Skip to main content
Log in

Morphofunctional Transformations of the Jaw Muscles in Rodent Evolution

  • Published:
Biology Bulletin Reviews Aims and scope Submit manuscript

Abstract

The paper summarizes results of long-term research on the jaw apparatus of modern rodents. The studied material includes original data on 22 families of the order Rodentia. The structure of the jaw muscles and the pathways of transformations during the evolution of the order, as well as the functional and phylogenetic aspects of its diversity in this group, are considered based on the concept of the jaw apparatus as an integral system. The structure of the jaw muscles has been studied in detail. It is shown that, despite their external diversity, aponeurotic carcasses have the same structure type; this can serve as a reliable basis for the identification and homologization of the elements of the internal muscle differentiation. The morphofunctional specialization of the jaw muscles is discussed. The morphotypes of the jaw apparatus, which reflect its adaptability to crushing and to vertical cutting are highlighted. Particular attention is paid to the description of two directions of specialization in the longitudinal grinding that is typical only for rodents. The first variant is manifested in hypertrophy of the anterior parts of the masseter, simplification of its differentiation, and a more horizontal orientation of its lateral and medial portions against the background of weakening of the temporal muscle. The second variant is associated with enhancement of internal differentiation of the masseter due to a special transformation of the lower jaw: an increase in its height, a shift of the angular process up to the dentition level, and a highly raised articular process. The correspondence of the types of jaw apparatus to the basal branches of Rodentia phylogenetic tree has been revealed. It is assumed that the typological diversity of this system evolved at the early stages of adaptive radiation of rodents. The similarity of these types within the phyletic lines results from the relatedness of the species. The functional specialization of the jaw apparatus within the basal groups was based on their structural type. It occurred mainly due to changes in the mandible and zygomatic arch and was expressed in similar spectra of its morphofunctional transformations in different rodent taxa.

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.

Similar content being viewed by others

REFERENCES

  1. Álvarez, A., Vieytes, E.C., Becerra, F., Olivares, A.I., Echeverría, A.I., et al., Diversity of craniomandibular morphology in caviomorph rodents: an overview of macroevolutionary and functional patterns, in Biology of Caviomorph Rodents: Diversity and Evolution, Vassallo, A.I. and Antenucci, D., Eds., Mendoza: Soc. Argent. Estudio Mamíferos, 2015, vol. 1, pp. 199–228.

    Google Scholar 

  2. Baverstock, H., Jeffery, N.S., and Cobb, S.N., The morphology of the mouse masticatory musculature, J. Anat., 2013, vol. 223, pp. 46–60. https://doi.org/10.1111/joa.12059

    Article  PubMed  PubMed Central  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, p. 71.

    Article  Google Scholar 

  4. Brandt, J.F., Beiträge sur näherch Kentniss der Säugetiere Rűsslands, Mem. Acad. Imp. Sci. St.-Petersbourg, 1855, vol. 9, no. 6, p. 336.

  5. Casanovas-Vilar, I. and van Dam, J., Conservatism and adaptability during squirrel radiation: What is mandible shape telling us? PLoS One, 2013, vol. 8, no. 4, p. e61298. https://doi.org/10.1371/journal.pone.0061298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Cox, P.G. and Baverstock, H., Masticatory muscle anatomy and feeding efficiency of the American beaver, Castor canadensis (Rodentia, Castoridae), J. Mamm. Evol., 2016, vol. 23, no. 2, pp. 191–200.

    Article  Google Scholar 

  7. Cox, P.G. and Faulkes, C.G., Digital dissection of the masticatory muscles of the naked mole-rat, Heterocephalus glaber (Mammalia, Rodentia), PeerJ, 2014, vol. 2, p. e448. https://doi.org/10.7717/peerj.448

    Article  PubMed  PubMed Central  Google Scholar 

  8. Cox, P.G. and Jeffery, N., Reviewing the morphology of the jaw-closing musculature in squirrels, rats, and guinea pigs with contrast-enhanced microCT, Anat. Rec., 2011, vol. 294, no. 6, pp. 915–928.

    Article  Google Scholar 

  9. Cox, P.G., Rayfield, E.J., Fagan, M.J., Herrel, A., Pataky, T.C., and Jeffery, N.S., Functional evolution of the feeding system in rodents, PLoS One, 2012, vol. 7, no. 4, p. e36299. https://doi.org/10.1371/journal.pone.0036299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Druzinsky, R.E., Functional anatomy of incisor biting in Aplodontia rufa and sciuromorph rodents—Part 1: Masticatory muscles, skull shape and digging, Cells Tissues Organs., 2010, vol. 191, no. 6, pp. 510–522.

    Article  Google Scholar 

  11. Druzinsky, R.E., Doherty, A.H., and de Vree, F.L., Mammalian masticatory muscles: homology, nomenclature, and diversification, Integr. Comp. Biol., 2011, vol. 51, no. 2, pp. 224–234.

