Skip to main content Accessibility help
×
Hostname: page-component-848d4c4894-tn8tq Total loading time: 0 Render date: 2024-07-05T15:14:41.799Z Has data issue: false hasContentIssue false

8 - Primate Olfaction: Anatomy and Evolution

from Section II - Social Functioning: Role of Evolution, Genetics and Gender

Published online by Cambridge University Press:  17 August 2009

Warrick J. Brewer
Affiliation:
Mental Health Research Institute of Victoria, Melbourne
David Castle
Affiliation:
University of Melbourne
Christos Pantelis
Affiliation:
University of Melbourne
Get access

Summary

Introduction

Primate origins

The living primates are commonly divided into two suborders: Strepsirrhini comprising the lemurs, lorises and galagos; and Haplorhini containing tarsiers and anthropoids (Table 8.1, Figure 8.1). These two groups had diverged from one another by the beginning of the Eocene period (Rose & Bown, 1991), where they are represented by the adapoids and omomyoids respectively. Together, the living and fossil strepsirrhines and haplorhines are known as ‘crown primates’ or ‘euprimates’. Any primates preceding the divergence of the two euprimate suborders would be called stem primates, and a growing body of evidence suggests that the plesiadapiforms, a diverse radiation known mainly from the Paleocene period, are such a group (Bloch & Boyer, 2002). While the origin of stem primates constitutes the true origin of the primate order, most adaptive scenarios of ‘primate origins’ have focused on anatomical differences between euprimates and other mammals.

Of the several theories that have been developed to account for the origin of primates (see Cartmill (1992) and Sussman (1999) for more thorough discussion and original references), two have specific bearing on the topic of this chapter. The arboreal theory (e.g. Jones, 1916; Smith, 1927) holds that the features which distinguish primates from other mammals (divergent hallux and pollex, regressive rostrum, more forward-facing position of the orbits (known as ‘orbital convergence’)) are adaptations for an arboreal existence.

