Advertisement

Composition of the canid auditory bulla and a new look at the evolution of carnivoran entotympanics

  • Dmitry V. IvanoffEmail author
Original Article
  • 18 Downloads

Abstract

The higher carnivoran taxa significantly differ in the morphology of the auditory bulla, but little is known about its non-ectotympanic elements and their contribution to phylogenetically informative bullar characters. The ventral entotympanic sinus, a principal hypotympanic compartment unique to Canidae, expands in post-ossification ontogeny from a distinct portion, rather than the whole, of what is considered the ‘caudal entotympanic’. To trace the earlier development of this sinus and to clarify the potential roles of individual entotympanics in formation of the canid auditory bulla, osteological observations were made on younger skulls of Canis lupus and four additional species. The ventral entotympanic sinus was found to invariably originate at a separate bone provisionally designated the ventral entotympanic. The rest of the caudal entotympanic is a fusion of the posterior (or the proper) caudal entotympanic ossifying near the tympanohyal, and the anterior caudal entotympanic ossifying between the ectotympanic and rostral entotympanic. Examination of the rostral entotympanic also revealed previously unknown details. In sum, the canid auditory bulla includes at least four rather than earlier recognised two (or suspected three) entotympanics. Based on these findings, the composition of the canid intrabullar septum and the homologies of the carnivoran entotympanics are discussed. Within the established phylogenetic framework, the rostral entotympanic and posterior caudal entotympanic appear as plesiomorphic for crown-group Carnivora, while the anterior caudal entotympanic is synapomorphic for Caniformia, and the ventral entotympanic is autapomorphic for Cynoidea. This hypothesis implies that the carnivoran entotympanic patterns may have emerged before complete fusions of bullar bones observed in the fossil record.

Keywords

Mammalia Carnivora Canidae Osteology Ear region Postnatal development 

Notes

Acknowledgements

I am grateful to Gennady Baryshnikov (ZIN), Barbara Herzig-Straschil (NMW) and Sergei Kruskop (ZMMU) for granting access to the specimens examined in this study, and to Cathrin Pfaff and two anonymous reviewers for constructive comments on the manuscript.

Compliance with ethical standards

Conflict of interest

The author declares that he has no conflict of interest.

Ethical approval

No animals were killed or harmed specifically for this study.

