W. (2013). The westernmost tarsier: A new genus and species from the Miocene of Pakistan. Journal of Human Evolution, 65, 544–550.CrossRefPubMedGoogle Scholar
  65. Ziyatdinov, A., Kanaan-Izquierdo, S., Trendafilov, N. T., Perera-Lluna, A. (2014). cpca: Methods to perform common principal component analysis (CPCA). R package version 0.1.2.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Rachel A. Munds
    • 1
    • 2
    Email author
  • Rachel H. Dunn
    • 3
  • Gregory E. Blomquist
    • 1
  1. 1.Department of AnthropologyUniversity of MissouriColumbiaUSA
  2. 2.Nocturnal Primate Research GroupOxford Brookes UniversityOxfordUK
  3. 3.Department of AnatomyDes Moines UniversityDes MoinesUSA

Personalised recommendations