Skip to main content

Advertisement

Log in

Morphology of the Middle Ear Ossicles in the Rodent Perimys(Neoepiblemidae) and a Comprehensive Anatomical and Morphometric Study of the Phylogenetic Transformations of these Structures in Caviomorphs

  • Original Paper
  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

Abstract

The extinct clade of caviomorph rodents Neoepiblemidae includes forms that lived in South America from the early Miocene to Pliocene. Among them is Perimys. The exceptional preservation of ear ossicles in this rodent is described and analyzed in a study of the phylogenetic transformations of these structures in caviomorphs including 21 extant and two extinct genera. Caviomorphs exhibit a conserved malleoincudal complex, with synostosis of the malleus and incus, “bullet-shaped” mallear head, and absence of orbicular apophysis. They also show a reduction of the mallear anterior process, in some cases even lacking this structure. The malleoincudal complex of Perimys shows an elongation of the head, but not as marked as in Chinchillinae. The incudal long process of Perimys is slightly more prolonged than the short process, as in chinchillids. In contrast, dinomyids have the incudal long process disproportionally more prolonged than in most caviomorphs. Concerning the disparity of caviomorph middle ear ossicles, Perimys shares the morphospace with chinchillids and other small forms. Within chinchilloids, Perimys is closer to chinchillids than to neoepiblemids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Albuquerque AGS, Rossato M, Oliveira JAA, Hyppolito MG (2009) Understanding the anatomy of ears from guinea pigs and rats and its use in basic otologic research. Braz J Otorhinolaryngol 75(1):43–49. https://doi.org/10.1016/S1808-8694(15)30830-2

    Article  PubMed  Google Scholar 

  • Argyle EC, Mason MJ (2008) Middle ear structures of Octodon degus (Rodentia: Octodontidae), in comparison with those of subterranean caviomorphs. J Mammal 89:1447–1455. https://doi.org/10.1644/07-MAMM-A-401.1

    Article  Google Scholar 

  • Bondesio P, Pascual R, Vucetich MG (1975) Los Neoepiblemidae (Rodentia, Caviomorpha): su caracterización y sus relaciones filogenéticas con los Chinchillidae. Actas del Primer Congreso Argentino de Paleontología y Bioestratigrafía, Tomo 2:431–447

    Google Scholar 

  • Bouxin G (2005) Ginkgo, a multivariate analysis package. J Veg Sci 16:355–359

    Article  Google Scholar 

  • Bryant JD, McKenna MC (1995) Cranial anatomy and phylogenetic position of Tsaganomys altaicus (Mammalia: Rodentia) from the Hsanda Gol Formation (Oligocene), Mongolia. Am Mus Novitates 3156:1–42

  • Cahn AR (1930) Auditory ossicles of living and giant beavers. J Mammal 11(3):292–299

    Article  Google Scholar 

  • Cisneros JC, Ruta M (2010) Morphological diversity and biogeography of procolophonids (Amniota: Parareptilia). J Syst Palaeontolol 8(4): 607–625. https://doi.org/10.1080/14772019.2010.491986

    Article  Google Scholar 

  • Cockerell TDA, Miller LI, Printz M (1914) The auditory ossicles of American rodents. Bull Am Mus Nat Hist, 33:347–380

    Google Scholar 

  • Costeur L, Mennecart B, Muller B, Schulz G (2016) Middle ear bones of a mid-gestation ruminant foetus extracted from X-ray computed tomography. In: Stock SR, Müller B, Wang G (eds) Developments in X-Ray Tomography X. Proceedings of SPIE - The International Society for Optical Engineering 9967:1–8. https://doi.org/10.1117/12.2238119

  • Doran AHG (1878) Morphology of the mammalian ossicula auditus. Trans Linn Soc Lond 1:371–497

    Article  Google Scholar 

  • Fabre P-H, Hautier L, Dimitrov D, Douzery EJP (2012) A glimpse on the pattern of rodent diversification: a phylogenetic approach. BMC Evol Biol 12(88): 1–19. https://doi.org/10.1186/1471-2148-12-88