References

  1. Becker, A. (1923). Das postembryonale Wachstum des deutschen Schäferhundschädels. Archiv für Naturgeschichte, Abteilung A, 89(9), 131–197.Google Scholar
  2. De Bonis, L., Peigné, S., Guy, F., Likius, A., Makaye, H. T., Vignaud, P., & Brunet, M. (2009). A new mellivorine (Carnivora, Mustelidae) from the Late Miocene of Toros Menalla, Chad. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen, 252, 33–54.  https://doi.org/10.1127/0077-7749/2009/0252-0033.CrossRefGoogle Scholar
  3. Doronina, L., Churakov, G., Shi, J., Brosius, J., Baertsch, R., Clawson, H., & Schmitz, J. (2015). Exploring massive incomplete lineage sorting in arctoids (Laurasiatheria, Carnivora). Molecular Biology and Evolution, 32, 3194–3204.  https://doi.org/10.1093/molbev/msv188.Google Scholar
  4. Drews, M. (1934). Über Ossifikationsvorgänge am Katzen-und Hundeschädel. Gegenbaurs Morphologisches Jahrbuch, 73, 185–237.Google Scholar
  5. Eizirik, E., Murphy, W. J., Koepfli, K.-P., Johnson, W. E., Dragoo, J. W., Wayne, R. K., & O’Brien, S. J. (2010). Pattern and timing of diversification of the mammalian order Carnivora inferred from multiple nuclear gene sequences. Molecular Phylogenetics and Evolution, 56, 49–63.  https://doi.org/10.1016/j.ympev.2010.01.033.CrossRefGoogle Scholar
  6. Evans, H. E., & De Lahunta, A. (2013). Miller’s anatomy of the dog (4th ed.). St Louis: Elsevier.Google Scholar
  7. Fischer, M. S. (1989). Zur Ontogenese der Tympanalregion der Procaviidae (Mammalia: Hyracoidea). Gegenbaurs Morphologisches Jahrbuch, 135, 795–840.Google Scholar
  8. Flower, W. H. (1869). On the value of the characters of the base of the cranium in the classification of the order Carnivora, and on the systematic position of Bassaris and other disputed forms. Proceedings of the Zoological Society of London, 1869, 4–37.  https://doi.org/10.1111/j.1469-7998.1869.tb07286.x
  9. Flower, W. H. (1885). An introduction to the osteology of the Mammalia (3rd ed.). London: Macmillan.  https://doi.org/10.5962/bhl.title.996.Google Scholar
  10. Flynn, J. J., & Galiano, H. (1982). Phylogeny of early Tertiary Carnivora, with a description of a new species of Protictis from the Middle Eocene of northwestern Wyoming. American Museum Novitates, 2725, 1–64.Google Scholar
  11. Flynn, J. J., & Nedbal, M. A. (1998). Phylogeny of the Carnivora (Mammalia): Congruence vs incompatibility among multiple data sets. Molecular Phylogenetics and Evolution, 9, 414–426.  https://doi.org/10.1006/mpev.1998.0504.CrossRefGoogle Scholar
  12. Flynn, J. J., & Wesley-Hunt, G. D. (2005). Carnivora. In K. D. Rose & J. D. Archibald (Eds.), The rise of placental mammals: Origins and relationships of the major extant clades (pp. 175–198). Baltimore: Johns Hopkins University Press.Google Scholar
  13. Flynn, J. J., Neff, N. A., & Tedford, R. H. (1988). Phylogeny of the Carnivora. In M. J. Benton (Ed.), Phylogeny and classification of the tetrapods. Vol. 2: Mammals (pp. 73–116). Oxford: Clarendon Press.Google Scholar
  14. Flynn, J. J., Finarelli, J. A., Zehr, S., Hsu, J., & Nedbal, M. A. (2005). Molecular phylogeny of the Carnivora (Mammalia): Assessing the impact of increased sampling on resolving enigmatic relationships. Systematic Biology, 54, 317–337.  https://doi.org/10.1080/10635150590923326.CrossRefGoogle Scholar
  15. Flynn, J. J., Finarelli, J. A., & Spaulding, M. (2010). Phylogeny of the Carnivora and Carnivoramorpha, and the use of the fossil record to enhance understanding of evolutionary transformations. In A. Goswami & A. Friscia (Eds.), Carnivoran evolution: New views on phylogeny, form, and function (pp. 25–63). Cambridge: Cambridge University Press.  https://doi.org/10.1017/CBO9781139193436.003.CrossRefGoogle Scholar
