Advertisement

Journal of Mammalian Evolution

, Volume 23, Issue 4, pp 353–368 | Cite as

Different Level of Intraspecific Variation of the Bony Labyrinth Morphology in Slow- Versus Fast-Moving Primates

  • Alexandre PerierEmail author
  • Renaud Lebrun
  • Laurent MarivauxEmail author
Original Paper

Abstract

The vestibular system of the inner ear detects the motions of the head and is involved in maintaining balance. For this reason, this organ has been deeply studied and several scientists have tried to link its morphology with the locomotor behavior of an animal. Via high-resolution computed microtomography and geometric morphometric methods, we analyzed the intraspecific variation of the 3D morphology of the bony labyrinth (inner ear) in four species of primates differing in their locomotor adaptations: two being slow-moving taxa (Nycticebus and Perodicticus), and two being fast-moving taxa (Callithrix and Microcebus). Basically, there are very few analyses of the inter-individual variation of this organ in mammals in general, and this approach has never been attempted in primates thus far. Our results show that variation of the bony labyrinth morphology is expressed by the same ways in the different species (e.g., differences in the size, shape, and orientation of the semicircular canals, and in the width and height of the cochlea), but that slow-moving taxa exhibit a higher amount of intraspecific variation than do fast-moving taxa. Our results strengthen support for a previously published hypothesis, according to which a relaxation of the selective pressure applied to the morphology of the bony labyrinth is the likely reason for this higher amount of intraspecific variation in slow-moving taxa, and that it may be related to a reduced functional demand for rapid postural adjustments.

Keywords

Inner ear Semicircular canals Intraspecific variation Geometric morphometrics Primates Locomotion 

Notes

Acknowledgments

We thank Jacques Cuisin (Muséum National d’Histoire Naturelle [MNHN], Paris), Robert Asher (University of Cambridge), Christopher Zollikofer and Marcia Ponce de León (Anthropological Institute and Museum, Zürich), Loic Costeur (Naturhistorisches Museum Basel, Basel), Nadine Mestre (Laboratoire Vieillissement Cérébral et Pathogenèse des Maladies Neurodégénératives, Montpellier [Petter-Rousseaux collection]), Peter Giere (Museum für Naturkunde, Berlin), and Suzanne Jiquel (ISE-M) for access to osteological collections; Guillaume Billet (MNHN, Paris) and Lionel Hautier (ISE-M) for discussions on this study; and Julien Claude (ISE-M) and Nathan Young (University of California, San Fransisco) for their advice regarding some statistical analyses. We are also grateful to the staff of beamlines ID19 and ID17 of the European Synchrotron Radiation Facility [ESRF], Grenoble) and especially to Paul Tafforeau. Moreover, we would like to thank Guillaume Billet (MNHN, Paris) and another anonymous reviewer who provided formal reviews of this manuscript that significantly enhanced the quality of the current version. Finally, many thanks to the Montpellier RIO Imaging (MRI) and the LabEx CeMEB for the access to the μCT-scanning station Skyscan 1076 (ISE-M). This research was supported by the French ANR-ERC PALASIAFRICA Program (ANR-08-JCJC-0017) and the Laboratoire de Paléontologie (ISE-M). This is ISE-M publication n° 2016–028 SUD.

Supplementary material

10914_2016_9323_MOESM1_ESM.pdf (151 kb)
ESM 1 (PDF 151 kb)

