Journal of Mammalian Evolution

, Volume 6, Issue 1, pp 39–65 | Cite as

The Entotympanic of Pangolins and the Phylogeny of the Pholidota (Mammalia)

  • Timothy J. Gaudin
  • John R. Wible


Entotympanics are independent elements present in the auditory bullae of various eutherians. An entotympanic has been reported for extant pangolins of the Order Pholidota, but the actual distribution of this element remains uncertain, in part, because it is a small, loosely attached structure that is often lost in macerated skulls. Consequently, it is unknown whether or not the entotympanic characterizes Pholidota primitively or has evolved within the group. This report addresses the morphology and distribution of the entotympanic among living and extinct pholidotans. An entotympanic occurs in the African pangolins Manis gigantea, M. temminckii, and in one specimen of M. tricuspis. In each, it is a small, nodular bone that occupies a distinct fossa primarily on the basioccipital, the presence of which allows us to assess the occurrence of an entotympanic even in specimens in which the bone has fallen out. Both the entotympanic and the basioccipital facet are lacking in the four remaining extant pangolin species and in the late Eocene pangolin Patriomanis. To assess the significance of this entotympanic distribution, a phylogenetic analysis of extant pangolins plus Patriomanis based on 67 cranial characters was performed. Four different outgroup analyses all resulted in the same single most parsimonious tree, in which the three extant Asian pangolins form a monophyletic clade and the four extant African pangolins fall into a paraphyletic assemblage. Optimization of the entotympanic distribution onto this tree results in two patterns, dependent on the outgroup choice. If Patriomanis is the sole outgroup to the extant pangolins, the entotympanic arises within pangolins as a synapomorphy of Manis gigantea and M. temminckii, convergently acquired in some M. tricuspis. If Xenarthra and Palaeanodonta are employed as outgroups, the entotympanic optimization is ambiguous: the pattern is either as above or the entotympanic is present primitively within Pholidota and lost secondarily in Patriomanis and a clade comprising M. tricuspis, M. tetradactyla, and the Asian forms.