  16. Gaudin, T. J., & Wible, J. R. (1999). The entotympanic of pangolins and the phylogeny of the Pholidota (Mammalia). Journal of Mammalian Evolution, 6, 39–65.  https://doi.org/10.1023/A:1020538313412.CrossRefGoogle Scholar
  17. Gregory, W. K., & Hellman, M. (1939). On the evolution and major classification of the civets (Viverridae) and allied fossil and recent Carnivora: A phylogenetic study of the skull and dentition. Proceedings of the American Philosophical Society, 81, 309–392.Google Scholar
  18. Hough, J. R. (1948). The auditory region in some members of the Procyonidae, Canidae and Ursidae: Its significance in the phylogeny of the Carnivora. Bulletin of the American Museum of Natural History, 92, 67–118.Google Scholar
  19. Hough, J. R. (1953). Auditory region in North American fossil Felidae: Its significance in phylogeny. United States Geological Survey Professional Papers, 243-G, 95–115.Google Scholar
  20. Hunt, R. M., Jr. (1974). The auditory bulla in Carnivora: An anatomical basis for reappraisal of carnivore evolution. Journal of Morphology, 143, 21–76.  https://doi.org/10.1002/jmor.1051430103.CrossRefGoogle Scholar
  21. Hunt, R. M., Jr. (1987). Evolution of the aeluroid Carnivora: Significance of auditory structure in the nimravid cat Dinictis. American Museum Novitates, 2886, 1–74.Google Scholar
  22. Hunt, R. M., Jr. (1991). Evolution of the aeluroid Carnivora: Viverrid affinities of the Miocene carnivoran Herpestides. American Museum Novitates, 3023, 1–34.Google Scholar
  23. Hunt, R. M., Jr. (1998). Evolution of the aeluroid Carnivora: Diversity of the earliest aeluroids from Eurasia (Quercy, Hsanda-Gol) and the origin of felids. American Museum Novitates, 3252, 1–65.Google Scholar
  24. Hunt, R. M., Jr. (2001). Basicranial anatomy of the living linsangs Prionodon and Poiana (Mammalia, Carnivora, Viverridae), with comments on the early evolution of aeluroid carnivorans. American Museum Novitates, 3330, 1–24.  https://doi.org/10.1206/0003-0082(2001)330<0001:BAOTLL>2.0.CO;2.CrossRefGoogle Scholar
  25. Hunt, R. M., Jr. (2011). Evolution of large carnivores during the Mid-Cenozoic of North America: The temnocyonine radiation (Mammalia, Amphicyonidae). Bulletin of the American Museum of Natural History, 358, 1–153.  https://doi.org/10.1206/358.1.CrossRefGoogle Scholar
  26. Hunt, R. M., Jr., & Tedford, R. H. (1993). Phylogenetic relationships within the aeluroid Carnivora and implications of their temporal and geographic distribution. In F. S. Szalay, M. J. Novacek, & M. C. McKenna (Eds.), Mammal phylogeny. Vol. 2: Placentals (pp. 53–73). New York: Springer-Verlag.CrossRefGoogle Scholar
  27. International Committee on Veterinary Gross Anatomical Nomenclature. (2017). Nomina anatomica veterinaria (6th ed.). Hannover: NAV Editorial Committee.Google Scholar
  28. Ivanoff, D. V. (2000). Origin of the septum in the canid auditory bulla: Evidence from morphogenesis. Acta Theriologica, 45, 253–270.  https://doi.org/10.4098/AT.arch.00-27.CrossRefGoogle Scholar
  29. Ivanoff, D. V. (2001). Partitions in the carnivoran auditory bulla: Their formation and significance for systematics. Mammal Review, 31, 1–16.  https://doi.org/10.1046/j.1365-2907.2001.00069.x.CrossRefGoogle Scholar
  30. Ivanoff, D. V. (2007). Unlocking the ring: Occurrence and development of the uninterrupted intrabullar septum in Canidae. Mammalian Biology, 72, 145–162.  https://doi.org/10.1016/j.mambio.2006.04.007.CrossRefGoogle Scholar
  31. Joeckel, R. M., Peigné, S., Hunt, R. M., Jr., & Skolnick, R. I. (2002). The auditory region and nasal cavity of Oligocene Nimravidae (Mammalia: Carnivora). Journal of Vertebrate Paleontology, 22, 830–847. https://doi.org/10.1671/0272-4634(2002)022[0830:TARANC]2.0.CO;2.Google Scholar