References

  1. Alloing-Séguier L, Sánchez-Villagra MR, Lee MSY, Lebrun R (2013) The bony labyrinth in diprotodontian marsupial mammals: diversity in extant and extinct forms and relationships with size and phylogeny. J Mammal Evol 20:191-198. doi:  10.1007/s10914-013-9228-3 CrossRefGoogle Scholar
  2. 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 38:607-633. doi:  10.1006/jhev.1999.0371 CrossRefPubMedGoogle Scholar
  3. Arnold SJ (1992) Constraints on phenotypic variation. Am Nat 140:85-107. doi:  10.1086/285398 CrossRefGoogle Scholar
  4. Ashton EH, Oxnard CE (1964) Locomotor patterns in Primates. Proc Zool Soc London B 142:1-28. doi:  10.1111/j.1469-7998.1964.tb05151.x CrossRefGoogle Scholar
  5. Bar-Oz G, Dayan T (2007) FOCUS: on the use of the petrous bone for estimating cranial abundance in fossil assemblages. J Archaeol Sci 34:1356-1360. doi:  10.1016/j.jas.2006.10.021 CrossRefGoogle Scholar
  6. Benoit J, Adnet S, El Mabrouk E, Khayati H, Ben Haj Ali M, Marivaux L, Merzeraud G, Merigeaud S, Vianey-Liaud M, Tabuce R (2013) Cranial remain from Tunisia provides new clues for the origin and evolution of Sirenia (Mammalia, Afrotheria) in Africa. PLoS ONE 8:e54307. doi:  10.1371/journal.pone.0054307 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Benoit J, Lehmann T, Vatter M, Lebrun R, Merigeaud S, Costeur L, Tabuce R (2015) Comparative anatomy and three dimensional geometric-morphometric study of the bony labyrinth of Bibymalagasia (Mammalia, Afrotheria). J Vertebr Paleontol 35:1-14. doi:  10.1080/02724634.2014.930043 CrossRefGoogle Scholar
  8. Berlin JC, Kirk EC, Rowe TB (2013) Functional implications of ubiquitous semicircular canal non-orthogonality in mammals. PLoS ONE 8(11):e79585. doi:  10.1371/journal.pone.0079585 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Biewener AA (1983) Allometry of quadrupedal locomotion: the scaling of duty factor, bone curvature and limb orientation to body size. J Exp Biol 105:147-171PubMedGoogle Scholar
  10. Billet G, Germain D, Ruf I, Muizon C de, Hautier L (2013) The inner ear of Megatherium and the evolution of the vestibular system in sloths. J Anat 223:557-567. doi:  10.1111/joa.12114
  11. Billet G, Hautier L, Asher RJ, Schwarz C, Crumpton N, Martin T, Ruf I (2012) High morphological variation of vestibular system accompanies slow and infrequent locomotion in three-toed sloths. Proc Roy Soc London B 279:3932-3939. doi:  10.1098/rspb.2012.1212 CrossRefGoogle Scholar
  12. Billet G, Hautier L, Lebrun R (2015) Morphological diversity of the bony labyrinth (inner ear) in extant xenarthrans and its relation to phylogeny. J Mammal 96:658-672. doi:  10.1093/jmammal/gyv074
  13. Bookstein FL (1991) Morphometrics Tools for Landmark Data: Geometry and Biology. Cambridge University Press, CambridgeGoogle Scholar
  14. Bookstein FL (1997) Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Med Image Anal 1:225-243. doi:  10.1016/S1361-8415(97)85012-8 CrossRefPubMedGoogle Scholar
  15. Bradshaw AP, Curthoys IS, Todd MJ, Magnussen JS, Taubman DS, Aw ST, Halmagyi GM (2010) A mathematical model of human semicircular canal geometry: a new basis for interpreting vestibular physiology. J Assoc Res Otolaryngol 11(2):145-159. doi:  10.1007/s10162-009-0195-6 CrossRefPubMedGoogle Scholar
  16. Brown JC, Yalden DW (1973) The description of mammals–2 Limbs and locomotion of terrestial mammals. Mammal Rev 3:107-134. doi:  10.1111/j.1365-2907.1973.tb00178.x CrossRefGoogle Scholar
  17. Butynski T, Jong Y de (2007) Distribution of the potto Perodicticus potto (Primates: Lorisidae) in eastern Africa, with a description of a new subspecies from Mount Kenya. J East Afr Nat Hist 96:113-147. doi:  10.2982/0012-8317(2007)96[113:DOTPPP]2.0.CO;2