    Article  Google Scholar 

  • Fields RW (1957) Hystricomorph rodents from the late Miocene of Colombia, South America. Univ Calif Publ Geo Sci 32:273–404

    Google Scholar 

  • Fleischer G (1973) Studien am Skelett des Gehörorgans der Säugetiere, einschließlich des Menschen. Säugetierkundliche Mitteilungen 21:131–239

  • Fleischer G (1978) Evolutionary principles of the mammalian middle ear. Adv Anat Embryol Cell Biol 55:1–70

  • Gaetano LC, Abdala F (2015) The stapes of gomphodont cynodonts: insights into the middle ear structure of non-mammaliaform cynodonts. PLoS One 10(7): e0131174. https://doi.org/10.1371/journal.pone.0131174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goloboff P, Catalano S (2016) TNT version 1.5, including a full implementation of phylogenetic morphometrics. Cladistics 32(3):221–238. https://doi.org/10.1111/cla.12160

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):1–9

  • Horovitz I, Sánchez-Villagra MR, Martin T, Aguilera AO (2006) The fossil record of Phoberomys pattersoni Mones 1980 (Mammalia, Rodentia) from Urumaco (late Miocene, Venezuela), with an analysis of its phylogenetic relationships. J Syst Palaeontol 4:293–306. https://doi.org/10.1017/S1477201906001908

  • Huchon D, Catzeflis FM, Douzery EJP (2000) Variance of molecular datings, evolution of rodents, and the phylogenetic affinities between Ctenodactylidae and Hystricognathi. Proc R Soc Lond B Biol Sci 267: 393–402. https://doi.org/10.1098/rspb.2000.1014

  • Huchon D, Madsen O, Sibbald MJJB, Ament K, Stanhope MJ, Catzeflis F, De Jong WW, Douzery EJP (2002) Rodent phylogeny and a timescale for the evolution of Glires: evidence from an extensive taxon sampling using three nuclear genes. Mol Biol Evol 19: 1053–1065

    Article  CAS  PubMed  Google Scholar 

  • Kemp TS (2007) Acoustic transformer function of the postdentary bones and quadrate of a non-mammalian cynodont. J Vertebr Paleontol 27:431–441

  • Kerber L, Negri FR, Ribeiro AM, Nasif N, Pereira Souza-Filho J, Ferigolo J (2017) Tropical fossil caviomorph rodents from the southwestern Brazilian Amazonia in the context of the South American faunas: systematics, biochronology, and paleobiogeography. J Mammal Evol 24:57–70. https://doi.org/10.1007/s10914-016-9340-2

    Article  Google Scholar 

  • Koyabu D, Hosojima M, Endo H (2017) Into the dark: patterns of middle ear adaptations in subterranean eulipotyphlan mammals. R Soc open sci 4: 170608. https://doi.org/10.1098/rsos.170608

    Article  PubMed  PubMed Central  Google Scholar 

  • Kraglievich L (1940) Los roedores de la familia extinguida Neoepiblemidae. In: Torcelli AJ, Morelli CA (eds) Obras de Geología y Paleontología 3 (Obras completas y trabajos científicos inéditos). Ministerio de Obras Públicas de la Província de Buenos Aires, Buenos Aires, pp 741–764

    Google Scholar 

  • Kramarz AG, Vucetich MG, Arnal M (2013) A new early Miocene chinchilloid hystricognath rodent; an approach to the understanding of the early chinchillid dental evolution. J Mammal Evol 20:249–261. https://doi.org/10.1007/s10914-012-9215-0

    Article  Google Scholar 

  • Luo Z-X (2011) Developmental patterns in Mesozoic evolution of mammal ears. Annu Rev Ecol Evol Syst 42:355–380

    Article  Google Scholar 

  • Luo Z-X, Schultz JA, Ekdale EG (2016) Evolution of the middle and inner ears of mammaliaforms: the approach to mammals. In: Clack JA, Fay, RR, Popper AN (eds) Evolution of the Vertebrate Ear—Evidence from the Fossil Record. Springer Handbook of Auditory Research 59:139–174. https://doi.org/10.1007/978-3-319-46661-3_6

    Chapter  Google Scholar 

  • Maddison WP, Maddison DR (2015) Mesquite: a modular system for evolutionary analysis. Version 3.03. Available in: http://mesquiteproject.org/. Accessed 11 April 2016.