  32. Lombaard, L. J. (1971). Age determination and growth curves in the black-backed jackal, Canis mesomelas Schreber, 1775 (Carnivora: Canidae). Annals of the Transvaal Museum, 27, 135–169.Google Scholar
  33. MacPhee, R. D. E. (1979). Entotympanics, ontogeny and primates. Folia Primatologica, 31, 23–47.  https://doi.org/10.1159/000155872.CrossRefGoogle Scholar
  34. MacPhee, R. D. E. (1981). Auditory regions of primates and eutherian insectivores: Morphology, ontogeny, and character analysis. Contributions to Primatology, 18, 1–284.Google Scholar
  35. MacPhee, R. D. E. (2014). The serrialis bone, interparietals, ‘X’ elements, entotympanics, and the composition of the notoungulate caudal cranium. Bulletin of the American Museum of Natural History, 384, 1–69.  https://doi.org/10.1206/384.1.CrossRefGoogle Scholar
  36. Maier, W., Tröscher, A., & Ruf, I. (2013). The entotympanic of Equus caballus (Perissodactyla, Mammalia). Mammalian Biology, 78, 231–234.  https://doi.org/10.1016/j.mambio.2012.05.002.CrossRefGoogle Scholar
  37. Moore, W. J. (1981). The mammalian skull. Cambridge: Cambridge University Press.Google Scholar
  38. Novacek, M. J. (1977). Aspects of the problem of variation, origin and evolution of the eutherian auditory bulla. Mammal Review, 7, 131–150.  https://doi.org/10.1111/j.1365-2907.1977.tb00366.x.CrossRefGoogle Scholar
  39. Novacek, M. J. (1993). Patterns of diversity in the mammalian skull. In J. Hanken & B. K. Hall (Eds.), The skull. Vol. 2: Patterns of structural and systematic diversity (pp. 438–545). Chicago: University of Chicago Press.Google Scholar
  40. Nyakatura, K., & Bininda-Emonds, O. R. P. (2012). Updating the evolutionary history of Carnivora (Mammalia): A new species-level supertree complete with divergence time estimates. BMC Biology, 10(12).  https://doi.org/10.1186/1741-7007-10-12.
  41. Owen, P. R. (2006). Description of a new late Miocene American badger (Taxidiinae) utilizing high-resolution X-ray computed tomography. Palaeontology, 49, 999–1011.  https://doi.org/10.1111/j.1475-4983.2006.00590.x.CrossRefGoogle Scholar
  42. Peigné, S., & De Bonis, L. (1999). The genus Stenoplesictis Filhol (Mammalia, Carnivora) from the Oligocene deposits of the Phosphorites of Quercy, France. Journal of Vertebrate Paleontology, 19, 566–575.  https://doi.org/10.1080/02724634.1999.10011165.CrossRefGoogle Scholar
  43. Peigné, S., & De Bonis, L. (2003). Juvenile cranial anatomy of Nimravidae (Mammalia, Carnivora): Biological and phylogenetic implications. Zoological Journal of the Linnean Society, 138, 477–493.  https://doi.org/10.1046/j.1096-3642.2003.00066.x.CrossRefGoogle Scholar
  44. Petter, G. (1966). Cynodictis, Canidé Oligocène d'Europe: Région tympanique et affinités. Annales de Paléontologie (Vertébrés), 52, 3–19.Google Scholar
  45. Pfaff, C., Martin, T., & Ruf, I. (2015). ‘Septal compass’ and ‘septal formula’: A new method for phylogenetic investigations of the middle ear region in the squirrel-related clade (Rodentia: Mammalia). Organisms Diversity & Evolution, 15, 721–730.  https://doi.org/10.1007/s13127-015-0222-x.CrossRefGoogle Scholar
  46. Pocock, R. I. (1921). The auditory bulla and other cranial characters in the Mustelidae. Proceedings of the Zoological Society of London, 1921, 473–486.  https://doi.org/10.1111/j.1096-3642.1921.tb03274.x.Google Scholar
  47. Presley, R. (1993a). Development and the phylogenetic features of the middle ear region. In F. S. Szalay, M. J. Novacek, & M. C. McKenna (Eds.), Mammal phylogeny. Vol. 1: Mesozoic differentiation, multituberculates, monotremes, early eutherians, and marsupials (pp. 21–29). New York: Springer-Verlag.CrossRefGoogle Scholar
