Palaeobiodiversity and Palaeoenvironments

, Volume 92, Issue 4, pp 507–525 | Cite as

Evolutionary morphology, cranial biomechanics and the origins of tarsiers and anthropoids

Original Paper

Abstract

During the Time of Messel, the dominant groups of primates were the adapiform strepsirhines and the tarsiiform haplorhines, both important in discussions of anthropoid origins. Living tarsiers are at the centre of these ideas as one school of thought, representing the Tarsier-Anthropoid Hypothesis, holds they are the sister-group of Anthropoidea. The Tarsier-Tarsiiform Hypothesis, however, maintains that tarsiers are phyletically nested among the (paraphyletic) fossil tarsiiforms (∼omomyids). Orbital morphology is crucial to this debate: the possibility that the postorbital septa of tarsiers and anthropoids are synapomorphic and that it evolved in their last common ancestor to insulate the eyeballs from muscular interference. Our biomechanical model of forces acting on the enormous eyeballs and orbits of tarsiers especially during locomotion provides a strong counterargument to this proposition. The uniquely specialised orbita of Tarsius, which include prominent circumorbital flanges that are continuous with the postorbital septum, are designed to sustain enormous inertial loads transmitted by the eyeballs during the acceleration and deceleration phases of powerful leaping, for which Tarsius is also famous. The eyeballs are thus secured, and pressure absorbed by the retina during acceleration is minimised, by enlarging its surface area of contact with a “walled socket”, i.e., by the extra-fossa expansion of these flanges. The tarsier septum is, therefore, a form–function convergence on the small-eyed anthropoid condition. Several related Eocene tarsiiforms exhibit a precisely Tarsius-like morphology of the rostrum relating to eyeball hypertrophy, although they lack the exaggerated circumorbital and septal morphology and only rarely exhibit postcranial features indicative of super leaping abilities.