  18. Curtis DJ (1995) Functional anatomy of the trunk musculature in the slow loris (Nycticebus coucang). Am J Phys Anthropol 97(4):367-379. doi:  10.1002/ajpa.1330970404 CrossRefPubMedGoogle Scholar
  19. Dagosto M (1983) Postcranium of Adapis parisiensis and Leptadapis magnus (Adapiformes, Primates). Folia Primatol 41:49-101. doi:  10.1159/000156119 CrossRefGoogle Scholar
  20. Dagosto M (1988) Implications of postcranial evidence for the origin of Euprimates. J Hum Evol 17:35-56. doi:  10.1016/0047-2484(88)90048-6 CrossRefGoogle Scholar
  21. Dagosto M (1993) Postcranial anatomy and locomotor behavior in Eocene primates. In: Gebo DL (ed) Postcranial Adaptation in Nonhuman Primates. Northern Illinois University Press, De Kalb, pp 199-219Google Scholar
  22. David R, Droulez J, Allain R, Berthoz A, Janvier P, Bennequin D (2010) Motion from the past. A new method to infer vestibular capacities of extinct species. CR Palevol 9:397-410. doi:  10.1016/j.crpv.2010.07.012 CrossRefGoogle Scholar
  23. Doran DM (1993) Comparative locomotor behavior of chimpanzees and bonobos: the influence of morphology on locomotion. Am J Phys Anthropol 91:83-98. doi:  10.1002/ajpa.1330910106 CrossRefPubMedGoogle Scholar
  24. Duarte DPF, Silva VL, Jaguaribe AM, Gilmore DP, Da Costa CP (2003) Circadian rhythms in blood pressure in free-ranging three-toed sloths (Bradypus variegatus). Braz J Med Biol Res 36:273-278. doi:  10.1590/S0100-879X2003000200016 CrossRefPubMedGoogle Scholar
  25. Ekdale EG (2015) Form and function of the mammalian inner ear. J Anat. doi:  10.1111/joa.12308 Google Scholar
  26. Fleagle JG (1977) Locomotor behavior and muscular anatomy of sympatric Malaysian leaf-monkeys (Presbytis obscura and Presbytis melalophos). Am J Phys Anthropol 46:297-307. doi:  10.1002/ajpa.1330460211 CrossRefPubMedGoogle Scholar
  27. Fleagle JG, Meldrum DJ (1988) Locomotor behavior and skeletal morphology of two sympatric pitheciine monkeys, Pithecia pithecia and Chiropotes satanas. Am J Primatol 16:227-249. doi:  10.1002/ajp.1350160305 CrossRefGoogle Scholar
  28. Forbes HO (1894) A Handbook to the Primates, Vol. I. WH Allen, LondonGoogle Scholar
  29. Gebo DL (1987) Locomotor diversity in prosimian primates. Am J Primatol 13:271-281. doi:  10.1002/ajp.1350130305 CrossRefGoogle Scholar
  30. Gebo DL (1988) Foot morphology and locomotor adaptation in Eocene primates. Folia Primatol 50:3-41. doi:  10.1159/000156332 CrossRefPubMedGoogle Scholar
  31. Gebo DL (2011) Vertical clinging and leaping revisited: vertical support use as the ancestral condition of strepsirrhine primates. Am J Phys Anthropol 146:323-335. doi:  10.1002/ajpa.21595 CrossRefPubMedGoogle Scholar
  32. Gower J (1975) Generalized Procrustes analysis. Psychometrika 40:33-51. doi:  10.1007/BF02291478 CrossRefGoogle Scholar
  33. Graf W, Klam F (2006) Le système vestibulaire : anatomie fonctionnelle et comparée, évolution et développement. CR Palevol 5:637-655. doi:  10.1016/j.crpv.2005.12.009 CrossRefGoogle Scholar
  34. Grohé C, Tseng ZJ, Lebrun R, Boistel R, Flynn JJ (2015) Bony labyrinth shape variation in extant Carnivora: a case study of Musteloidea. J Anat. doi:  10.1111/joa.12421 PubMedGoogle Scholar
  35. Gunz P, Mitteroecker P (2013) Semilandmarks: a method for quantifying curves and surfaces. Hystrix 24:103-109. doi:  10.4404/hystrix-24.1-6292 Google Scholar
  36. Gunz P, Mitteroecker P, Bookstein FL (2005) Semilandmarks in three dimensions. In: Slice D (ed) Modern Morphometrics in Physical Anthropology. Kluwer Academic/Plenum Publishers, New York, pp 73-98CrossRefGoogle Scholar
