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Morphological Specificity of the Auditory Capsule of Sciurid (Sciuridae, Rodentia)

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Abstract—

Specific features of the sciurid auditory capsule have been analyzed based on 63 species from 20 genera. Its morphological specificity is characterized by a peculiar combination of primitive and advanced features stable within the group. They are (1) a rounded and inflated bulla with internal septa and a primitive attachment of the tympanic ring to the inner tympanic wall; (2) a transverse position of the bulla relative to the axis of the promontorium, resulting in the presence of deep petrosal fossae in front of and above the promontorium which are not covered by the tympanic bone; (3) a fully formed osseus facial canal and a developed bone tube of the stapedial artery; (4) the presence of a meato-cochlear bridge connecting the promontorium to the posterior wall of the acoustic duct which, in a fully developed form, does not occur in any other recent rodents; (5) pneumatization of the mastoid due to the expanding of the epitympanic chamber both anteriorly and posteriorly, with the formation of a premeatal pocket and a large epitympano-mastoid chamber divided into parts. The sciurid auditory capsule can generally be considered as morphologically advanced. Its diversity within the family concerns functionally significant features and is manifested in the structure of the external acoustic meatus, the size of the tympanic membrane, the length of the processes of auditory ossicles, and, most importantly, the degree of pneumatization of the auditory capsule. This is associated with quantitative variations of the characters and does not affect its structural plan, as a rule.

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REFERENCES

  1. Alexander, R.M., Animals Mechanics, London: Sidgwick and Jackson, 1968.

    Google Scholar 

  2. Argyle, E.C. and Mason, M.J., Middle ear structures of Octodon degus (Rodentia: Octodontidae), in comparison with those of subterranean caviomorphs, J. Mammal., 2008, vol. 89, pp. 1447–1455.

    Article  Google Scholar 

  3. Blanga-Kanfi, S., Miranda, H., Penn, O., Pupko, T., DeBry, R.W., and Huchon, D., Rodent phylogeny revised: analysis of six nuclear genes from all major rodent clades, BMC Evol. Biol., 2009, vol. 9, no. 1, p. 71. https://doi.org/10.1186/1471-2148-9-71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Churakov, G., Sadasivuni, M.K., Rosenbloom, K.R., Huchon, D., Brosius, J., and Schmitz, J., Rodent evolution: back to the root, Mol. Biol. Evol., 2010, vol. 27, no. 6, pp. 1315–1326.

    Article  CAS  Google Scholar 

  5. Farr, M.R.B. and Mason, M.J., Middle ear morphology in dormice (Rodentia: Gliridae), Mamm. Biol., 2008, vol. 73, no. 4, pp. 330–334. https://doi.org/10.1016/j.mambio.2007.02.010

    Article  Google Scholar 

  6. Goodrich, E.S., Studies on the Structure and Development of Vertebrates, London: McMillan, 1930.

    Book  Google Scholar 

  7. Han, G., Mao, F., Bi, S., Wang, Y., and Meng, J., A Jurassic gliding euharamiyidan mammal with an ear of five auditory bones, Nature, 2017. https://doi.org/10.1038/nature24483

    Article  CAS  Google Scholar 

  8. Hunt, R.M., Jr., The auditory bulla in Carnivora: an anatomical basis for reappraisal of carnivore evolution, J. Morphol., 1974, vol. 143, no. 1, pp. 21–76.

    Article  Google Scholar 

  9. Hunt, R.M., Jr., Evolution of the aeluroid canivora: significance of auditory structure in the nimravid cat Dinictis,Am. Mus. Novit., 1987, no. 2886, pp. 1–74.

  10. Jansa, S.A. and Weksler, M., Phylogeny of muroid rodents: relationships within and among major lineages as determined by IRBP gene sequences, Mol. Phylogenet. Evol., 2004, vol. 31, no. 1, pp. 256–276.

