|
Fallen in a dead ear: intralabyrinthine preservation of stapes in fossil artiodactyls
Keywords:
allometry; bony labyrinth; inner ear; middle ear ossicles
doi: 10.18563/pv.40.1.e3
Cite this article:
Orliac M. J., Billet G., 2016. Fallen in a dead ear: intralabyrinthine preservation of stapes in fossil artiodactyls. Palaeovertebrata 40 (1)-e3. doi: 10.18563/pv.40.1.e3
Export citation
Abstract
The stapes is the last of the middle ear ossicle chain and the smallest bone of the mammalian skeleton. Because it rests on the membrane of the fenestra vestibuli during life, the stapes may often fall within the bony labyrinth cavity when soft structures decay after death. In this work, we highlight the unexpected role that the bony labyrinth plays in the preservation of the stapes. Systematic investigation of the bony labyrinth of 50 petrosal bones of extinct and extant artiodactyls led to the discovery of eight cases of “intralabyrinthine” stapes. Three dimensional reconstructions of these stapes allow documenting stapes morphology of four extinct artiodactyl taxa: Microstonyx erymanthius (Suidae), Elomeryx borbonicus (Hippopotamoidea), ?Helohyus plicodon (Helohyidae), and an undetermined Cainotheriidae; and four extant ones Choeropsis and Hippopotamus (Hippopotamidae), and Tayassu and Phacochoerus (Suoidea). ?Helohyus plicodon from the Middle Eocene documents the oldest stapes known for the order Artiodactyla. Morphological study and metric analyses of our sample of artiodactylan stapes show that stapes are likely to carry relevant phylogenetic characters/signal within artiodactyls, and a potential Euungulata signature.
Published in Vol.40-1 (2016)
Bibliography
Allin, E. F., Hopson, J. A., 1992. Evolution of the auditory system in Synapsida ("mammal-like reptiles" and primitive mammals) as seen in the fossil record. In: Webster, D. B., Popper, A. N., Fay, R. R. (Eds), The evolutionary biology of hearing. Springer New York. pp. 587-614. http://dx.doi.org/10.1007/978-1-4612-2784-7
Alroy, J., 1998. Cope's Rule and the dynamics of body mass evolution in North American fossil mammals. Science 280, 731-734. http://dx.doi.org/10.1126/science.280.5364.731
Archibald, J. D., 1979. Oldest known eutherian stapes and a marsupial petrosal bone from the Late Cretaceous of North America. Nature 281, 669-670. http://dx.doi.org/10.1038/281669a0
Asher, R. J., Helgen, K. M., 2010. Nomenclature and placental mammal phylogeny. BMC Evolutionary Biology 10(1), 102. http://dx.doi.org/10.1186/1471-2148-10-102
Barklow, W. E., 2004. Amphibious communication with sound in hippos, Hippopotamus amphibius. Animal Behaviour 68, 1125–1132. http://dx.doi.org/10.1016/j.anbehav.2003.10.034
Benoit, J., E. M. Essid, W. Marzougui, H. Khayati Ammar, R. Lebrun, R. Tabuce, and L. Marivaux. 2013. New insights into the ear region anatomy and cranial blood supply of advanced stem Strepsirhini: evidence from three primate petrosals from the Eocene of Chambi, Tunisia. Journal of Human Evolution 65, 551-572. http://dx.doi.org/10.1016/j.jhevol.2013.06.014
Billet, G., Muizon, C., Schellhorn, R., Ruf, I., Ladevèze, S., Bergqvist, L. 2015. Petrosal and inner ear anatomy and allometry amongst specimens referred to Litopterna (Placentalia). Zoological Journal of the Linnean Society 173, 956-987. http://dx.doi.org/10.1111/zoj.12219
BiochroM'97 (collectif), 1997. Synthèses et Tableaux de corrélations. In: Aguilar, J.-P., Legendre, S., Michaux, J. (Eds.), Actes du Congrès BiochroM'97. Mémoires et Travaux de l'École Pratique des Hautes Études, Institut de Montpellier, Montpellier, pp. 769-805.