  37. Gunz P, Ramsier M, Kuhrig M, Hublin JJ, Spoor F (2012) The mammalian bony labyrinth reconsidered, introducing a comprehensive geometric morphometric approach. J Anat 220:529-543. doi:  10.1111/j.1469-7580.2012.01493.x CrossRefPubMedPubMedCentralGoogle Scholar
  38. Hautier L, Billet G, Eastwood B, Lane J (2014) Patterns of morphological variation of extant sloth skulls and their implication for future conservation efforts. Anat Rec 297:979–1008. doi:  10.1002/ar.22916 CrossRefGoogle Scholar
  39. Hill CA, Radovcic J, Frayer DW (2014) Brief communication: investigation of the semicircular canal variation in the Krapina neandertals. Am J Phys Anthropol 154:302-306. doi:  10.1002/ajpa.22506 CrossRefPubMedGoogle Scholar
  40. Hullar TE (2006) Semicircular canal geometry, afferent sensitivity and animal behavior. Anat Rec (A) 288(4):466-472. doi:  10.1002/ar.a.20304 CrossRefPubMedCentralGoogle Scholar
  41. Hunt K, Cant J, Gebo D, Rose M (1996) Standardized descriptions of primate locomotor and postural modes. Primates 37:363-387. doi:  10.1007/BF02381373 CrossRefGoogle Scholar
  42. Jeffery N, Ryan TM, Spoor F (2008) The primate subarcuate fossa and its relationship to the semicircular canals. part II: adult interspecific variation. J Hum Evol 55:326-339. doi:  10.1016/j.jhevol.2008.02.010 CrossRefPubMedGoogle Scholar
  43. Jeffery N, Spoor F (2004) Prenatal growth and development of the modern human labyrinth. J Anat 204:71-92. doi:  10.1111/j.1469-7580.2004.00250.x CrossRefPubMedPubMedCentralGoogle Scholar
  44. Jones GM, Spells KE (1963) A theoretical and comparative study of the functional dependence of the semicircular canal upon its physical dimensions. Proc Roy Soc London B 157:403-419. doi:  10.1098/rspb.1963.0019 CrossRefGoogle Scholar
  45. Jørgensen MB, Kristensen HK, Buch NH (2007) Thalidomide-induced aplasia of the inner ear. J Laryngol Otol 78:1095-1101. doi:  10.1017/S0022215100063234 CrossRefGoogle Scholar
  46. Jungers W (1979) Locomotion, limb proportions, and skeletal allometry in lemurs and lorises. Folia Primatol 28:8-28. doi:  10.1159/000155901 CrossRefGoogle Scholar
  47. Lawrence M, McCabe BF (1959) Inner-ear mechanics and deafness, special consideration of Meniere’s syndrome. J Am Med Assoc 171:1927-1932. doi:  10.1001/jama.1959.03010320017005 CrossRefPubMedGoogle Scholar
  48. Lebrun R (2008) Evolution and development of the strepsirrhine primate skull. PhD, Universität Zürich, Université Montpellier IIGoogle Scholar
  49. Lebrun R (2014) ISE-MeshTools, a 3D interactive fossil reconstruction freeware. 12th Annual Meeting of EAVP, Torino, ItalyGoogle Scholar
  50. Lebrun R, de León, MP, Tafforeau P, Zollikofer C (2010) Deep evolutionary roots of strepsirrhine primate labyrinthine morphology. J Anat 216:368-380. doi:  10.1111/j.1469-7580.2009.01177.x CrossRefPubMedGoogle Scholar
  51. Lebrun R, Godinot M, Couette S, Tafforeau P, Zollikofer C (2012) The labyrinthine morphology of Pronycticebus gaudryi (Primates, Adapiformes). Palaeobiodiversity and Palaeoenvironments 92:527-537. doi:  10.1007/s12549-012-0099-z CrossRefGoogle Scholar
  52. Lindeman HH (1969) Regional differences in sensitivity of the vestibular sensory epithelia to ototoxic antibiotics. Acta Oto-Laryngol 67:177-189. doi:  10.3109/00016486909125441 CrossRefGoogle Scholar
  53. Malinzak M, Kay RF, Hullar TE (2012) Locomotor head movements and semicircular canal morphology in primates. Proc Natl Acad Sci USA 109:17914-17919. doi:  10.1073/pnas.1206139109 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Martin RD (1972) Behaviour and ecology of nocturnal prosimians. Z Tierpsychol 9:43-89Google Scholar
  55. Martin RD (1990) Primate Origins and Evolution. A Phylogenetic Reconstruction. Chapman and Hall, LondonGoogle Scholar