Pholidota entotympanics pangolins phylogeny 


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  1. Barlow, J. C. (1984). Xenarthrans and pholidotes. In: Orders and Families of Recent Mammals of the World, S. Anderson and J. Knox Jones, Jr., eds., pp. 219–239, John Wiley & Sons, New York.Google Scholar
  2. Cifelli, R. L. (1983). Eutherian tarsals from the late Paleocene of Brazil. Am. Mus. Novitates 2761: 1–31.Google Scholar
  3. Corbet, G. B., and Hill, J. E. (1991). A World List of Mammalian Species, 3rd ed., British Museum (Natural History), London.Google Scholar
  4. Czelusniak, J., Goodman, M., Koop, B. F., Tagle, D. A., Shoshani, J., Braunitzer, G., Kleinschmidt, T. K., DeJong, W. W., and Matsuda, G. (1990). Perspectives from amino acid and nucleotide sequences on cladistic relationships among higher taxa of Eutheria. In: Current Mammalogy, Vol. 2, H. H. Genoways, ed., pp. 545–572, Plenum Press, New York.Google Scholar
  5. De Beer, G. R. (1937). The Development of the Vertebrate Skull, Clarendon Press, Oxford.Google Scholar
  6. Emry, R. J. (1970). A North American Oligocene pangolin and other additions to the Pholidota. Bull. Am. Mus. Nat. Hist. 142: 455–510.Google Scholar
  7. Engelmann, G. F. (1978). The Logic of Phylogenetic Analysis and the Phylogeny of the Xenarthra (Mammalia), Ph.D. dissertation, Columbia University, New York.Google Scholar
  8. Engelmann, G. F. (1985). The phylogeny of the Xenarthra. In: The Ecology and Evolution of Armadillos, Sloths, and Vermilinguas, G. G. Montgomery, ed., pp. 51–64, Smithsonian Institution Press, Washington, DC.Google Scholar
  9. Eschweiler, R. (1899). Zur vergleichenden Anatomie der Muskeln und der Topographie des Mittelohres verschiedener Säugethiere. Arch. Mikr. Anat. 53: 558–622.Google Scholar
  10. Frechkop, S. (1931). Notes sur les mammifères. VI. Quelques observations sur la classification des pangolins (Manidae). Bull. Mus. Roy. Sci. Nat. Belg. 7: 1–14.Google Scholar
  11. Gaudin, T. J. (1993). Phylogeny of the Tardigrada (Mammalia, Xenarthra) and the Evolution of Locomotor Function in the Xenarthra, Ph.D. dissertation, University of Chicago, Chicago.Google Scholar
  12. Gaudin, T. J. (1995). The ear region of edentates and the phylogeny of the Tardigrada (Mammalia, Xenarthra). J. Vert. Paleontol. 15: 672–705.Google Scholar
  13. Gaudin, T. J., and Branham, D. G. (1998). The phylogeny of the Myrmecophagidae (Mammalia, Xenarthra, Vermilingua) and the relationship of Eurotamandua to the Vermilingua. J. Mammal. Evol. 5: 237–265.Google Scholar
  14. Gaudin, T. J., Wible, J. R., Hopson, J. A., and Turnbull, W. D. (1996). Reexamination of the morphological evidence for the Cohort Epitheria (Mammalia, Eutheria). J. Mammal. Evol. 3: 31–79.Google Scholar
  15. Glass, B. P. (1985). History of classification and nomenclature in Xenarthra (Edentata). In: The Ecology and Evolution of Armadillos, Sloths, and Vermilinguas, G. G. Montgomery, ed., pp. 1–3, Smithsonian Institution Press, Washington, DC.Google Scholar
  16. Grassé, P.-P. (1955). Ordre de Pholidotes. In: Traité de Zoologie, Vol. 17, Mammifères, P.-P. Grassé, ed., pp. 1267–1282, Masson et Cie, Paris.Google Scholar
  17. Graur, D., Duret, L., and Gouy, M. (1996). Phylogenetic position of the order Lagomorpha (rabbits, hares and allies). Nature 379: 333–335.PubMedGoogle Scholar
  18. Hershkovitz, P. (1992). Ankle bones: The Chilean opposum Dromiciops gliroides Thomas, and marsupial phylogeny. Bonn. Zool. Beitr. 43: 181–213.Google Scholar
  19. Hoffstetter, R. (1982). Les édentés xenartres, un groupe singulier de la faune neotropical. In: Paleontology, Essential of Historical Geology, E. M. Gallitelli, ed., pp. 385–443, STEM Mocchi Modena Press, Modena, Italy.Google Scholar
  20. Jollie, M. (1968). The head skeleton of a new-born Manis javanica with comments on the ontogeny and phylogeny of the mammal head skeleton. Acta Zool. 49: 227–305.Google Scholar
  21. Koenigswald, W. v., and Martin, T. (1990). Ein Skelett von Necromanis franconica, einem Schuppentier (Pholidota, Mammalia) aus dem Aquitan von Saulcet im Allier-Becken (Frankreich). Ecol. Geol. Helv. 83: 845–864.Google Scholar
