Multivariate Craniodental Allometry of Tarsiers

Abstract

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.

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References

  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.

    Article  PubMed  CAS  Google Scholar 

  4. Bolker, B., Phillips, P. C. (n.d.). Common principal components/back-projections analysis. cpcbp package version 0.3.3.

  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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Burnaby, T. P. (1966). Growth-invariant discrimination functions and generalized distances. Biometrics, 22, 96–110.

    Article  Google 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.

  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.

  10. Cheverud, J. M. (1982). Relationships among ontogenetic, static, and evolutionary allometry. American Journal of Physical Anthropology, 59, 139–149.

    Article  PubMed  CAS  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  PubMed  PubMed Central  CAS  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  PubMed  CAS  Google Scholar 

  21. Gould, S. J. (1975). On the scaling of tooth size in mammals. American Zoologist, 15, 353–362.

    Article  Google Scholar 

  22. Groves, C. (1998). Systematics of tarsiers and lorises. Primates, 39, 13–27.

    Article  Google Scholar 

  23. Groves, C., & Shekelle, M. (2010). The genera and species of Tarsiidae. International Journal of Primatology, 31, 1071–1082.

    Article  Google 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.

    Article  Google Scholar 

  26. Hennig, C. (2015). Package ‘fpc’.

  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.

    Article  PubMed  Google 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.

    Article  Google 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.

    Article  Google 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.

    Google Scholar 

  32. Klingenberg, C. P. (2016). Size, shape, and form: Concepts of allometry in geometric morphometrics. Development Genes and Evolution, 226, 113–137.

    Article  PubMed  PubMed Central  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  PubMed Central  Google 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.

    Article  PubMed  CAS  Google 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.

  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.

    Article  Google Scholar 

  43. Paradis, E. (2010). pegas: An R package for population genetics with an integrated-modular approach. Bioinformatics, 26, 419–420.

    Article  PubMed  CAS  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  CAS  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  PubMed  Google 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.

    Article  PubMed  PubMed Central  CAS  Google 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.

    Article  Google Scholar 

  52. Schluter, D. (1996). Adaptive radiation along genetic lines of least resistance. Evolution, 50(5), 1766–1774.

    Article  PubMed  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  PubMed  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  PubMed  CAS  Google Scholar 

  62. Wilson, L. A. B. (2013). Allometric disparity in rodent evolution. Ecology and Evolution, 3(4), 971–984.

    Article  PubMed  PubMed Central  Google 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.

    Article  PubMed  Google 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.

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Acknowledgments

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.

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Correspondence to Rachel A. Munds.

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Munds, R.A., Dunn, R.H. & Blomquist, G.E. Multivariate Craniodental Allometry of Tarsiers. Int J Primatol 39, 252–268 (2018). https://doi.org/10.1007/s10764-018-0034-x

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Keywords

  • Carlito
  • Cephalopachus
  • Evolutionary allometry
  • Miocene
  • Tarsius