    Article  Google Scholar 

  12. Gambaryan, P.P., Potapova, E.G., and Fokin, I.M., Morphofunctional features of the muscular apparatus of the head of jerboas: natural system of Dipodoidea, Rodentia, and Mammalia, in Funktsional’naya morfologiya mlekopitayushchikh (gryzuny, vodnye mlekopitayushchie) (Functional Morphology of Mammals: Rodents and Aquatic Mammals), Tr. Zool. Inst., Akad. Nauk SSSR vol. 91, Leningrad, 1980, pp. 3–51.

  13. Ginot, S., Herrel, A., Claude, J., and Hautier, L., Skull size and biomechanics are good estimators of in vivo bite force in murid rodents, Anat. Rec., 2018, vol. 301, no. 2, pp. 256–266.

    Article  Google Scholar 

  14. Greaves, W.S., The mammalian jaw mechanism—the high glenoid cavity, Am. Nat., 1980, vol. 116, no. 3, pp. 432–440.

    Article  Google Scholar 

  15. Hautier, L. and Saksiri, S., Masticatory muscle architecture in the Laotian rock rat Laonastes aenigmamus (Mammalia, Rodentia): new insights into the evolution of hystricognathy, J. Anat., 2009, vol. 215, no. 4, pp. 401–410.

    Article  Google Scholar 

  16. Heinse, W., Die Kaumusculatur des Scweines in anatomischer und funktioneller Hinsicht, Anat.Ans., 1961, vol. 109, no. 3, pp. 269–291.

    Google Scholar 

  17. Kesner, M.H., Functional morphology of the masticatory musculature of the rodent subfamily Microtinae, J. Morphol., 1980, vol. 165, no. 2, pp. 205–222.

    Article  CAS  Google Scholar 

  18. Klingener, D.J., The comparative myology of four dipodoid rodents (genus Zapus, Napaeozapus, Sicista and Jaculus), Misc. Publ. Mus. Zool., 1964, vol. 124, pp. 1–100.

    Google Scholar 

  19. Maier, W. and Schrenk, F., The hystricomorphy of the Bathyergidae, as determined from ontogenetic evidence, Z. Saugetierkd., 1987, vol. 52, no. 3, pp. 256–264.

    Google Scholar 

  20. Moss, M.L., Functional cranial analysis of mammalian mandibular ramal morphology, Acta Anat., 1968, vol. 71, no. 3, pp. 423–447.

    CAS  PubMed  Google Scholar 

  21. Nikol’skii, V.S., General principles of biomechanical of mandibular apparatus of mammals, Zool. Zh., 1997, vol. 76, no. 1, pp. 94–103.

    Google Scholar 

  22. Offermans, M. and de Vree, F., Morphology of the masticatory apparatus in the springhare, Pedetes capensis,J. Mamm., 1989, vol. 70, no. 4, pp. 701–711.

    Google Scholar 

  23. Pavlinov, I.Ya. and Potapova, E.G., Cladistic analysis of the dormice genus Graphiurus Smuts, 1832 (Rodentia, Gliridae) with comments on evolution of its zygomasseteric construction and subgeneric taxonomy, Russ. J. Theriol., 2003, vol. 2, no. 1, pp. 49–58.

    Google Scholar 

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

  25. Potapova, E.G., Parallelism in the development of the mandibular muscles by the example Dipodoidea rodents, Tr. Biol.-Pochv. Inst., Dal’nevost. Otd.,Ross. Akad. Nauk, 1979, vol. 52 (155), pp. 73–90.

    Google Scholar 

  26. Potapova, E.G., Skull and mandibular apparatus, in Ondatra. Morfologiya, sistematika, ekologiya (Morphology, Systematics, and Ecology of the Muskrat), Moscow: Nauka, 1993, pp. 96–112.

  27. Potapova, E.G., Transformation of low mandible of Dipodoidea species (Rodentia) and role of various adaptations in its transformation, Zool. Zh., 2000, vol. 79, no. 12, pp. 1445–1456.

    Google Scholar 

  28. Potapova, E.G., Zygomasseteric structure in rodents: typological, adaptive, and classification aspects, Zool. Zh., 2014, vol. 93, no. 7, pp. 841–856.

    Google Scholar 

  29. Potapova, E.G., Evolutionary transformations of mandibular muscles of Laonastes aenigmamus and Ctenodactylus gundi (Ctenodactyloidea, Rodentia), Tr. Zool. Inst.,Ross. Akad. Nauk, 2015a, vol. 319, no. 3, pp. 401–417.

    Google Scholar 

  30. Potapova, E.G., Structural and phylogenetic aspect of typology of the lower mandible in rodents, Materialy 59-oi Sessii Paleontologicheskogo obshchestva Rossiiskoi Akademii Nauk “Sovremennye problemy paleontologii” (Proc. 59th Session of Paleontological Society, Russian Academy of Sciences “Modern Problems in Paleontology”), St. Petersburg, 2015b, pp. 166–167.