  48. Presley, R. (1993b). Preconception of adult structural pattern in the analysis of the developing skull. In J. Hanken & B. K. Hall (Eds.), The skull. Vol. 1: Development (pp. 347–377). Chicago: University of Chicago Press.Google Scholar
  49. Prevosti, F. J. (2010). Phylogeny of the large extinct South American canids (Mammalia, Carnivora, Canidae) using a ‘total evidence’ approach. Cladistics, 26, 456–481.  https://doi.org/10.1111/j.1096-0031.2009.00298.x.CrossRefGoogle Scholar
  50. Rozen-Rechels, D., Peigné, S., Germain, D., & Ladevèze, S. (2016). Intraspecific morphological variation of the middle ear in the European badger, Meles meles (Carnivora: Mustelidae). Biological Journal of the Linnean Society, 119, 106–116.  https://doi.org/10.1111/bij.12800.CrossRefGoogle Scholar
  51. Sato, J. J., Wolsan, M., Minami, S., Hosoda, T., Sinaga, M. H., Hiyama, K., Yamaguchi, Y., & Suzuki, H. (2009). Deciphering and dating the red panda’s ancestry and early adaptive radiation of Musteloidea. Molecular Phylogenetics and Evolution, 53, 907–922.  https://doi.org/10.1016/j.ympev.2009.08.019.CrossRefGoogle Scholar
  52. Schliemann, H. (1966). Zur Morphologie und Entwicklung des Craniums von Canis lupus f. familiaris L. Gegenbaurs Morphologisches Jahrbuch, 109, 501–603.Google Scholar
  53. Schmitt, F. (1903). Ueber das postembryonale Wachstum des Schädels verschiedener Hunderassen. Archiv für Naturgeschichte, 69(1), 69–134.Google Scholar
  54. Starck, D. (1964). Über das Entotympanicum der Canidae und Ursidae (Mammalia, Carnivora, Fissipedia). Acta Theriologica, 8, 181–188.  https://doi.org/10.4098/AT.arch.64-11.CrossRefGoogle Scholar
  55. Takada, Y., Izumi, M., & Gotoh, K. (2009). Comparative anatomy of the hyoid apparatus of carnivores. Mammal Study, 34, 213–218.  https://doi.org/10.3106/041.034.0406.CrossRefGoogle Scholar
  56. Tomiya, S. (2011). A new basal caniform (Mammalia: Carnivora) from the Middle Eocene of North America and remarks on the phylogeny of early carnivorans. PLoS One, 6(9), e24146.  https://doi.org/10.1371/journal.pone.0024146.CrossRefGoogle Scholar
  57. Tomiya, S. (2013). New carnivoraforms (Mammalia) from the middle Eocene of California, USA, and comments on the taxonomic status of ‘Miacisgracilis. Palaeontologia Electronica, 16(2), 14A.  https://doi.org/10.26879/364.Google Scholar
  58. Van der Klaauw, C. J. (1922). Über die Entwickelung des Entotympanicums. Tijdschrift der Nederlandsche Dierkundige Vereeniging, Serie 2(18), 135–176.Google Scholar
  59. Van der Klaauw, C. J. (1931). On the auditory bulla in some fossil mammals, with a general introduction to this region of the skull. Bulletin of the American Museum of Natural History, 62, 1–352.Google Scholar
  60. Van Kampen, P. N. (1905). Die Tympanalgegend des Säugetierschädels. Gegenbaurs Morphologisches Jahrbuch, 34, 321–722.  https://doi.org/10.5962/bhl.title.15705.Google Scholar
  61. Wang, X., & Tedford, R. H. (1994). Basicranial anatomy and phylogeny of primitive canids and closely related miacids (Carnivora: Mammalia). American Museum Novitates, 3092, 1–34.Google Scholar
  62. Wang, X., McKenna, M. C., & Dashzeveg, D. (2005). Amphicticeps and Amphicynodon (Arctoidea, Carnivora) from Hsanda Gol Formation, central Mongolia, and phylogeny of basal arctoids with comments on zoogeography. American Museum Novitates, 3483, 1–57. https://doi.org/10.1206/0003-0082(2005)483[0001:AAAACF]2.0.CO;2.Google Scholar
  63. Wegner, R. N. (1942). Die Paukeninnenbeine (Endotympanicum und Epipterygoid) bei den Säugetieren. Photographie und Forschung, 3, 289–303.Google Scholar