  • Maier W, Ruf I (2016) The anterior process of the malleus in Cetartiodactyla. J Anat 228:313–323. https://doi.org/10.1111/joa.12393

    Article  PubMed  Google Scholar 

  • Maier W, Van Den Heever J (2002) Middle ear structures in the Permian Glanosuchus sp. (Therocephalia, Therapsida), based on thin sections. Mitteil Mus Naturkd Berl Geowiss 5:309–318

    Google Scholar 

  • Martins LL, Almeida-Silva I, Rossato M, Murashima AAB, Hyppolito MA, Machado MRF (2015) Macroscopic description of the external and middle ear of paca (Cuniculus paca Linnaeus, 1766). Pesqui Vet Bras 35(6):583–589. https://doi.org/10.1590/S0100-736X2015000600017

    Article  Google Scholar 

  • Mason MJ (2004) The middle ear apparatus of the tuco-tuco Ctenomys sociabilis (Rodentia, Ctenomyidae). J Mammal 85:797–805. https://doi.org/10.1644/BEL-102

    Article  Google Scholar 

  • Mason MJ (2013) Of mice, moles and guinea-pigs: functional morphology of the middle ear in living mammals. Hear Res 301:4–18. https://doi.org/10.1016/j.heares.2012.10.004

    Article  PubMed  Google Scholar 

  • Mason MJ (2015) Functional morphology of rodent middle ears. In: Cox PG, Hautier L (eds) Evolution of the Rodents: Advances in Phylogeny, Functional Morphology and Development. Cambridge University Press, Cambridge, pp 373–404.

    Chapter  Google Scholar 

  • Meng J (1992) The stapes of Lamdopsalis bulla (Multituberculata) and transformational analyses on some stapedial features in Mammaliaformes. J Vertebr Paleontol 12(4):459–171

    Article  Google Scholar 

  • Meng J, Bi S, Zheng X, Wang X (2016) Ear ossicle morphology of the Jurassic euharamiyidan Arboroharamiya and evolution of mammalian middle ear. J Morphol. https://doi.org/10.1002/jmor.20565

  • Meng J, Wang YQ, Li CK (2011) Transitional mammalian middle ear from a new Cretaceous Jehol eutriconodont. Nature 472:181–185. https://doi.org/10.1038/nature09921

    Article  CAS  PubMed  Google Scholar 

  • Mones A (1974) Estudios sobre la familia Hydrochoeridae (Rodentia), III. Osteología comparada de la región auditiva de Hydrochoerus Brisson con formas afines. Ameghiniana 11(1):39–57

    Google Scholar 

  • Mones A (1997) Estudios sobre la familia Dinomyidae, II. Aportes para una osteologia comparada de Dinomys branickii Peters, 1873 (Mammalia: Rodentia). Comunicaciones Paleontológicas del Museo Nacional de Historia Natural de Montevideo 29:1–40

    Google Scholar 

  • Moore WJ (1981) The Mammalian Skull. Cambridge University Press, Cambridge

    Google Scholar 

  • Nasif N (2009) Los Dinomyidae (Rodentia, Caviomorpha) del Mioceno superior del noroeste argentino. Su anatomía cráneo-dentaria. Ph.D. Thesis, Facultad de Ciencias Naturales and Instituto Miguel Lillo Universidad Nacional de Tucumán, Tucumán, 363 pp

  • Novacek MJ (1993) Patterns of diversity in the mammalian skull. In: Hanken J, Hall BK (eds) The Skull. 2. Patterns of Structural and Systematic Diversity. University of Chicago Press, Chicago, pp 438–545