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2006

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allen, H. (1882) On a revision of the ethmoid bone in Mammalia, with special reference to the description of this bone in and of the sense of smell in the Chiroptera. Bull Mus Comp Zool Harv, 10, 135–64.Google Scholar
Ankel-Simons, F. (2000) Primate Anatomy: An Introduction. New York: Academic Press.
Arreola, A. G., Lopez Serna, N., Hoyos Parra, R., et al. (1996) Morphogenesis of the lateral nasal wall from 6 to 36 weeks. Otolaryngol Head Neck Surg, 114, 54–60.Google Scholar
Aujard, F. (1997) Effect of vomeronasal organ removal on male socio-sexual responses to female in a prosimian primate (Microcebus murinus). Physiol Behav, 62, 1003–8.Google Scholar
Baron, G., Frahm, H. D., Bhatnagar, K. P., et al. (1983) Comparison of brain structure volumes in Insectivora and Primates. III. Main olfactory bulb (MOB). J fur Hirnforschung, 24, 551–68.Google Scholar
Barton, R. A., Purvis, A. & Harvey, P. H. (1995) Evolutionary radiation of visual and olfactory brain systems in primates, bats and insectivores. Philos Trans R Soc Lond B Biol Sci, 348, 381–92.Google Scholar
Beard, K. C. (1988) The phylogenetic significance of strepsirrhinism in Paleogene primates. Int J Primatol, 9, 83–96.Google Scholar
Beard, K. C., Krishtalka, L. & Stucky, R. K. (1991) First skulls of the early Eocene primate Shoshonius cooperi and the anthropoid-tarsier dichotomy. Nature, 349, 64–7.Google Scholar
Bhatnagar, K. P. & Kallen, F. C. (1974) Cribriform plate of ethmoid, olfactory bulb and olfactory acuity in forty species of bats. J Morphol, 142, 71–89.Google Scholar
Blanton, P. L. & Biggs, N. L. (1968) Eighteen hundred years of controversy: the paranasal sinuses. Am J Anat, 124, 135–47.Google Scholar
Bloch, J. I. & Boyer, D. M. (2002) Grasping primate origins. Science, 298, 1606–10.Google Scholar
Buck, L. & Axel, R. (1991) A Novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell, 65, 175–87.
Bush, E., Simons, E. & Allman, A. (2004) High resolution CT study of the cranium of a fossil anthropoid primate, Parapithecus grangeri: new insights into the evolutionary history of primate sensory systems. Anat Rec, 281A, 1083–7.Google Scholar
Cartmill, M. (1970) The Orbits of Arboreal Mammals: A Reassessment of the Arboreal Theory of Primate Evolution. Chicago: University of Chicago Press.
Cartmill, M. (1992) New views on primate origins. Evol Anthropol, 1, 105–111.
Cave, A. J. E. (1967) Observations on the platyrrhine nasal fossa. Am J Phys Anthropol, 26, 277–88.Google Scholar
Cave, A. J. E. (1973) The primate nasal fossa. Biol J Linnean Soc, Lond, 5, 377–87.Google Scholar
Cave, A. J. E. & Haines, R. W. (1940) The paranasal sinuses of anthropoid apes. J Anat, 74, 493–523.Google Scholar
Dagg, A. I. & Taub, A. (1970) Flehmen. Mammalia, 34, 686–95.Google Scholar
Beer, G. (1937) The Development of the Vertebrate Skull. Oxford: Oxford University Press.
Dennis, J. C., Smith, T. D., Bhatnagar, K. P., et al. (2004) Expression of neuron-specific markers by the vomeronasal neuroepithelium in six primate species. Anat Rec, 281A, 1190–200.Google Scholar
Dominy, N. J., Ross, C. F. & Smith, T. D. (2004) Evolution of primate special senses: past, present and future. Anat Rec, 281A, 1078–82.Google Scholar
Enlow, D. H. & Hans, M. G. (1996) Essentials of Facial Growth. Philadelphia: W. B. Saunders Company.
Estes, R. D. (1972) The role of the vomeronasal organ in mammalian reproduction. Mammalia, 36, 315–41.Google Scholar
Frahm, H. D. (1985) Comparison of main olfactory bulb size in mammals. Fortschritte der Zoologie, 30, 691–3.Google Scholar
Gilad, Y., Man, O., Pääbo, S., et al. (2003) Human specific loss of olfactory receptor genes. Proc Nat Acad Sci USA, 100, 3324–7.Google Scholar
Gilad, Y., Wiebe, V., Przeworski, M., et al. (2004) Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLOS Biol, 2, 1–6.Google Scholar