Blanco, R. E., Rinderknecht, A., 2012. Fossil evidence of frequency range of hearing independent of body size in South American Pleistocene ground sloths (Mammalia, Xenarthra). Comptes Rendus Palevol 11(8), 549-554. http://dx.doi.org/10.1016/j.crpv.2012.07.003
Crompton, A. W., Luo, Z., 1993. Relationships of the Liassic mammals Sinoconodon, Morganucodon oehleri, and Dinnetherium. In: S. Szalay, F., Novacek, M. J., McKenna, M. C. (Eds), Mammal Phylogeny. Springer New York, pp. 30-44. http://dx.doi.org/10.1007/978-1-4613-9249-1_4
Doran, A. H., 1878. XVIII. Morphology of the Mammalian Ossicula auditûs. Transactions of the Linnean Society of London. 2nd Series: Zoology 1(7), 371-497. http://dx.doi.org/10.1111/j.1096-3642.1878.tb00663.x
Ekdale, E. G., 2011. Morphological variation in the ear region of Pleistocene Elephantimorpha (Mammalia, Proboscidea) from central Texas. Journal of Morphology 272(4), 452-464. http://dx.doi.org/10.1002/jmor.10924
Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125, 1-15. http://dx.doi.org/10.1086/284325
Fleischer, G., 1973. Studien am Skelett des Gehörorgans der Säugetiere, einschließlich des Menschen. Säugetierkundliche Mitteilungen 21, 131–239.
Fortelius, M. (coordinator), 2013. New and Old Worlds Database of Fossil Mammals (NOW). University of Helsinki. Available at: http://www.helsinki.fi/science/now/
Gatesy, J., Geisler, J. H., Chang, J., Buell, C., Berta, A., Meredith, R. W., Springer, M. S., McGowen, M. R., 2013. A phylogenetic blueprint for a modern whale. Molecular Phylogenetics and Evolution, 66(2), 479-506. http://dx.doi.org/10.1016/j.ympev.2012.10.012
Gregory, W. K., 1920. On the structure and relations of Notharctus, an American Eocene primate. Memoirs of the AMNH 3, 45-243. Available at: http://hdl.handle.net/2246/5725
Gunz, P., Ramsier, M., Kuhrig, M., Hublin, J. J., Spoor, F., 2012. The mammalian bony labyrinth reconsidered, introducing a comprehensive geometric morphometric approach. Journal of Anatomy, 220(6), 529-543. http://dx.doi.org/10.1111/j.1469-7580.2012.01493.x
Guth, C., 1957. Le stapes de quelques édentés fossiles. Mammalia 21(2), 121-124. http://dx.doi.org/10.1515/mamm.1957.21.2.121
Guth, C., 1961. La région temporale des Édentés. Thèse de doctorat, Université de Paris, Imprimerie Jeanne d'Arc.
Hammer, Ø., Harper, D. A. T., Ryan, P. D. 2001 PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 9. Available at http://palaeo-electronica.org/2001_1/past/issue1_01.htm
Heffner, R. S., Heffner, H. E., 1990. Hearing in domestic pigs (Sus scrofa) and goats (Capra hircus). Hearing Research 48(3), 231-240. http://dx.doi.org/10.1016/0378-5955(90)90063-U
Heffner, R. S., Heffner, H. E., 1992. Evolution of sound localization in mammals. In: Webster, D. B., Popper, A. N., Fay, R. R. (Eds), The evolutionary biology of hearing. Springer, New York, pp. 691-715. http://dx.doi.org/10.1007/978-1-4612-2784-7_43
Heffner, R. S., Heffner, H. E., 2008. High-frequency hearing. In: Dallos, P., Oertel, D., Hoy, R., (Eds), Handbook of the senses: audition. Elsevier, New York, pp. 55-60. http://dx.doi.org/10.1016/b978-012370880-9.00004-9
Hemilä, S., Nummela, S., Reuter, T., 1995. What middle ear parameters tell about impedance matching and high frequency hearing. Hearing Research, 85(1), 31-44. http://dx.doi.org/10.1016/0378-5955(95)00031-X
Janis, C., 1990. Correlation of cranial and dental variables with body size in ungulates and macropodoids. In: Damuth, J., MacFadden, B. J., (Eds), Body size in mammalian paleobiology. Cambridge University Press, Cambridge, pp. 255-299.