  31. Potapova, E.G., Morphofunctional specialization of the mandible apparatus of Anomaluridae (Rodentia, Mammalia), Materialy Vserossiiskoi konferentsii i shkoly dlya molodykh uchenykh pamyati F.Ya. Dzerzhinskogo “Evolyutsionnaya i funktsional’naya morfologiya pozvonochnykh” (Proc. All-Russ. Conf. and School for Young Scientists in Memoriam of F.Ya. Dzerzhinskii “Evolutionary and Functional Morphology of Vertebrates”), Moscow: KMK, 2017, pp. 240–246.

  32. Potapova, E.G. and Puzachenko, A.Yu., Similarity analysis in the structure of the lower jaw of Dipodoidea species (Rodentia), Zool. Zh., 2000, vol. 79, no. 9, pp. 1102–1113.

    Google Scholar 

  33. Potapova, E.G. and Rossolimo, O.L., Morphological diversity of lower mandible of Gliroidea (Rodentia): adaptive and phylogenetic aspects, in Zoologicheskie issledovaniya (Zoological Studies), Tr. Zool. Muz., Mosk. Gos. Univ. vol. 49, Moscow: Mosk. Gos. Univ., 2008, pp. 390–412.

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

    Google Scholar 

  35. Reppening, Ch.A., Musculature and origin of the subfamily Arvicolinae (Rodentia), Acta Zool. Cracov., 1968, vol. 13, no. 3, pp. 29–72.

    Google Scholar 

  36. Rinker, G.C., The comparative myology of the mammalian genera Sigmodon, Oryzomys, Neotoma, and Peromyscus (Cricetinae), with remarks of their intergeneric relationships, Misc. Publ. Mus. Zool., 1954, vol. 83.

    Google Scholar 

  37. Rossolimo, O.L., Potapova, E.G., Pavlinov, I.Ya., Kruskop, S.V., and Voltsit, O.V., Soni (Myoxidae) mirovoi fauny (Dormice (Myoxidae) in the World Fauna), Moscow: Mosk. Gos. Univ., 2001.

  38. Satoh, K. and Iwaku, F., Jaw muscle functional anatomy in northern grasshopper mouse, Onychomys leucogaster, a carnivorous murid, J. Morphol., 2006, vol. 267, no. 8, pp. 987–999.

    Article  Google Scholar 

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

  40. Tullberg, T., Über das System der Nagethiere: eine Phylogenetische Studie, Nova Acta Regiae Soc. Sci. Ups. vol. 18, Uppsala: Akadem. Buchdruckerei, 1899.

  41. Turnbull, W.D., Mammalian masticatory apparatus, Fieldiana: Geol., 1970, vol. 18, no. 2, pp. 149–356.

    Google Scholar 

  42. Vianey-Liaud, M., Parallelism among Gliridae (Rodentia): the genus Gliravus Stehlin and Schaub, Hist. Biol., 1989, vol. 2, no. 3, pp. 213–226.

    Google Scholar 

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

  44. Wolf-Exalto, E.A., On differences in the lower jaw of animalivorous and herbivorous mammals, Proc. K. Ned. Akad. Wet., Ser. C: Biol. Med. Sci., 1951, vol. 54, no. 2, pp. 1–52.

    Google Scholar 

  45. Wood, A.E., Eocene radiation of the rodents, Evolution, 1959, vol. 13, pp. 354–361.

    Google Scholar 

  46. Wood, A.E., Grades and clades among rodents, Evolution, 1965, vol. 19, pp. 115–130.

    Google Scholar 

  47. Woods, C.A., Comparative myology of jaw, hyoid and pectoral appendicular regions of New and Old World hystricomorph rodents, Bull. Am. Mus. Nat. Hist., 1972, vol. 147, pp. 115–198.

    Google Scholar 

  48. Woods, C.A. and Howland, E.B., Adaptive radiation of capromyid rodents: anatomy of the masticatory apparatus, J. Mamm., 1979, vol. 60, no. 1, pp. 95–116.

    Google Scholar 

  49. Zherebtsova, O.V. and Potapova, E.G., Morphological adaptations in modern species of Diatomyidae and Ctenodactylidae (Rodentia), Zool. Zh., 2018, vol. 97, no. 8, pp. 977–997.

    Google Scholar 

Download references

ACKNOWLEDGMENTS

The author is grateful to the staff of the Zoological Museum of Moscow State University (Moscow), the Zoological Institute of the Russian Academy of Sciences (St. Petersburg), the Museum of Natural History (London), and the Royal Museum of Central Africa (Tervuren, Belgium) for the opportunity to use the collections of these museums. The author is grateful to colleagues from various institutes of the Russian Academy of Sciences and Moscow University for the fruitful cooperation on this study.

Funding

The work was carried out on the topic of the State Assignment of the Laboratory of Ecology, Physiology, and Functional Morphology of Higher Vertebrates of the Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences within the framework of the Federal Agency for Scientific Organization (project no. 0120-1356-032).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. G. Potapova.

Ethics declarations

Conflict of interests. The authors declare that they have no conflicts of interest.

Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Translated by T. Kuznetsova

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Potapova, E.G. Morphofunctional Transformations of the Jaw Muscles in Rodent Evolution. Biol Bull Rev 10, 394–406 (2020). https://doi.org/10.1134/S2079086420050072

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079086420050072

Navigation