Gingerich, P. D. (1976) Cranial anatomy and evolution of early Tertiary Plesiadapidae (Mammalia:Primates). University of Michigan, Mus Paleontol Papers Paleontol, 15, 1–141.Google Scholar
Gingerich, P. D. & Martin, R. D. (1981) Cranial morphology and adaptations in Eocene Adapidae. II. The Cambridge skull of Adapis parisiensis. Am J Physical Anthropol, 56, 235–57.Google Scholar
Glendenning, K. K. & Masterson, R. B. (1998) Comparative morphometry of mammalian central auditory systems: variation in nuclei and form of the ascending system. Brain, Behav Evol, 51, 59–89.Google Scholar
Harkema, J. R. (1991) Comparative aspects of nasal airway anatomy: relevance to inhalation toxicology. Toxicol Pathol, 19, 321–36.Google Scholar
Hershkovitz, P. (1977) Living New World Monkeys (Platyrrhini). Chicago: University of Chicago Press.
Hofer, H. O. (1977) The anatomical relations of the Ductus vomeronasalis and the occurrence of taste buds in the Papilla palatina of Nycticebus coucang (Primates, Prosmiae) with remarks on strepsirrhinism. Gegenbaurs Morphologische Jahrbuch, 123, 836–56.Google Scholar
Hofer, H. O. (1980) The external anatomy of the oro-nasal region of primates. Zeitschrift fur Morphologie und Anthropologie, 71, 233–49.Google Scholar
Horovitz, I. & MacPhee, R. D. E. (1999) The Quaternary Cuban platyrrhine Paralouatta varonai and the origin of Antillean monkeys. J Hum Evol, 36, 33–68.Google Scholar
Jones, F. W. (1916) Arboreal Man. London: Edward Arnold.
Kay, R. F. & Cartmill, M. (1974) Skull of Palaechthon nacimienti. Nature, 252, 37–8.Google Scholar
Kay, R. F., Ross, C. F. & Williams, B. A. (1997) Anthropoid origins. Science, 275, 797–804.Google Scholar
Kay, R. F., Rossie, J. B., Colbert, M. W., et al. (2004) Observations of Tremacebus harringtoni (Platyrrhini, Early Miocene, Sacanana, Argentina) based on high-resolution X-ray CT-scans. Anat Rec, 281A, 1157–72.Google Scholar
Keith, A. (1948) Human Embryology and Morphology (6th edn). London: Edward Arnold & Co.
Kollmann, M. & Papin, L. (1925) Etudes sur lémuriens. Anatomie compareé des fosses nasales et de leurs annexes. Archs Morph Gén Exp, 22, 1–60.Google Scholar
Laska, M., Seibt, A. & Weber, A. (2000) ‘Microsmatic’ primates revisited: olfactory sensitivity in the squirrel monkey. Chem Senses, 25, 47–53.Google Scholar
Laska, M., Wieser, A., Rivas Bautista, R. M., et al. (2004) Olfactory sensitivity for carboxylic acids in Spider monkeys and pigtail macaques. Chem Senses, 29, 101–9.Google Scholar
Gros Clark, W. (1925) On the skull of Tupaia. Proc Zoolog Soc Lond 1925, 559–67.Google Scholar
Gros Clark, W. (1926) On the anatomy of the pen-tailed tree shrew (Ptilocercus lowii). Proc Zoolog Soc Lond 1926, 1179–1309.Google Scholar
Gros Clark, W. (1959) The Antecedents of Man. Edinburgh: Edinburgh University Press.
Lieberman, D. E., Ross, C. F. & Ravosa, M. J. (2000) The primate cranial base: ontogeny, function, and integration. Am J Physic Anthropol, Suppl 31, 117–69.Google Scholar
Liman, E. R. & Innan, H. (2003) Relaxed selective pressure on an essential component of pheromone transduction in primate evolution. Proc Nat Acad Sci USA, 100, 3328–32.Google Scholar
Maier, W. (1980) Nasal structures in Old and New World primates. In Evolutionary Biology of New World Monkeys and Continental Drift (eds. Ciochon, R. & Chiarelli, A. B.), pp. 219–241. New York: Plenum.
Maier, W. (1987) Functional principals of the growing skull of primates as shown by the posterior cupula of the nasal capsule. In Définition et Origines de l'Homme (ed Sakka, M.), pp. 199–207. Paris: CNRS.
Maier, W. (1991) Aspects of the ontogenetic development of nasal and facial skeletons in primates. In Craniofacial Abnormalities and Clefts of the Upper Lip (ed. Pfeiffer, G.), pp. 115–24. Stuttgart: Thieme.
Maier, W. (1993) Zur evolutiven und funktionellen Morphologie des Gesichtsschaedels der Primaten. Zeitschrift fur Morphologie und Anthropologie, 79, 279–99.Google Scholar
Maier, W. (1997) The nasopalatine duct and the nasal floor cartilages in catarrhine primates. Zeitschrift fur Morphologie und Anthropologie, 81, 289–300.Google Scholar