  64. Wesley, G. D., & Flynn, J. J. (2003). A revision of Tapocyon (Carnivoramorpha), including analysis of the first cranial specimens and identification of a new species. Journal of Paleontology, 77, 769–783.  https://doi.org/10.1666/0022-3360(2003)077%3C0769:AROTCI%3E2.0.CO;2.CrossRefGoogle Scholar
  65. Wesley-Hunt, G. D., & Flynn, J. J. (2005). Phylogeny of the Carnivora: Basal relationships among the carnivoramorphans, and assessment of the position of ‘Miacoidea’ relative to Carnivora. Journal of Systematic Palaeontology, 3, 1–28.  https://doi.org/10.1017/S1477201904001518.CrossRefGoogle Scholar
  66. Wesley-Hunt, G. D., & Werdelin, L. (2005). Basicranial morphology and phylogenetic position of the upper Eocene carnivoramorphan Quercygale. Acta Palaeontologica Polonica, 50, 837–846.Google Scholar
  67. Wible, J. R. (1984). The ontogeny and phylogeny of the mammalian cranial arterial pattern. Ph.D. dissertation, Duke University, Durham.Google Scholar
  68. Wible, J. R. (2010). Petrosal anatomy of the nine-banded armadillo, Dasypus novemcinctus Linnaeus, 1758 (Mammalia, Xenarthra, Dasypodidae). Annals of Carnegie Museum, 79, 1–28.  https://doi.org/10.2992/007.079.0101.CrossRefGoogle Scholar
  69. Wible, J. R., & Davis, D. L. (2000). Ontogeny of the chiropteran basicranium, with reference to the Indian false vampire bat, Megaderma lyra. In R. A. Adams & S. C. Pedersen (Eds.), Ontogeny, functional ecology, and evolution of bats (pp. 214–246). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  70. Wible, J. R., & Novacek, M. J. (1988). Cranial evidence for the monophyletic origin of bats. American Museum Novitates, 2911, 1–19.Google Scholar
  71. Wible, J. R., & Spaulding, M. (2013). On the cranial osteology of the African palm civet, Nandinia binotata (Gray, 1830) (Mammalia, Carnivora, Feliformia). Annals of Carnegie Museum, 82, 1–114.  https://doi.org/10.2992/007.082.0101.CrossRefGoogle Scholar
  72. Wińcza, H. (1896). Über einige Entwickelungsveränderungen in der Gegend des Schädelgrundes bei den Säugethieren. Bulletin International de l’Académie des Sciénces de Cracovie, 1896, 326–337.Google Scholar
  73. Wińcza, H. (1898). O niektórych zmianach podczas rozwoju osady głowy u zwierząt ssących. Rozprawy Akademii Umiejętności, Wydział Matematyczno-Przyrodniczy, Serya 2(13), 10–26.Google Scholar
  74. Winge, H. (1941). The interrelationships of the mammalian genera. Vol. 2: Rodentia, Carnivora, Primates. Copenhagen: CA Reitzels Forlag.Google Scholar
  75. Wyss, A. R., & Flynn, J. J. (1993). A phylogenetic analysis and definition of the Carnivora. In F. S. Szalay, M. J. Novacek, & M. C. McKenna (Eds.), Mammal phylogeny. Vol. 2: Placentals (pp. 32–52). New York: Springer-Verlag.CrossRefGoogle Scholar
  76. Yu, L., Li, Q.-W., Ryder, O. A., & Zhang, Y.-P. (2004). Phylogenetic relationships within mammalian order Carnivora indicated by sequences of two nuclear DNA genes. Molecular Phylogenetics and Evolution, 33, 694–705.  https://doi.org/10.1016/j.ympev.2004.08.001.CrossRefGoogle Scholar
  77. Yudin, V. G. (1989). The dental system of Canis lupus (Carnivora, Canidae) from the Far East of the USSR. Zoologichesky Zhurnal, 68, 115–123. (in Russian).Google Scholar
  78. Zeller, U. A. (1986). Ontogeny and cranial morphology of the tympanic region of the Tupaiidae, with special reference to Ptilocercus. Folia Primatologica, 47, 61–80.  https://doi.org/10.1159/000156266.CrossRefGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2019

Authors and Affiliations

  1. 1.Department of Palaeontology, National Museum of Natural HistoryNational Academy of Sciences of UkraineKievUkraine

Personalised recommendations