Kermack, K.A., Mussett, F. Rigney, H. W., 1981. The skull of Morganucodon. Zoological Journal of the Linnean Society 71, 1-158. http://dx.doi.org/10.1111/j.1096-3642.1981.tb01127.x
Lancaster, W. C., 1990. The middle ear of the Archaeoceti. Journal of Vertebrate Paleontology 10(1), 117-127. http://dx.doi.org/10.1080/02724634.1990.10011795
Lillegraven, J. A., Krusat, G., 1991. Cranio-mandibular anatomy of Haldanodon exspectatus (Docodonta; Mammalia) from the Late Jurassic of Portugal and its implications to the evolution of mammalian characters. Rocky Mountain Geology 28(2), 39-138.
Luo, Z. X., Crompton, A. W., Sun, A. L., 2001. A new mammaliaform from the early Jurassic and evolution of mammalian characteristics. Science 292(5521), 1535-1540 http://dx.doi.org/10.1126/science.1058476
Luo, Z. X., 2011. Developmental patterns in Mesozoic evolution of mammal ears. Annual Review of Ecology, Evolution, and Systematics 42, 355-380. http://dx.doi.org/10.1146/annurev-ecolsys-032511-142302
Maddison, W. P., Maddison, D. R., 2009. Mesquite: a modular system for evolutionary analysis. Version 2.71. Available at: http://mesquiteproject.org
Martinez, J. N., Sudre, J., 1995. The astragalus of Paleogene artiodactyls: comparative morphology, variability and prediction of body mass. Lethaia 28(3), 197-209. http://dx.doi.org/10.1111/j.1502-3931.1995.tb01423.x
Mason, M. J., 2004. Functional morphology of the middle ear in Chlorotalpa golden moles (Mammalia, Chrysochloridae): predictions from three models. Journal of Morphology 261, 162-174. http://dx.doi.org/10.1002/jmor.10235
Meng, J., 1992. The stapes of Lambdopsalis bulla (Multituberculata) and transformational analyses on some stapedial features in Mammaliaformes. Journal of Vertebrate Paleontology 12(4), 459-471. http://dx.doi.org/10.1080/02724634.1992.10011474
Meng, J., Fox, R. C., 1995. Osseous inner ear structures and hearing in early marsupials and placentals. Zoological Journal of the Linnean Society 115(1), 47-71. http://dx.doi.org/10.1006/zjls.1995.0033
Miao D., Lillegraven, J. A., 1986. Discovery of three ear ossicles in a multituberculate mammal. National Geographic Research 2(4), 500-507.