Maier, W. (2000) Ontogeny of the nasal capsule in cercopithecoids: a contribution to the comparative and evolutionary morphology of catarrhines. In Old World Monkeys (eds Whitehead, P. F. & Jolly, C. J.), pp. 99–132. Cambridge: Cambridge University Press.
Martin, R. D. (1990) Primate Origins and Evolution. A Phylogenetic Reconstruction. Princeton, NJ: Princeton University Press.
Menco, B. Ph. M. & Morrison, E. E. (2003) Morphology of the mammalian olfactory epithelium: form, fine structure, function, and pathology. In Handbook of Olfaction and Gustation (ed Doty, R. L.), pp. 17–49. New York: Marcel Dekker.
Moore, W. J. (1981) The Mammalian Skull. Cambridge: Cambridge Univ. Press.
Moss-Salentijn, L. (1991) Anatomy and embryology. In Surgery of the Paranasal Sinuses (ed Blitzer, A., Lawson, W. & Friedman, W.), pp. 1–24. Philadelphia: Saunders.
Moulton, D. G. (1967) Olfaction in mammals. Am Zoolog, 7, 421–9.Google Scholar
Negus, V. (1958) The Comparative Anatomy and Physiology of the Nose and Paranasal Sinuses. London: Livingstone.
Paulli, S. (1900) Über die Pneumaticität des Schädels bei den Säugethieren. III. Über die Morphologie des Siebbeins der Pneumaticität bei den Insectivoran, Hyracoideen, Chiropteren, Carnivoren, Pinnepedien, Edentates, Rodentiern, Prosimien und Primaten. Gegenbaurs Morphologische Jahrbuch, 28, 483–564.Google Scholar
Pocock, R. I. (1918) On the external characters of the lemurs and Tarsius. Proc Zoolog Soc Lond 1918, 19–53.Google Scholar
Radinsky, L. (1970) The fossil evidence of prosimian brain evolution. In The Primate Brain: Advances in Primatology - Volume 1 (eds Noback, C. R. & Montagna, W.), pp. 209–24. New York: Appleton-Century-Crofts.
Radinsky, L. (1977) Early primate brains: fact and fiction. J Hum Evol, 6, 79–86.Google Scholar
Rae, T. C., Koppe, T., Spoor, C. F., et al. (2002) Ancestral loss of the maxillary sinus in Old World monkeys and independent acquisition in Macaca. Am J Physical Anthropol, 117, 293–6.Google Scholar
Rasmussen, D. T., Shekelle, M., Walsh, S. L., et al. (1995) The dentition of Dyseolemur, and comments on the use of the anterior teeth in primate systematics. J Hum Evol, 29, 301–20.Google Scholar
Rose, K. D. & Brown, T. M. (1991) Additional fossil evidence on the differentiation of the earliest euprimates. Proc Nat Acad Sci USA, 88, 98–101.Google Scholar
Ross, C. F. (1994) The craniofacial evidence for anthropoid and tarsier relationships. In Anthropoid Origins (eds Fleagle, J. G. & Kay, R. F.), pp. 469–547. New York: Plenum Press.
Ross, C. F. (1995) Allometric and functional influences on primate orbit orientation and the origins of the Anthropoidea. J Hum Evol, 29, 201–27.
Ross, C. F. & Ravosa, M. J. (1993) Basicranial flexion, relative brain size, and facial Kyphosis in nonhuman primates. Am J Phys Anthropol, 91, 305–24.
Rossie, J. B. (2003) Ontogeny, Homology, and Phylogenetic Significance of Anthropoid Paranasal Sinuses. Yale University.
Rossie, J. B. (2006) Ontogeny and homology of the paranasal sinuses in Platyrrhini (Mammalia: Primates). J Morphol, 267, 1–40.Google Scholar
Rossie, J. B. (2005) Anatomy of the nasal cavity and paranasal sinuses in Aegyptopithecus and early Miocene African catarrhines. Am J Phys Anthropol, 126, 250–67.Google Scholar
Rossie, J. B. & Beard, K. C. (2004) Intracranial anatomy of Shoshonius cooperi (Tarsiiformes, Primates) as revealed by high-resolution computed tomography. J Verteb Paleontol, 24 (Suppl 3), 106A.Google Scholar
Rossie, J. B., Ni, X. & Beard, K. C (2006) Cranial remains of an Ecocene tarsier. Proc Natl Acad Sci, USA, 103, 4381–85.
Rouquier, S., Blancher, A. & Giorgi, D. (2000) The olfactory receptor gene repertoire in primates and mouse: evidence for reduction of the functional fraction in primates. Proc Nat Acad Sci USA, 97, 2870–4.Google Scholar
Seiffert, E. R., Kappelman, J. & Ryan, T. M. (1999) The nasal fossa of Rooneyia viejaensis as revealed by high-resolution X-ray computed tomography. A J Phys Anthropol, 28, 247–8.Google Scholar