  56. Maynard Smith J, Burian R, Kauffman S, Alberch P, Campbell J, Goodwin B, Lande R, Raup D, Wolpert L (1985) Developmental constraints and evolution. Q Rev Biol 60:265-287. doi: 10.1086/414425 CrossRefGoogle Scholar
  57. Mittermeier RA, Tattersall I, Konstant WR, Meyers DM, Mast RB (1994) Lemurs of Madagascar. Conservation International, Washington, D.C.Google Scholar
  58. Muizon C de, Billet G, Argot C, Ladevèze S, Goussard F (2015) Alcidedorbignya inopinata, a basal pantodont (Placentalia, Mammalia) from the early Palaeocene of Bolivia: anatomy, phylogeny and palaeobiology. Geodiversitas 37(4): 397-634. doi:  10.5252/g2015n4a1
  59. Napier JR, Napier PH (1967) A Handbook of Living Primates. Academic Press, LondonGoogle Scholar
  60. Némoz-Bertholet F, Aujard F (2003) Physical activity and balance performance as a function of age in a prosimian primate (Microcebus murinus). Exp Gerontol 38:407-414. doi:  10.1016/S0531-5565(02)00244-9 CrossRefPubMedGoogle Scholar
  61. Orliac MJ, Benoit J, O’Leary MA (2012) The inner ear of Diacodexis, the oldest artiodactyl mammal. J Anat 221:417-426. doi:  10.1111/j.1469-7580.2012.01562.x CrossRefPubMedPubMedCentralGoogle Scholar
  62. Orliac MJ, Ladevèze S (2007) Morphological study of the otic region and petrosal bone of Listriodontinae (Suidae, Mammalia). J Morphol 268:1113-1114.Google Scholar
  63. Ortmann S, Heidmaier G, Schmid J, Ganzhorn JU (1997) Spontaneous daily torpor in Malagasy mouse lemurs. Naturwissenschatfen 84:28-32. doi:  10.1007/s001140050344 CrossRefGoogle Scholar
  64. Panagiotopoulou O, Rankin J, Gatesy S, Hutchinson J (2015) Biomechanics of mammalian feet during locomotion: an integrative 3D analysis. FASEB J 29:342.5Google Scholar
  65. Pearson K (1901) On lines and planes of closest fit to systems of points in space. Phil Mag 2:559-572CrossRefGoogle Scholar
  66. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical computing, Vienna, Austria. URL http://www.R-project.org/
  67. Rabbitt RD, Damiano ER, Grant JW (2004) Biomechanics of the semicircular canals and otolith organs. In: Highstein SM, Fay RR, Popper AN (eds) The Vestibular System. Springer, New York, pp 153-200. doi:  10.1007/0-387-21567-0_4 CrossRefGoogle Scholar
  68. Ravel A, Orliac M (2014) The inner ear morphology of the ‘condylarthran’ Hyopsodus lepidus. Hist Biol 1-13. doi: 10.1080/08912963.2014.915823
  69. Rollinson JMM, Martin RD (1981) Comparative aspects of primate locomotion, with special reference to arboreal cercopithecines. Symp Zool Soc London 48:377-427Google Scholar
  70. Rowe N, Goodall J, Mittermeier R (1996) The Pictorial Guide to the Living Primates (Vol. 9). Pogonias Press, New YorkGoogle Scholar
  71. Ryan TM, Silcox MT, Walker A, Mao X, Begun DR, Benefit BR, Gingerich PD, Köhler M, Kordos L, McCrossin ML, Moyà-Solà S, Sanders WJ, Seiffert ER, Simons E, Zalmout IS, Spoor F (2012) Evolution of locomotion in Anthropoidea: the semicircular canal evidence. Proc Roy Soc London B 279:3467-3475. doi:  10.1098/rspb.2012.0939 CrossRefGoogle Scholar
  72. Schmelzle T, Sanchez-Villagra MR, Maier W (2007) Vestibular labyrinth diversity in diprotodontian marsupial mammals. Mammal Stud 32:83-97. doi:  10.3106/1348-6160(2007)32[83:VLDIDM]2.0.CO;2 CrossRefGoogle Scholar
  73. Schuknecht HF (1969) Cupulolithiasis. Arch Otolaryngol 90:765-778. doi:  10.1001/archotol.1969.00770030767020 CrossRefPubMedGoogle Scholar
  74. Silcox MT, Bloch JI, Boyer DM, Godinot M, Ryan TM, Spoor F, Walker A (2009) Semicircular canal system in early primates. J Hum Evol 56:315-327. doi:  10.1016/j.jhevol.2008.10.007 CrossRefPubMedGoogle Scholar