Midford, P. E., Garland Jr, T., Maddison, W. P., 2008. PDAP package of Mesquite, version 1.14. Available at: http://mesquiteproject.org/pdap_mesquite/
Moggi-Cecchi, J., Collard, M., 2002. A fossil stapes from Sterkfontein, South Africa, and the hearing capabilities of early hominids. Journal of Human Evolution 42(3), 259-265. http://dx.doi.org/10.1006/jhev.2001.0524
Novacek, M. J., Wyss, A., 1986. Origin and transformation of the mammalian stapes. Rocky Mountain Geology 24(special paper 3), 35-53. http://dx.doi.org/10.2113/gsrocky.24.special_paper_3.35
Nummela, S., 1995. Scaling of the mammalian middle ear. Hearing Research 85(1), 18-30. http://dx.doi.org/10.1016/0378-5955(95)00030-8
Nummela, S., 2008. Hearing in aquatic mammals. In Nummela, S., Thewissen, J. G. M. (Eds.), Sensory evolution on the threshold, adaptation in secondarily vertebrates. University of California Press, Berkley and Los Angeles, pp. 211–226. http://dx.doi.org/10.1525/california/9780520252783.003.0013
Nummela, S., Sánchez-Villagra, M. R., 2006. Scaling of the marsupial middle ear and its functional significance. Journal of Zoology 270(2), 256-267. http://dx.doi.org/10.1111/j.1469-7998.2006.00126.x
Nummela, S., Thewissen, J. G. M., Bajpai, S., Hussain, T., Kumar, K., 2007. Sound transmission in archaic and modern whales: anatomical adaptations for underwater hearing. The Anatomical Record 290(6), 716-733. http://dx.doi.org/10.1002/ar.20528
O'Leary, M. A., Patel, B. A., Coleman, M. N., 2012. Endocranial petrosal anatomy of Bothriogenys (Mammalia, Artiodactyla, Anthracotheriidae) and petrosal volume and density comparisons among aquatic and terrestrial artiodactyls and outgroups. Journal of Paleontology, 86, 44-50. http://dx.doi.org/10.1666/10-091.1
Orliac, M. J., 2012. The petrosal bone of extinct Suoidea (Mammalia, Artiodactyla). Journal of Systematic Palaeontology 11(8), 925-945. http://dx.doi.org/10.1080/14772019.2012.704409
Orliac, M. J., Benoit, J., O'Leary, M. A., 2012. The inner ear of Diacodexis, the oldest artiodactyl mammal. Journal of Anatomy 221, 417-426. http://dx.doi.org/10.1111/j.1469-7580.2012.01562.x
Orliac, M., Guy, F., Lebrun, R., 2014. Osteological connexions of the petrosal bone of the extant Hippopotamidae Hippopotamus amphibius and Choeropsis liberiensis. MorphoMuseuM, 1(1), e1, 1-6. http://dx.doi.org/10.18563/m3.1.1.e1
Patterson, B., Segall, W., Turnbull, W. D., Gaudin, T. J., 1992. The ear region in xenarthrans (= Edentata, Mammalia). Part II. Pilosa (sloths, anteaters), palaeanodonts, and a miscellany. Fieldiana, Geology n.s. 24, 1-79.
Rosowski, J. J., Graybeal, A., 1991. What did Morganucodon hear? Zoological Journal of the Linnean Society 101(2), 131-168. http://dx.doi.org/10.1111/j.1096-3642.1991.tb00890.x
Ruf, I., Luo, Z. X., Martin, T., 2013. Reinvestigation of the basicranium of Haldanodon exspectatus (Mammaliaformes, Docodonta). Journal of Vertebrate Paleontology 33(2), 382-400. http://dx.doi.org/10.1080/02724634.2013.722575
Solntseva, G., 2013. Adaptive features of the middle ear of mammal in ontogeny. Acta Zoologica Bulgarica 65, 101-116.
Spoor, F., Garland Jr, T., Krovitz, G., Ryan, T. M., Silcox, M. T., Walker, A., 2007. The primate semicircular canal system and locomotion. Proceedings of the National Academy of Sciences, USA 104, 10 808–10 812. http://dx.doi.org/10.1073/pnas.0704250104
West, C. D., 1985. The relationship of the spiral turns of the cochlea and the length of the basilar membrane to the range of audible frequencies in ground dwelling mammals. Journal of the Acoustical Society of America 77, 1091-1101. http://dx.doi.org/10.1121/1.392227
Woodward, A. S., 1900. On some remains of Grypotherium (Neomylodori) listai and associated Mammals from a Cavern near Consuelo Cove, Last Hope Inlet, Patagonia. Proceedings of the Zoological Society of London 69(1), 64-78. http://dx.doi.org/10.1111/j.1096-3642.1890.tb01704.x
|
PDF |
S.I. Data |