Seiler, R. (1976) Die Gesichtsmuskeln. In Primatologia, Vol.4 (eds Hofer, H. O., Schultz, A. H. & Starck, D.), pp. 1–252. White Plains: S. Karger.
Silcox, M. T. (2003) New discoveries on the middle ear anatomy of Ignacius graybullianus (Paromomyidae, Primates) from ultra high resolution X-ray computed tomography. J Hum Evol, 44, 73–86.Google Scholar
Smith, G. E. (1927) The Evolution of Man. London: Oxford University Press.
Smith, T. D. & Bhatnagar, K. P. (2004) ‘Microsmatic’ primates: reconsidering how and when size matters. Anat Rec, 279B, 24–31.Google Scholar
Smith, T. D., Siegel, M. I. & Bhatnagar, K. P. (2001) A reappraisal of the vomeronasal system of catarrhine primates: ontogeny, morphology, functionality, and persisting questions. Anat Rec (New Anatomist), 265, 176–92.Google Scholar
Smith, T. D., Bhatnagar, K. P., Bonar, C. J., et al. (2003) Ontogenetic characteristics of the vomeronasal organ in Saguinus geoffroyi and Leontopithecus rosalia with comparisons to other primates. Am J Phys Anthropol, 121, 342–53.Google Scholar
Smith, T. D., Bhatnagar, K. P., Shimp, K. L., et al. (2002) Histological definition of the vomeronasal organ in humans and chimpanzees, with a comparison to other primates. Anat Rec, 267, 166–76.Google Scholar
Smith, T. D., Bhatnagar, K. P., Tuladhar, P., et al. (2004) Distribution of olfactory epithelium in the primate nasal cavity: are ‘microsmia’ and ‘macrosmia’ valid morphological concepts?Anat Rec, 281A, 1173–81.Google Scholar
Starck, D. (1984) The nasal cavity and nasal skeleton of Tarsius. In Biology of Tarsiers (ed Niemitz, C.), pp. 275–90. Stuttgart: Fischer Verlag.
Stephan, H., Frahm, H. & Baron, G. (1981) New and revised data on volumes of brain structures in insectivores and primates. Folia Primatologica, 35, 1–29.Google Scholar
Szalay, F. S. (1969) Mixodectidae, Microsyopidae, and the insectivore-primate transition. Bull Am Mus Nat Hist, 140, 193–330.Google Scholar
Szalay, F. & Delson, E. (1979) Evolutionary History of the Primates. New York: Academic Press.
Takai, M., Shigehera, N., Egi, N., et al. (2003) Endocranial cast and morphology of the olfactory bulb of Amphipithecus mogaungensis (latest middle Eocene of Myanmar). Primates, 44, 137–44.Google Scholar
Turner, W. (1891) The convolutions of the brain: a study in comparative anatomy. J Anat Physiol, 25, 105–53.Google Scholar
Wako, K., Hiratsuka, H., Katsuta, O., et al. (1999) Anatomical structure and surface epithelial distribution in the nasal cavity of the common cotton-eared marmoset (Callithrix jacchus). Exp Animals, 48, 31–6.Google Scholar
Ward, S. C. & Brown, B. (1986) The facial skeleton of Sivapithecus indicus. In Comparative Primate Biology, Vol. 1: Systematics, Evolution and Anatomy (eds Swindler, D. R. & Erwin, J.), pp. 413–52. New York: Alan R. Liss.
Webb, D. M., Cortés-Ortiz, L. & Zhang, J. (2004) Genetic evidence for the coexistence of pheromone perception and full trichromatic vision in howler monkeys. Molec Biol Evol, 21, 697–704.Google Scholar
Whinnett, A. & Mundy, N. I. (2003) Isolation of novel olfactory receptor genes in marmosets (Callithrix): insights into pseudogene formation and evidence for functional degeneracy in non-human primates. 304, 87–96.
Witmer, L. M. (1997) The evolution of the antorbital cavity of archosaurs: a study in soft-tissue reconstruction in the fossil record with an analysis of the function of pneumaticity. J Verteb Paleontol, 17, 1–73.Google Scholar
Witt, M., Georgiewa, B., Knecht, M., et al. (2002) On the chemosensory nature of the vomeronasal epithelium in adult humans. Histochem CellBiol, 117, 493–509.Google Scholar
Wysocki, C. J. & Preti, G. (2004) Facts, fallacies, fears and frustrations with human pheromones. Anat Rec, 281A, 1201–11.Google Scholar
Zhang, J. & Webb, D. M. (2003) Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates. Proc Nat Acad Sci USA, 100, 8337–41.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×