Keywords

Tarsiers Anthropoids Biomechanics Postorbital septum Phylogeny Adaptation 

References

  1. Anemone RL, Covert HH (2000) New skeletal remains of Omomys (Primates, Omomyidae): functional morphology of the hindlimb and locomotor behavior of a Middle Eocene primate. J Hum Evol 38:607–633CrossRefGoogle Scholar
  2. Bajpai S, Kay RF, Williams BA, Das DP, Kapur VV, Tiwari NB (2008) The oldest Asian record of Anthropoidea. Proc Natl Acad Sci USA 105:11093–11098CrossRefGoogle Scholar
  3. Beard KC, MacPhee RDE (1994) Cranial anatomy of Shoshonius and the antiquity of Anthropoidea. In: Fleagle JG, Kay RF (eds) Anthropoid origins. Plenum Press, New York, pp 55–97Google Scholar
  4. Beard KC, Krishtalka L, Stucky RK (1991) First skulls of the early Eocene primate Shoshonius cooperi and the anthropoid-tarsier dichotomy. Nature 349:64–67CrossRefGoogle Scholar
  5. Bock WJ (1990) From biologische Anatomie to ecomorphology. Neth J Zool 40:254–277CrossRefGoogle Scholar
  6. Burger BJ (2010) Skull of the Eocene primate Omomys carteri from western North America. Paleon Contrib 2, paleo.ku.edu/contributions. http://hdl.handle.net/1808/6360
  7. Burmeister H (1846) Beiträge zur näheren Kenntniss der Gattung Tarsius. George Reimer, BerlinGoogle Scholar
  8. Cartmill M (1980) Morphology, function, and evolution of the anthropoid postorbital septum. In: Ciochon RL, Chiarelli AB (eds) Evolutionary biology of the New World monkeys and continental drift. Plenum Press, New York, pp 243–274Google Scholar
  9. Cartmill M (1994) Anatomy, antinomies, and the problem of anthropoid origins. In: Fleagle JG, Kay RF (eds) Anthropoid origins. Plenum Press, New York, pp 549–566Google Scholar
  10. Cartmill M, Kay RF (1978) Craniodental morphology, tarsier affinities, and primate suborders. In: Chivers DJ, Joysey KA (eds) Recent advances in primatology. Academic Press, London, pp 205–214Google Scholar
  11. Cartmill M, MacPhee RDE, Simons EL (1981) Anatomy of the temporal bone in early anthropoids, with remarks on the problem of anthropoid origins. Am J Phys Anthropol 56:1–21CrossRefGoogle Scholar
  12. Castenholtz E (1984) The eye of Tarsius. In: Niemitz C (ed) Biology of tarsiers. Gustav Fischer, Stuttgart, pp 303–318Google Scholar
  13. 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. Proc R Soc Lond B 278:1956–1963CrossRefGoogle Scholar
  14. Cope ED (1882) An anthropomorphous lemur. Am Nat 16:73–74Google Scholar
  15. Cummings JR, Muchlinski MN, Kirk EC, Rehorek SJ, DeLeon VB et al (2012) Eye size at birth in prosimian primates: life history correlates and growth patterns. PLoS One 7(5):e36097CrossRefGoogle Scholar
  16. Curtis N, Witzel U, Fitton L, O’Higgins P, Fagan M (2011) The mechanical significance of the temporal fascia in Macaca fascicularis: An investigation using finite Element Analysis. Anat Rec 294:1178–1190CrossRefGoogle Scholar
  17. Dagosto M (1993) Postcranial anatomy and locomotor behavior in Eocene primates. In: Gebo DL (ed) Postcranial adaptation in nonhuman primates. Northern Illinois University Press, DeKalb, pp 199–219Google Scholar
  18. Dagosto M, Gebo DL (1994) Postcranial anatomy and the origin of the Anthropoidea. In: Fleagle JG, Kay RF (eds) Anthropoid origins. Plenum Press, New York, pp 567–593Google Scholar
  19. Dagosto M, Gebo DL, Beard KC (1999) Revision of the Wind River faunas, early Eocene of central Wyoming. Part 14. Postcranium of Shoshonius cooperi (Mammalia: Primates). Ann Carnegie Mus 68:175–211Google Scholar