  22. MacPhee, R. D. E. (1979). Entotympanics, ontogeny and primates. Folia Primatol. 31: 23–47.PubMedGoogle Scholar
  23. MacPhee, R. D. E. (1981). Auditory regions of primates and eutherian insectivores: Morphology, ontogeny and character analysis. Contrib. Primatol. 18: 1–282.Google Scholar
  24. MacPhee, R. D. E. (1994). Morphology, adaptations, and relationships of Plesiorycteropus, and a diagnosis of a new order of eutherian mammals. Bull. Am. Mus. Nat. Hist. 220: 1–214.Google Scholar
  25. MacPhee, R. D. E., and Novacek, M. J. (1993). Definition and relationships of Lipotyphla. In: Mammal Phylogeny: Placentals, F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds., pp. 13–31, Springer-Verlag, New York.Google Scholar
  26. Maier, W. (1989). Morphologische Untersuchungen am Mittelohr der Marsupialia. Z. Zool. Syst. Evol.-Forsch. 27: 149–168.Google Scholar
  27. Matthew, W. D. (1918). A revision of the lower Eocene Wasatch and Wind River faunas. Part V. Insectivora (continued), Glires, Edentata. Bull. Am. Mus. Nat. Hist. 38: 565–657.Google Scholar
  28. McKenna, M. C. (1992). The alpha crystallin A chain of the eye lens and mammalian phylogeny. Ann. Zool. Fenn. 28: 349–360.Google Scholar
  29. McKenna, M. C., and Bell, S. K. (1997). Classification of Mammals Above the Species Level, Colombia University Press, New York.Google Scholar
  30. Miyamoto, M. M., and Goodman, M. (1986). Biomolecular systematics of eutherian mammals: Phylogenetic pattern and classification. Syst. Zool. 35: 230–240.Google Scholar
  31. Norman, J. E., and Ashley, M. V. (1994). Molecular systematics of the xenarthrans. Am. Soc. Mamm. 75th Anniv. Mtg., Abstr. 271.Google Scholar
  32. Norris, C. A. (1993). Changes in the composition of the auditory bulla in southern Solomon Islands populations of the grey cuscus, Phalanger orientalis breviceps (Marsupialia, Phalangeridae). Zool. J. Linn. Soc. 107: 93–106.Google Scholar
  33. Novacek, M. J. (1977). Aspects of the problem of variation, origin and evolution of the eutherian auditory bulla. Mammal Rev. 7: 131–149.Google Scholar
  34. Novacek, M. J. (1986). The skull of leptictid insectivorans and the higher-level classification of eutherian mammals. Bull. Am. Mus. Nat. Hist. 183: 1–112.Google Scholar
  35. Novacek, M. J. (1992). Mammalian phylogeny: Shaking the tree. Nature 356: 121–125.PubMedGoogle Scholar
  36. Novacek, M. J. (1993). Patterns of diversity in the mammalian skull. In: The Skull, Vol. 2: Patterns of Structural and Systematic Diversity, J. Hanken and B. K. Hall, eds., pp. 438–545, University of Chicago Press, Chicago.Google Scholar
  37. Novacek, M. J., and Wyss, A. (1986). Higher-level relationships of the recent eutherian orders: morphological evidence. Cladistics 2: 257–287.Google Scholar
  38. Novacek, M. J., Wyss, A. R., and McKenna, M. C. (1988). The major groups of eutherian mammals. In: The Phylogeny and Classification of Tetrapods, Vol. 2. Mammals, M. J. Benton, ed., pp. 31–71, Clarendon Press, Oxford.Google Scholar
  39. Nowak, R. M. (1991). Walker's Mammals of the World, 5th ed., Johns Hopkins University Press, Baltimore.Google Scholar
  40. Patterson, B. (1978). Pholidota and Tubulidentata. In: Evolution of African Mammals, V. J. Maglio and H. B. S. Cooke, eds., pp. 268–278, Harvard University Press, Cambridge, MA.Google Scholar
  41. Patterson, B., Segall, W., and Turnbull, W. D. (1989). The ear region in xenarthrans (=Edentata, Mammalia). Part I. Cingulates. Fieldiana Geol. n.s. 18: 1–46.Google Scholar
  42. Patterson, B., Segall, W., Turnbull, W. D., and Gaudin, T. J. (1992). The ear region in xenarthrans (=Edentata, Mammalia). Part II. Pilosa (sloths, anteaters), palaeanodonts, and a miscellany. Fieldiana Geol. n.s. 24: 1–79.Google Scholar
  43. Pocock, R. I. (1924). The external characters of the pangolins (Manidae). Proc. Zool. Soc. London 1924: 707–723.Google Scholar
  44. Reiss, K. Z. (1996). Evolution of the feeding apparatus in ant-eating mammals: When do we stop believing in convergence? Am. Zool. 36(5): 85A.Google Scholar
  45. Reiss, K. Z. (1997). Myology of the feeding apparatus of myrmecophagid anteaters (Xenarthra: Myrmecophagidae). J. Mammal. Evol. 4: 87–117.Google Scholar