  75. Specht M, Lebrun R, Zollikofer CPE (2007) Visualizing shape transformation between chimpanzee and human braincases. Visual Comput 23:743-751. doi:  10.1007/s00371-007-0156-1 CrossRefGoogle Scholar
  76. Spoor F, Bajpai S, Hussain ST, Kumar K, Thewissen JGM (2002) Vestibular evidence for the evolution of aquatic behaviour in early cetaceans. Nature 417:163-166. doi:  10.1038/417163a CrossRefPubMedGoogle Scholar
  77. Spoor F, Garland T, Krovitz G, Ryan TM, Silcox MT, Walker A (2007) The primate semicircular canal system and locomotion. Proc Natl Acad Sci USA 104:10808-10812. doi:  10.1073/pnas.0704250104 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Spoor F, Wood B, Zonneveld F (1994) Implications of early hominid labyrinthine morphology for evolution of human bipedal locomotion. Nature 369:645-648. doi:  10.1038/369645a0 CrossRefPubMedGoogle Scholar
  79. Spoor F, Zonneveld F (1995) Morphometry of the primate bony labyrinth: a new method based on high-resolution computed tomography. J Anat 186:271-286PubMedPubMedCentralGoogle Scholar
  80. Spoor F, Zonneveld F (1998) Comparative review of the human bony labyrinth. Am J Phys Anthropol Suppl 27:211-251. doi:  10.1002/(SICI)1096-8644(1998)107:27+<211::AID-AJPA8>3.0.CO;2-V CrossRefGoogle Scholar
  81. Stevenson MF, Poole TB (1976) An ethogram of the common marmoset (Calithrix jacchus jacchus): general behavioural repertoire. Anim Behav 24:428-451. doi:  10.1016/S0003-3472(76)80053-X CrossRefPubMedGoogle Scholar
  82. Van Valkenburgh B (1985) Locomotor diversity within past and present guilds of large predatory mammals. Paleobiology 11:406-428. doi:  10.2307/2400556 CrossRefGoogle Scholar
  83. Van Valkenburgh B (1987) Skeletal indicators of locomotor behavior in living and extinct carnivores. J Vertebr Paleontol 7:162-182. doi:  10.1080/02724634.1987.10011651 CrossRefGoogle Scholar
  84. Walker A (1969) The locomotion of the lorises, with special reference to the potto. E Afr Wildlife J 8:l-5. doi:  10.1111/j.1365-2028.1969.tb01187.x Google Scholar
  85. Walker A (1974) Locomotor adaptations in past and present prosimian primates. In: FA Jenkins (ed) Primate Locomotion. Academic Press, New York and London, pp 349-382Google Scholar
  86. Walker A, Ryan TM, Silcox MT, Simons EL, Spoor F (2008) The semicircular canal system and locomotion:the case of extinct lemuroids and lorisoids. Evol Anthropol 17(3):135-145. doi:  10.1002/evan.20165 CrossRefGoogle Scholar
  87. Webster M, Sheets HD (2010) A practical introduction to landmark-based geometric morphometrics. Quantitative Methods in Paleobiology 16:168-188.Google Scholar
  88. Yang A, Hullar TE (2007) Relationship of semicircular canal size to vestibular-nerve afferent sensitivity in mammals. J Neurophysiol 98:3197-3205 doi:  10.1152/jn.00798.2007 CrossRefPubMedGoogle Scholar
  89. Young NM (2006) Function, ontogeny and canalization of shape variance in the primate scapula. J Anat 209:623-636. doi:  10.1111/j.1469-7580.2006.00639.x CrossRefPubMedPubMedCentralGoogle Scholar
  90. Young JW (2009) Substrate determines asymmetrical gait dynamics in marmosets (Callithrix jacchus) and squirrel monkeys (Saimiri boliviensis). Am J Phys Anthropol 138:403-420. doi:  10.1002/ajpa.20953 CrossRefPubMedGoogle Scholar
  91. Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric Morphometrics for Biologists: A Primer. Academic Press, New YorkGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Laboratoire de Paléontologie, Institut des Sciences de l’Évolution de Montpellier (ISE-M, UMR 5554, CNRS/UM/IRD/EPHE), c.c. 064Université de MontpellierMontpellier Cedex 05France
  2. 2.African Primate Initiative for Ecology and Speciation, Department of Zoology and EntomologyUniversity of Fort HareAliceSouth Africa

Personalised recommendations