  20. Demes B, Günther MM (1989a) Biometrics and allometric scaling in primate locomotion and morphology. Folia Primatol 53:125–141CrossRefGoogle Scholar
  21. Demes B, Günther MM (1989b) Wie die Körpermasse den Springstil von Halbaffen und deren Proportionen bestimmt. Z Morph Anthropol 77:209–225Google Scholar
  22. Fleagle JG (1999) Primate adaptation and evolution, 2nd edn. Academic Press, New YorkGoogle Scholar
  23. Franzen JL, Gingerich PD, Habersetzer J, Hurum JH, von Koenigswald W, Smith BH (2009) Complete primate skeleton from the middle Eocene of Messel in Germany: morphology and paleobiology. PLoS One 4(e5723):1e27Google Scholar
  24. Gebo DL (1998) Foot morphology and locomotor adaptation in Eocene primates. Folia Primatol 50:3–41CrossRefGoogle Scholar
  25. Gingerich PD, Franzen JL, Habersetzer J (2012) Darwinius masillae is a Haplorhine – Reply to Williams et al. 2010. J Hum Evol 59:574–579CrossRefGoogle Scholar
  26. Ginsburg L, Mein P (1987) Tarsius thailandica nov. sp., premier Tarsiidae (Primates, Mammalia) fossile d’Asie. CR Acad Sci 304:1213–1215Google Scholar
  27. Godinot M, Dagosto M (1983) The astragalus of Necrolemur (Primates, Microchoerinae). J Paleontol 57:1321–1324Google Scholar
  28. Grand TI, Lorenz R (1968) Functional analysis of thre hip joint in Tarsius bancanus (Horesfield, 1821) and Tarsius syrichta (Linnaeus, 1758). Folia Primatol 9:161–181CrossRefGoogle Scholar
  29. Grassé P-P (1968) Traité de zoologie, anatomie, systématique, biologie. Tome XVI, Fascicule 2: Mammifères. Musculature. Masson, ParisGoogle Scholar
  30. Groves C, Shekelle M (2010) The genera and species of Tarsiidae. Int J Primatol 31:1071–1082CrossRefGoogle Scholar
  31. Gunnell G, Rose KD (2002) Tarsiiformes: evolutionary history and adaptation. In: Hartwig WC (ed) The primate fossil record. Cambridge University Press, Cambridge, pp 45–82Google Scholar
  32. Günther M-M (1989) Funktionsmorphologische Untersuchungen zum Sprungverhalten an mehreren Halbaffenarten. Dissertation, Freie Universität BerlinGoogle Scholar
  33. Günther MM, Preuschoft H, Ishida H, Nakano Y (1992) Can prosimian-like leaping be considered a preadaptation to bipedal walking in hominids? In: Matano S, Tuttle RH, Ishida H, Goodman M (eds) Topics in primatology, Vol, 3 Evolutionary Biology, Reproductive Endocrinology and Virology. University of Tokyo Press, Tokyo, pp 153–165Google Scholar
  34. Gursky SL (2007) The spectral tarsier. Pearson-Prentice Hall, Upper Saddle RiverGoogle Scholar
  35. Gursky-Doyen S (2010) The Tarsiidae. In: Bearder S, Campbell C, Fuentes A, MacKinnon K, Panger M (eds) Primates in perspective, 2nd edn. Oxford University Press, Oxford, pp 79–90Google Scholar
  36. Haubold H, Hellmund M (1998) Das Geiseltalmuseum am Institut für Geologische Wissenschaften. Veröffentlichungen der Akad Sgl und Mus der Martin-Luther Univ Halle-Wittenberg, pp 1–39Google Scholar
  37. Heesy CP, Ross CF (2001) Evolution of activity patterns and chromatic vision in primates: morphometrics, genetics and cladistics. J Hum Evol 40:111–149CrossRefGoogle Scholar
  38. Heesy CP, Ross CF, Demes B (2007) Oculomotor stability and the functions of the postorbital bar and septum. In: Ravosa MJ, Dagosto M (eds) Primate origins: adaptations and evolution. Springer, New York, pp 357–283Google Scholar
  39. Hershkovitz P (1977) Living New World Monkeys (Platyrrhini) with an Introduction to Primates, vol 1. University of Chicago Press, ChicagoGoogle Scholar
  40. Hill WCO (1955) Primates: Comparative Anatomy and Taxonomy. II. Haplorhini: Tarsioidea. A Monograph. Edinburgh University Press, EdinburghGoogle Scholar