    Article  CAS  Google Scholar 

  11. Jones, G.M. and Spells, K.E., A theoretical and comparative study of the functional dependence of the semicircular canal upon its physical dimensions, Proc. R. Soc. London, Ser. B: Biol. Sci., 1962, vol. 157, no. 968, pp. 403–419. https://doi.org/10.1098/rspb.1963.0019

  12. Lange, S., Stalleicken, J., and Burda, H., Functional morphology of the ear in fossorial rodents, Microtus arvalis and Arvicola terrestris,J. Morphol., 2004, vol. 262, no. 3, pp. 770–779. https://doi.org/10.1002/jmor.10277

    Article  PubMed  Google Scholar 

  13. Lavocat, R.R.M. and Parent, J.-P., Phylogenetic analysis of middle ear feature in fossil and living rodents, in Evolutionary Relationships among Rodents: A Multidisciplinary Analysis, Luckett, W. P. and Hartenberger, J.-L., Eds., NATO ASI Series A: Life Sciences, New York: Plenum Press, 1985, vol. 92, pp. 333–354.

    Chapter  Google Scholar 

  14. Lay, D.M., The anatomy, physiology, functional significance and evolution of specialized hearing organs of gerbilline rodents, J. Morphol., 1972, vol. 138, no. 1, pp. 41–120.

    Article  CAS  Google Scholar 

  15. Mammal Species of the World: A Taxonomic and Geographic Reference, Wilson, D.E. and Reeder, D.M., Eds., Baltimore: Johns Hopkins Univ. Press, 2005, 3rd ed., pp. 894–1531.

    Google Scholar 

  16. Mason, M.J., Middle ear structures in fossorial mammals: a comparison with non-fossorial species, J. Zool., 2001, vol. 255, pp. 467–486.

    Article  Google Scholar 

  17. Mason, M.J., The middle ear apparatus of the tuco-tuco Ctenomys sociabilis (Rodentia, Ctenomyidae), J. Mamm., 2004, vol. 85, no. 4, pp. 797–805.

    Article  Google Scholar 

  18. Mason, M.J., Of mice, moles and guinea-pigs: functional morphology of the middle ear in living mammals, Hear. Res., 2012, vol. 301. https://doi.org/10.1016/j.heares.2012.10.004

    Article  Google Scholar 

  19. Mason, M.J., Structure and function of the mammalian middle ear. II: Inferring function from structure, J. Anat., 2016, vol. 228, pp. 300–312. https://doi.org/10.1111/joa.1231626100915

    Article  PubMed  Google Scholar 

  20. Mason, M.J., Lai, F.W.S., Li, J.-G., and Nevo, E., Middle ear structure and bone conduction in Spalax, Eospalax and Tachyoryctes mole-rats (Rodentia: Spalacidae), J. Morphol., 2010, vol. 271, p. 462–472. PMID: 19941379. https://doi.org/10.1002/jmor.10810.

  21. Mason, M.J., Willi, U.B., and Narins, P.M., Comments on “Tympanic-membrane and malleus-incus-complex co-adaptations for high-frequency hearing in mammals,” by Sunil Puria and Charles Steele, Hear. Res., 2010a, vol. 267, pp. 1–3. https://doi.org/10.1016/j.heares.2010.04.010

    Article  PubMed  Google Scholar 

  22. Mason, M.J., Cornwall, H.L., and Smith, E.St.J., Ear structures of the naked mole-rat, Heterocephalus glaber, and its relatives (Rodentia: Bathyergidae), PLoS One, 2016, vol. 11, no. 12. e0167079. https://doi.org/10.1371/journal.pone.0167079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Meng, J., The auditory region of Reithroparamys delicatissimus (Mammalia, Rodentia) and its systematic implications, Am. Mus. Novit., 1990, no. 2972, pp. 1–36.

  24. Moore, W.J., The Mammalian Skull, London: Cambridge Univ. Press, 1981.

    Google Scholar 

  25. Parent, J.-P., Recherche sur l’oreille moyenne des Rongeurs actuels et fossiles, Mèmoires et Travail ècole Pratique des Hautes ètudes,Institut de Montpellier, 1980, vol. 11.

    Google Scholar 

  26. Pavlinov, I.Ya., Evolution and taxonomic significance of the bone middle ear structure in the gerbil subfamily Gerbillinae (Rodentia: Cricetidae), Byull. Mosk. O-va Ispyt. Prir.,Otd. Biol., 1980, vol. 85, no. 4, pp. 20–33.

    Google Scholar 

  27. Pavlinov, I.Ya., Evolution of the mastoid part of the auditory drum in desert rodents, Zool. Zh., 1988, vol. 67, no. 5, pp. 739–750.

    Google Scholar 

  28. Pavlinov, I.Ya., Sistematika sovremennykh mlekopitayushchikh (Systematics of Modern Mammals), Moscow: Mosk. Univ., 2006, 2nd ed.