    Google Scholar 

  • Novacek MJ, Wyss A (1986) Origin and transformation of the mammalian stapes. Contrib Geol Univ Wyoming Spec Pap 3:35–53

    Google Scholar 

  • Orliac MJ, Billet G (2016) Fallen in a dead ear: intralabyrinthine preservation of stapes in fossil artiodactyls. Palaeovertebrata 40(1)-e3:1–10. https://doi.org/10.1080/08912963.2017.1294168

  • Rasia LL, Candela AM (2017) Reappraisal of the giant caviomorph rodent Phoberomys burmeisteri (Ameghino, 1886) from the late Miocene of northeastern Argentina, and the phylogeny and diversity of Neoepiblemidae. Historical Biol. https://doi.org/10.1080/08912963.2017.1294168

  • Rich TH, Hopson JA, Musser AM, Flannery TF, Vickers P (2005). Independent origins of middle ear bones in monotremes and therians. Science 307:910–914. https://doi.org/10.1126/science.1105717

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues PG, Ruf I, Schultz CL (2013) Digital reconstruction of the otic region and inner ear of the non-mammalian cynodont Brasilitherium riograndensis (Late Triassic, Brazil) and its relevance to the evolution of the mammalian ear. J Mammal Evol 20:291–307. https://doi.org/10.1007/s10914-012-9221-2

    Article  Google Scholar 

  • Rohlf FJ (2017) TPSDig software series, digitize landmarks & outlines from image files, scanner, or video, version 2.29. Stony Brook, Department of Ecology and Evolution, State University of New York. http://life.bio.sunysb.edu/morph/index.html. Accessed 30 January 2016

  • Sánchez-Villagra MR, Aguilera O, Horovitz I (2003) The anatomy of the world’s largest extinct rodent. Science 301:1708–1710. https://doi.org/10.1126/science.1089332

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Villagra MR, Gemballa S, Nummela S, Smith KK, Maier W (2002) Ontogenetic and phylogenetic transformations of the ear ossicles in marsupial mammals. J Morphol 251:219–238. https://doi.org/10.1002/jmor.1085

    Article  PubMed  Google Scholar 

  • Sánchez-Villagra MR, Nummela S (2001) Bullate stapes in some phalangeriform marsupials. Mammal Biol 66:174–177

    Google Scholar 

  • Schleich CE, Busch C (2004) Functional morphology of the middle ear of Ctenomys talarum (Rodentia: Octodontidae). J Mammal 85:290–295

    Article  Google Scholar 

  • Schmelzle T, Nummela S, Sánchez-Villagra MR (2007) Phylogenetic transformations of the ear ossicles in marsupial mammals, with special reference to diprotodontians: a character analysis. Ann Carnegie Mus 74(3):189–200

    Article  Google Scholar 

  • Sidorkewicj NS, Casanave EB (2012) Morphology of the middle ear in three species of armadillos (Dasypodidae, Xenarthra) from Argentina. Internatl J Morphol 30(4):1500–1507. https://doi.org/10.4067/S0717-95022012000400038

    Article  Google Scholar 

  • Stoessel A, Gunz P, David R, Spoor F (2016) Comparative anatomy of the middle ear ossicles of extant hominids: introducing a geometric morphometric protocol. J Hum Evol 91:1–25. https://doi.org/10.1016/j.jhevol.2015.10.013

    Article  PubMed  Google Scholar 

  • Upham NS, Patterson BD (2015) Evolution of the caviomorph rodents: a complete phylogeny and time tree of living genera. In: Vassallo A, Antonucci D (ed) Biology of Caviomorph Rodents: Diversity and Evolution. Sociedad Argentina para el estudio de los Mamíferos, Buenos Aires, pp 63–120

  • Voloch CM, Vilela JF, Loss-Oliveira L, Schrago CG (2013) Phylogeny and chronology of the major lineages of New World hystricognath rodents: insights on the biogeography of the Eocene/Oligocene arrival of mammals in South America. BMC Res Notes 6(160):1–9. https://doi.org/10.1186/1756-0500-6-160