  41. Hubrecht AAW (1897) The descent of the primates. Charles Scribner, New YorkGoogle Scholar
  42. Jeffery N, Davies K, Kockenberger W, Williams S (2007) Craniofacial growth in fetal Tarsius bancanus: brains, eyes and nasal septa. J Anat 210:703–722CrossRefGoogle Scholar
  43. Kay RF, Kirk EC (2000) Osteological evidence for the evolution of activity pattern and visual acuity in primates. Am J Phys Anthropol 113:235–262CrossRefGoogle Scholar
  44. Kay RF, Ross CF, Williams BA (1997) Rethinking anthropoid origins. Science 275:797–804CrossRefGoogle Scholar
  45. Kirk EC (2006) Eye morphology in cathemeral lemurids and other mammals. Folia Primatol 77:27–49CrossRefGoogle Scholar
  46. Le Gros Clark WE (1934) Early forerunners of man. Bailliere, Tindall and Cox, LondonGoogle Scholar
  47. Le Gros Clark WE (1959) The antecedents of man. University of Edinburgh Press, EdinburghGoogle Scholar
  48. MacPhee RDE, Cartmill M (1986) Basicranial structures and primate systematics. In: Swindler DR, Erwin J (eds) Comparative primate biology, volume 1: systematics, evolution, and anatomy. Alan R Liss, New York, pp 219–275Google Scholar
  49. Maiolino S, Boyer DM, Bloch JI, Gilbert CC, Groenke J (2012) Evidence for a grooming claw in a North American adapiform primate: Implications for Anthropoid Origins. PLoS One 7(1):e29135. doi:10.1371/journal.pone.0029135 CrossRefGoogle Scholar
  50. Marivaux L, Pierre-Olivier A, Baqri SRH, Benammi M, Chaimanee Y, Crochet J-Y, de Franceschi D, Iqbal N, Jaeger J-J, Métais G, Roohi G, Welcomme J-L (2005) Anthropoid primates from the Oligocene of Pakistan (Bugti Hills): Data on early anthropoid evolution and biogeography. Proc Natl Acad Sci USA 102:8436–8441CrossRefGoogle Scholar
  51. Martin RD (1990) Primate origins and evolution: a phylogenetic reconstruction. Chapman and Hall, LondonGoogle Scholar
  52. Merker S, Groves C (2010) Tarsius lariang: A new primate species from Western Central Sulawesi. Int J Primatol 27:265–485Google Scholar
  53. Musser GG, Dagosto M (1987) The identity of Tarsius pumilus, a pygmy species endemic to the montane mossy forests of central Sulawesi. Am Mus Nov 2867:1–53Google Scholar
  54. Napier JR, Napier PH (1967) A Handbook of living primates. Morphology, ecology and behaviour of nonhuman primates. Academic Press, LondonGoogle Scholar
  55. Napier JR, Walker A (1968) Vertical clinging and leaping – a newly recognized category of locomotor behavuour of primates. Folia Primatol 6:204–219CrossRefGoogle Scholar
  56. Niemitz C (1977) Zur Funktionsmorphologie und Biometrie der Gattung Tarsius, Storr, 1780 (Mammalia, Primates, Tarsiidae). Cour Forsch-Inst Senckenberg 25:1–161Google Scholar
  57. Niemitz C (1979) Relationships among anatomy, ecology and behavior: A model developed in the genus Tarsius with thoughts about phylogenetic mechanisms and adaptive interactions. In: Morbeck ME, Preuschoft H, Gomberg N (eds) Environment, behavior and morphology: dynamic interactions in primates. Gustav Fischer, New York, pp 119–137Google Scholar
  58. Niemitz C (1984a) Biology of tarsiers. Gustav Fischer, StuttgartGoogle Scholar
  59. Niemitz C (1984b) Locomotion and posture of Tarsius bancanus. In: Niemitz C (ed) Biology of tarsiers. Gustav Fischer, New York, pp 191–225Google Scholar
  60. Niemitz C (2010) Progreditur ordinara saltando et retrorsum…Normally proceeds in a leaping fashion, and backwards…. Int J Primatol 31:941–957CrossRefGoogle Scholar