  29. Pavlinov, I.Ya., A Review of Phylogeny and Classification of Gerbillinae (Mammalia: Rodentia), Zool. Issled., Moscow: Mosk. Univ., 2008, no. 9.

  30. Pavlinov, I.Ya., Dubrovskii, Yu.A., Rossolimo, O.L., and Potapova, E.G., Peschanki mirovoi fauny (Gerbils of the World Fauna), Moscow: Nauka, 1990.

  31. Pfaff, C., Martin, T., and Ruf, I., “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 Evol., 2015, vol. 15, pp. 721–730. https://doi.org/10.1007/s13127-015-0222-x

    Article  Google Scholar 

  32. Pfaff, C., Martin, T., and Ruf, I., Bony labyrinth morphometry indicates locomotor adaptations in the squirrel-related clade (Rodentia, Mammalia), Proc. R. Soc. London, Ser. B: Biol. Sci., 2015a, vol. 282, no. 1809. https://doi.org/10.1098/rspb.2015.0744

    Article  Google Scholar 

  33. Potapova, E.G., Pathways of the transformation of the middle ear bone in Dipodoidea (Rodentia), Zool. Zh., 1998, vol. 77, no. 1, pp. 80–87.

    Google Scholar 

  34. Potapova, E.G., Morphological patterns and evolutionary pathways of the middle ear in dormice (Gliridae, Rodentia), Trakya Univ. J. Sci. Res. Ser. B: Nat. Appl. Sci., 2001, vol. 2, no. 2, pp. 159–170.

    Google Scholar 

  35. Potapova, E.G., Phylogenetic relationships of Palearctic Cricetinae (Rodentia, Muroidea) based on the structure of the auditory bulla, in Sistematika, paleontologiya i filogeniya gryzunov (Systematics, Paleontology, and Phylogeny of Rodents), Abramson, N.I. and Averianov, A.O., Eds., Tr. Zool. Inst. Ross. Akad. Nauk, St. Petersburg, 2005, vol. 306, pp. 116–141.

  36. Potapova, E.G., Intraspecific variability of the auditory capsule of the forest dormouse (Rodentia, Gliridae) in the Caucasus region, in Materialy mezhdunarodnoi konferentsii “Mlekopitayushchie gornykh territorii,” 18–23 avgusta 2007 (Proc. Int. Conf. “Mammals of Mountainous Territories,” August 18–23, 2007), Rozhnov, V.V. and Tembotova, F.A., Eds., Moscow: KMK, 2007, pp. 249–255.

  37. Potapova, E.G., Morpho-biological approach in phylogenetics (opportunities and limitations), in Sovremennye problemy biologicheskoi sistematiki (Current Problems of Biological Systematics), Alimov, A.F. and Stepan’yants, S.D., Eds., Tr. Zool. Inst. Ross. Akad. Nauk, Appendix 2, St. Petersburg: Tov. Nauch. Izd. KMK, 2013, pp. 53–65.

  38. Potapova, E.G., Selection of traits for the reconstruction of phylogeny on the analysis of mastoid pneumatization in gerbils (Gerbillidae, Rodentia) as an example, Vestn. Tver. Gos. Univ.,Ser. Biol. Ekol., 2014, vol. 31, no. 4, pp. 177–185.

    Google Scholar 

  39. Potapova, E.G., The diversity of mastoid pneumatization in gerbils of genera Taterillus and Gerbilliscus (Rodentia, Gerbillidae): morphogenetic and phylogenetic aspects, Sb. Tr. Zool. Muz. Mosk. Gos. Univ.im.M.V. Lomonosova, 2016, vol. 54, pp. 356–379.

    Google Scholar 

  40. Potapova, E.G. and Vorontsov, N.N., Taxonomic position of the genus Tachyoryctes and the relationships of families Rhizomyidae and Spalacidae (Rodentia: Mammalia), Zool. Zh., 2004, vol. 83, no. 8, pp. 1044–1058.

    Google Scholar 

  41. Rossolimo, O.L., Potapova, E.G., Pavlinov, I.Ya., Krupkop, S.V., and Voltsit, O.V., Soni (Myoxidae) mirovoi fauny (Dormice (Myoxidae) of the World), Moscow: Mosk. Univ., 2001.