    Article  Google Scholar 

  • Voss RS (2011) Revisionary notes on Neotropical porcupines (Rodentia: Erethizontidae). 3. An annotated checklist of species of Coendou Lacépède, 1799. Am Mus Novitates 3720:1–36

    Article  Google Scholar 

  • Vrettakos PA, Steve T, Dear SP, Saunders JC (1988) Middle ear structure in the chinchilla: a quantitative study. Am J Otolaryngol 9:58–67

    Article  CAS  PubMed  Google Scholar 

  • Vucetich MG (1975) La anatomia del oido medio como indicadora de rleaciones sistematicas y filogeneticas en algunos grupos de roedores Caviomorpha. Actas del Primer Congreso Argentino de Paleontología y Bioestratigrafía 2:447–494

  • Vucetich MG, Arnal M, Deschamps CM, Pérez ME, Vieytes EC (2015) A brief history of caviomorph rodents as told by the fossil record. In: Vassallo A, Antonucci D (eds) Biology of Caviomorph Rodents: Diversity and Evolution. Sociedad Argentina para el estudio de los Mamíferos, Buenos Aires, pp 11–62

  • Vucetich MG, Vieytes EC, Perez ME, Carlini AA (2010) The rodents from La Cantera and the early evolution of caviomorphs in South America. In: Madden RH, Carlini AA, Vucetich MG, Kay RF (eds) The Paleontology of Gran Barranca, Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge University Press, Cambridge, pp 189–201

  • Wible JR, Spaulding M (2012) A reexamination of the Carnivora malleus (Mammalia, Placentalia). PLoS One 7(11):e50485. https://doi.org/10.1371/journal.pone.0050485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilkins KT, Roberts JC, Roorda CS, Hawkins JE (1999) Morphometrics and functional morphology of middle ears of extant pocket gophers (Rodentia, Geomyidae). J Mammal 80:180–198. https://doi.org/10.2307/1383218

    Article  Google Scholar 

  • Wills MA (1998) Cambrian and recent disparity: the picture from priapulids. Paleobiology 24:177–199

  • Wills MA, Briggs DEG, Fortey RA (1994) Disparity as an evolutionary index: a comparison of Cambrian and Recent arthropods. Paleobiology 20:93–130. https://doi.org/10.1017/S009483730001263X

Download references

Acknowledgements

We would like to express our gratitude to: CNPq (Conselho Nacional de Pesquisa e Tecnologia) [Process CNPq 8, 201356/ 2015-5 (L.K)]. Elio Massoia organized the collection of most of the specimens analyzed herein; they were extracted from the middle ear of these rodents by him and other researches. Maria Guiomar Vucetich kindly gave us most of the specimens – another example of her extraordinary mentorship to younger (and not so young) rodent researchers. Universität Zürich provided the infrastructure for this work. Rodrigo Temp Müller helped us with the disparity morphospace occupation analysis, Felipe Pinheiro, read and commented the first draft of this manuscript, and Juan D. Carrillo kindly revised an advanced version and provided useful comments. We thank Diego Verzi for his assistance as curator of the mastozoology section at the MLP and Martina Schenkel curator at the Zoologisches Museum, University of Zurich; two reviewers and the editor-in-chief John Wible for their useful comments. TNT v.1.5 was used for phylogenetic analysis. This is a program made freely available thanks to a subsidy by the Willi Hennig Society.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Leonardo Kerber.

Electronic supplementary material

ESM 1

(XLSX 11 kb)

ESM 2

(NEXUS 15 kb)

ESM 3

(NEXUS 12 kb)

ESM 4

(DOCX 405 kb)

ESM 5

(XLSX 15 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kerber, L., Sánchez-Villagra, M.R. Morphology of the Middle Ear Ossicles in the Rodent Perimys(Neoepiblemidae) and a Comprehensive Anatomical and Morphometric Study of the Phylogenetic Transformations of these Structures in Caviomorphs. J Mammal Evol 26, 407–422 (2019). https://doi.org/10.1007/s10914-017-9422-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-017-9422-9

Keywords

Navigation