  61. Peters A, Preuschoft H (1984) External biomechanics of leaping in Tarsius and its morphological and kinematic consequences. In: Niemitz C (ed) Biology of tarsiers. Gustav Fischer, New York, pp 227–255Google Scholar
  62. Preuschoft H, Witzel U (2004) A biomechanical approach to craniofacial shape in primates using FESA. Ann Anat 186:397–404CrossRefGoogle Scholar
  63. Preuschoft H, Witzel U (2005) Functional shape of the skull in vertebrates: Which forces determine skull morphology in lower primates and ancestral synapsids? Anat Rec 283A:402–413CrossRefGoogle Scholar
  64. Radinsky LB (1967) The oldest primate endocast. Am J Phys Anthropol 27:385–388CrossRefGoogle Scholar
  65. Roberts M, Kohn F (1993) Habitat use, foraging behavior and activity patterns in reproducing western tarsiers, Tarsius bancanus, in captivity: a management synthesis. Zoo Biol 12:217–232CrossRefGoogle Scholar
  66. Rose KD, Rana RS, Sahni A, Kumar K, Missiaen O, Singh L, Smith T (2009) Early Eocene primates from Gujarat, India. J Human Evol 56:366–404CrossRefGoogle Scholar
  67. Rosenberger AL (1985) In favor of the Necrolemur-Tarsius hypothesis. Folia Primatol 45:179–194CrossRefGoogle Scholar
  68. Rosenberger AL (2010a) Platyrrhines, PAUP, parallelism, and the long lineage hypothesis: a reply to Kay et al. (2008). J Hum Evol 59:214–217Google Scholar
  69. Rosenberger AL (2010b) The skull of Tarsius: functional morphology, eyeballs, and the non-pursuit predatory lifestyle. Int J Primatol 31:1032–1054CrossRefGoogle Scholar
  70. Rosenberger AL (2011a) Evolutionary morphology, platyrrhine evolution and systematics. Anat Rec 294:1955–1974CrossRefGoogle Scholar
  71. Rosenberger AL (2011b) Strigorhysis: another large-eyed Eocene North American fossil tarsiiform. Anat Rec 294:797–812CrossRefGoogle Scholar
  72. Rosenberger AL, Hogg R, Wong SM (2008) Rooneyia, postorbital closure, and the beginnings of the age of Anthropoidea. In: Sargis EJ, Dagosto M (eds) Mammalian evolutionary morphology: a tribute to Frederick S. Szalay. Springer, Dordrecht, pp 325–346CrossRefGoogle Scholar
  73. Ross C (1994) The craniofacial evidence for anthropoid and tarsier relationships. In: Fleagle JG, Kay RF (eds) Anthropoid origins. Plenum Press, New York, pp 469–547Google Scholar
  74. Rossie JB, Ni X, Beard KC (2006) Cranial remains of an Eocene tarsier. PNAS 103:4381–4385CrossRefGoogle Scholar
  75. Schlosser M (1907) Beitrag zur Osteologie und systematischen Stellung der Gattung Necrolemur, sowie zur Stammesgeschichte der Primaten überhaupt. N Jb Mineral Geol Paleontol Festband 197–225Google Scholar
  76. Schmid P (1979) Evidence of microchoerine evolution from Diesldorf (Zürich region, Switzerland): a preliminary report. Folia Primatol 31:301–311CrossRefGoogle Scholar
  77. Schmid P (1982) Die systematische Revision der europischen Microchoeridae Lydekker, 1887 (Omomyiformes Primates). University of Zürich, ZürichGoogle Scholar
  78. Schultz AH (1940) The size of the orbit and of the eye in primates. Am J Phys Anthropol 26:398–408CrossRefGoogle Scholar
  79. Seiffert ER, Simons EL, Clyde WC, Rossie JB, Attia Y, Bown TM, Chatrath P, Mathison ME (2005) Basal anthropoids from Egypt and the antiquity of Africa’s higher primate radiation. Science 310:300–304CrossRefGoogle Scholar
  80. Shekelle M, Gursky-Doyen SL (2010) Building bridges toward a new understanding of Tarsier diversity. Guest Editors. Int J Primatol 31(6):937–1207CrossRefGoogle Scholar
  81. Simons EL (1960) Notes on Eocene tarsioids and a revision of some Necrolemurinae. Bull Br Mus Nat Hist Geol 5:43–70Google Scholar