  42. Schleich, E. and Busch, C., Functional morphology of the middle ear of Ctenomys talarum (Rodentia: Octodontidae), J. Mammal., vol. 85, no. 2, pp. 290–295. https://doi.org/10.1644/1545-1542(2004)085<0290: FMOTME>2.0.CO;2.

    Article  Google Scholar 

  43. Schutz, H., Jamniczky, H.A., Hallgrimsson, B., and Garland, T., Jr., Shape-shift: semicircular canal morphology responds to selective breeding for increased locomotor activity, Evolution, 2014, vol. 68, pp. 3184–3198. https://doi.org/10.1111/evo.12501

    Article  PubMed  Google Scholar 

  44. Simpson, G.G., The principles of classification and a classification of mammals, Bull. Am. Mus. Nat. Hist., 1945, vol. 85.

  45. Spoor, F., Bajpal, S., Hussain, S.T., Kumar, K., and Thewissen, J.G.M., Vestibular evidence for the evolution of aquatic behaviour in early cetaceans, Nature, 2002, no. 417, pp. 163–166. https://doi.org/10.1038/417163a

    Article  CAS  Google Scholar 

  46. Vedurmudi, A.P., Young, B.A., and van Hemmen, J.L., Internally coupled ears: mathematical structures and mechanisms underlying ice, Biol. Cybern., 2016, vol. 110, pp. 359–382. https://doi.org/10.1007/s00422-016-0696-4

    Article  PubMed  Google Scholar 

  47. Wahlert, J.H., Sawitzke, S.L., and Holden, M.E., Cranial anatomy and relationships of dormice (Rodentia, Myoxidae), Am. Mus. Novit., 1993, no. 3061, pp. 1–32.

  48. Webster, D.B., Ear structure and function in modern mammals, Am. Zool., 1966, vol. 6, pp. 451–466.

    Article  CAS  Google Scholar 

  49. Webster, D.B., Auditory systems of heteromyidae: postnatal development of the ear of Dipodomys merriami,J. Morphol., 1975, vol. 146, no. 2, pp. 377–394.

    Article  CAS  Google Scholar 

  50. Webster, D.B. and Webster, M., Auditory systems of Heteromyidae: functional morphology and evolution of the middle ear, J. Morphol., 1975, vol. 146, no. 2, pp. 343–376.

    Article  CAS  Google Scholar 

  51. Webster, D.B. and Webster, M., Morphological adaptations of the ear in the rodent family heteromyidae, Am. Zool., 1980, vol. 20, pp. 247–254.

    Article  Google Scholar 

  52. Yakhontov, E.L. and Potapova, E.G., The position of dormice Gliroidea in the system of rodents, in Voprosy sistematiki, faunistiki i paleontologii melkikh mlekopitayushchikh (Problems of Taxonomy, Zoogeography, and Paleontology of Small Mammals), Zaitsev, M.V., Ed., Tr. Zool. Inst. SSSR, Leningrad, 1993, vol. 243, pp. 127–147.

  53. Yang, A. and Hullar, T.E., Relationship of semicircular canal size to vestibular nerve afferent sensitivity in mammals, J. Neurophysiol., 2007, vol. 98, pp. 3197–3205. https://doi.org/10.1152/jn.00798.2007

    Article  PubMed  Google Scholar 

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ACKNOWLEDGMENTS

The author is grateful to the staff of the Zoological Museum of Moscow State University (Moscow) and the Zoological Institute of the Russian Academy of Sciences (St. Petersburg) for the opportunity to use the bone collections of these museums. The author is grateful to the staff of the Department of Zoology of Vertebrates, Moscow State University (L.P. Korzun, K.B. Gerasimov, and L.N. Skurat) for providing a workplace and the opportunity to work on a binocular Zeiss Stemi microscope with a drawing device and a digital camera.

This work was carried out using the equipment of the Joint Usage Center for Instrumental Analysis in Ecology, Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences.

Funding

This work was conducted within the framework of the project of the Federal Agency for Scientific Organizations (project no. 0120-1356-032) and was supported in part by the Russian Foundation or Basic Research (project no. 16-04-00294).

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  1. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 119071, Moscow, Russia

    E. G. Potapova

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Potapova, E.G. Morphological Specificity of the Auditory Capsule of Sciurid (Sciuridae, Rodentia). Biol Bull Russ Acad Sci 46, 730–743 (2019). https://doi.org/10.1134/S1062359019070094

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