  46. Rose, K. D. (1979). A new Paleocene palaeanodont and the origin of the Metacheiromyidae (Mammalia). Breviora Mus. Comp. Zool. 455: 1–14.Google Scholar
  47. Rose, K. D., and Emry, R. J. (1993). Relationships of Xenarthra, Pholidota, and fossil “edentates.” In: Mammal Phylogeny: Placentals, F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds., pp. 81–102, Springer-Verlag, New York.Google Scholar
  48. Sarich, V. M. (1985). Xenarthran systematics: albumin immunological evidence. In: The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas, G. G. Montgomery, ed., pp. 77–81, Smithsonian Institution Press, Washington, DC.Google Scholar
  49. Schlitter, D. A. (1993). Order Pholidota. In: Mammal Species of the World, D. E. Wilson and D. M. Reeder, eds., p. 415, Smithsonian Institution Press, Washington, DC.Google Scholar
  50. Schneider, R. (1955). Zur Entwicklung des Chondrocraniums der Gattung Bradypus. Gegenbaurs Morph. Jb. 95: 209–301.Google Scholar
  51. Segall, W. (1973). Characteristics of the ear, especially the middle ear in fossorial mammals, compared with those in the Manidae. Acta Anat. 86: 96–110.PubMedGoogle Scholar
  52. Simpson, G. G. (1931). Metacheiromys and the relationships of the Edentata. Bull. Am. Mus. Nat. Hist. 59: 295–381.Google Scholar
  53. Simpson, G. G. (1945). The principles of classification and a classification of mammals. Bull. Am. Mus. Nat. Hist. 85: 1–350.Google Scholar
  54. Spatz, W. B. (1966). Zur Ontogenese der Bulla tympanica von Tupaia glis Diard 1820 (Prosimiae, Tupaiiformes). Folia Primatol. 4: 26–50.PubMedGoogle Scholar
  55. Springer, M. S., Cleven, G. C., Madsen, O., de Jong, W. W., Waddell, V. G., Amrine, H. M., and Stanhope, M. J. (1997). Endemic African mammals shake the phylogenetic tree. Nature 388: 61–64.PubMedGoogle Scholar
  56. Starck, D. (1941). Zur Morphologie des Primordialkraniums von Manis javanica Desm. Gegenbaurs Morph. Jb. 86: 1–122.Google Scholar
  57. Storch, G. (1978). Eomanis waldi, ein Schuppentier aus dem Mittel-Eozän der “Grube Messel” bei Darmstadt (Mammalia: Pholidota). Senckenberg. lethaea 59: 503–529.Google Scholar
  58. Storch, G., and Martin, T. (1994). Ecomanis krebsi, ein neues Schuppentier aus dem Mittel-Eozän der Grube Messel bei Darmstadt (Mammalia: Pholidota). Berliner geowiss. Abh. E13: 83–97.Google Scholar
  59. Swofford, D. L. (1993). PAUP: Phylogenetic Analysis Using Parsimony, Version 3.1.1, Smithsonian Institution, Washington, DC.Google Scholar
  60. Szalay, F. S. (1977). Phylogenetic relationships and a classification of eutherian Mammalia. In: Major Patterns in Vertebrate Evolution, M. K. Hecht, P. C. Goody, and B. M. Hecht, eds., pp. 315–374, Plenum Press, New York.Google Scholar
  61. van Kampen, P. N. (1905). Die Tympanalgegend des Säugetiereschädels. Gegenbaurs Morph. Jb. 34: 321–722.Google Scholar
  62. van Kampen, P. N. (1915). De Phylogenie van het entotympanicum. Tijdschr. Ned. Dierkd. Ver. 14: xxiv.Google Scholar
  63. van der Klaauw, J. C. (1922). Über die Entwicklung des Entotympanicums. Tijdschr. Ned. Dierkd. Ver. 18: 135–174.Google Scholar
  64. van der Klaauw, J. C. (1931). On the auditory bulla in some fossil mammals. Bull. Am. Mus. Nat. Hist. 62: 1–352.Google Scholar
  65. Wible, J. R. (1984). The Ontogeny and Phylogeny of the Mammalian Cranial Arterial Pattern, Ph.D. dissertation, Duke University, Durham, NC.Google Scholar
  66. Wible, J. R. (1986). Transformations in the extracranial course of the internal carotid artery in mammalian phylogeny. J. Vert. Paleontol. 6: 313–325.Google Scholar
  67. Wible, J. R., and Martin, J. R. (1993). Ontogeny of the tympanic floor and roof in archontans. In: Primates and Their Relatives in Phylogenetic Perspective, R. D. E. MacPhee, ed., pp. 111–148, Plenum Press, New York.Google Scholar
  68. Wible, J. R., and Novacek, M. J. (1988). Cranial evidence for the monophyletic origin of bats. Am. Mus. Novitates 2911: 1–19.Google Scholar

Copyright information

© Plenum Publishing Corporation 1999

Authors and Affiliations

  1. 1.Department of Biological and Environmental SciencesUniversity of Tennessee at ChattanoogaChattanooga
  2. 2.Section of MammalsCarnegie Museum of Natural HistoryPittsburgh

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