  82. Simons EL (1963) A critical appraisal of Tertiary primates. In: Buettner-Janusch (ed) Evolutionary and genetic biology of primates. Academic Press, New York, pp 62–129Google Scholar
  83. Simons EL (1972) Primate evolution, an introduction to man’s place in nature. Macmillan, New YorkGoogle Scholar
  84. Simons EL (2003) The fossil record of tarsier evolution. In: Wright PC, Simons EL, Gursky S (eds) Tarsiers: past, present, and future. Rutgers University Press, New Brunswick, pp 9–34Google Scholar
  85. Simons EL, Rasmussen DT (1989) Cranial morphology of Aegyptopithecus and Tarsius and the question of the tarsier-anthropoidean clade. Am J Phys Anthropol 79:1–23CrossRefGoogle Scholar
  86. Simons EL, Russell D (1960) Notes on the cranial anatomy of Necrolemur. Breviora 127:1–14Google Scholar
  87. Spatz WB (1965) Die Bedeutung der Augen für die sagittale Gestaltung des Schädels von Tarsius (Prosimiae, Tarsiiformes). Folia Primatol 9:22–40CrossRefGoogle Scholar
  88. Sprankel H (1965) Untersuchungen an Tarsius. I. Morphologies des Schwanzes nebst ethologischen Bemerkungen. Folia Primatol 3:153–188CrossRefGoogle Scholar
  89. Starck D (1975) The development of the chondrocranium in Primates. In: Luckett WP, Szalay FS (eds) Phylogeny of the primates. Academic Press, New York, pp 127–155CrossRefGoogle Scholar
  90. Stehlin HG (1912) Die Säugetiere des schweizerischen Eocänes, Adapis. Abh Schweiz Paläont Gesell 41:1299–1552Google Scholar
  91. Strassen O (1877) Brehms Thierleben. Allgemeine Kunde des Tierreichs. 4th edition, vol.3 Säugetiere 3. Bibliographisches Institut, LeipzigGoogle Scholar
  92. Szalay FS (1976) Systematics of the Omomyidae (Tarsiiformes, Primates), taxonomy, phylogeny and adaptations. Bull Am Mus Nat Hist 156:157–449Google Scholar
  93. Szalay FS, Delson E (1979) Evolutionary history of the Primates. Academic Press, New YorkGoogle Scholar
  94. Teilhard de Chardin P (1921) Les mammifères de l’éocène inférieur français et leur gisements. Ann Paléont 10:1–114Google Scholar
  95. Thalmann U (1994) Die Primaten aus dem eozänen Geiseltal bei Halle/Saale (Deutschland). Cour Forsch-Inst Senckenberg 175:1–161Google Scholar
  96. Williams BA, Kay RF, Kirk EC, Ross CF (2010) Darwinius masillae is a strepsirhine: a reply to Franzen et al. (2009). J Hum Evol 59:567–573CrossRefGoogle Scholar
  97. Wilson DE, Reeder MD (1993) Mammal species of the world, 2nd edn. Smithosnian Institution Press, WashingtonGoogle Scholar
  98. Witzel U, Preschoft H (2002) Function-dependent shape characteristics of the human skull. Anthrop Anz 2:113–135Google Scholar
  99. Witzel U, Preschoft H (2004) The functional structure of the facial skull in hominoids. Folia Primatol 75:219–252CrossRefGoogle Scholar
  100. Witzel U, Preuschoft H, Sick H (2004) The role of the zygomatic arch in the statics of the skull and its adaptive shape. Folia Primatol 75:202–218CrossRefGoogle Scholar
  101. Wright PC, Simons EL, Gursky SL (2010) Tarsiers. Past, present and future. Rutgers University Press, New BrunswickGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer 2012

Authors and Affiliations

  1. 1.Department of Anthropology and ArchaeologyBrooklyn College, CUNYBrooklynUSA
  2. 2.Department of AnthropologyCity University of New York Graduate CenterNew YorkUSA
  3. 3.Consortium in Evolutionary Primatology (NYCEP)New YorkUSA
  4. 4.Department of MammalogyAmerican Museum of Natural HistoryNew YorkUSA
  5. 5.Formerly Subdepartment of Functional Morphology, Anatomical Institute, Medical FacultyRuhr-UniversitätBochumGermany

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