Chueva A., Gelashvili D., Yakimov V., Bragazin A., Mukhanov A. Сomprehensive craniological analysis of geographically remote muskrat populations (Ondatra zibethicus Linnaeus, 1766) // Principy èkologii. 2020. № 1. P. 121‒135. DOI: 10.15393/

Issue № 1

Original research


Сomprehensive craniological analysis of geographically remote muskrat populations (Ondatra zibethicus Linnaeus, 1766)

   Anna Viktorovna
Lobachevsky State University of Nizhny Novgorod,
   David Bezhanovich
Lobachevsky State University of Nizhny Novgorod,
   Vasily Nikolaevich
Lobachevsky State University of Nizhny Novgorod,
   Alexander Andreevich
Lobachevsky State University of Nizhny Novgorod,
   Alexey Valeryevich
Lobachevsky State University of Nizhny Novgorod,
digital 3D-model of the skull
geometric morphometry
fluctuating asymmetry
Nizhny Novgorod Volga region
South Kazakhstan
Summary: In this article, a comprehensive craniological analysis of two geographically remote muskrat populations (Ondatra zibethicus Linnaeus, 1766) was carried out. The research material was samples of muskrat skulls from two geographical populations more than 2000 km away from each other: the vicinity of the village of Aristovo, Semenovsky district, Nizhny Novgorod region and the valley of the Ili River, Balkhash district of the Republic of Kazakhstan. A standard craniometric analysis of the samples from Nizhny Novgorod and Kazakhstan revealed inter-population differences in only one of eight linear measurements (the length of the incisive foramen). The analysis of skull shape based on digital 3D-models revealed inter-population differences in the symmetric component of the form. The analysis of the asymmetric component of the skull form revealed the presence of both fluctuating and directional asymmetry. At the same time the fluctuating asymmetry is about 10 times higher than the directional one. Procrustes ANOVA based on the asymmetric component of muskrat skull shape revealed that that directional asymmetry, in contrast to fluctuating asymmetry, is characterized by inter-population specificity, that is, muskrat skulls in different populations deviate differently from strict bilateral symmetry. At this stage of research, it is impossible to find out whether this specificity has an adaptive value or is the result of isolation and genetic-automatic processes. The obtained results complement our understanding of the processes of morphological adaptation in muskrat populations as an introduced species.

© Petrozavodsk State University

Received on: 29 July 2019
Published on: 12 March 2020


Adams D. C., Collyer M. L., Kaliontzopoulou A., Sherratt E. Geomorph: Software for geometric morphometric analyses. R package version 0.5. 2017. P. 1–139. URL:

Adams D. C., Otárola-Castillo E. Geomorph: an R package for the collection and analysis of geometric morphometric shape data, Methods in Ecology and Evolution. 2013. Vol. 4. Issue 4. P. 393–399. DOI: 10.1111/2041-210X.12035

Amshokova A. H. Variability of craniometric patterns of the pygmy wood mouse (Sylvaemus uralensis) at various altitudinal levels in the Central Caucasus, Vestnik Nizhegorodskogo universiteta im. N. I. Lobachevskogo. 2010. No. 3-1. P. 126–133.

Aver'yanov A. O. Lopatin A. V. Phylogeny of tricodonts and symmetrodonts and the origin of modern mammals, Doklady Akademii nauk. 2011. T. 436. No. 2. P. 276–279.

Badyaev A. V., Foresman K. R. Extreme environmental change and evolution: stress-induced morphological variation is strongly concordant with patterns of evolutionary divergence in shrew mandibles, Proc. R. Soc. Lond. 2000. Issue 267. P. 371-377.

Baryshnikov G. F. Puzachenko A. Yu. Craniometric diversity of island populations of the brown bear (Ursus arctos, Carnivora) from Hokkaido, Sakhalin and the Southern Kuriles, Trudy Zoologicheskogo instituta RAN. 2009. T. 313. No. 2. P. 119–142.

Baryshnikov G. F. Puzachenko A. Yu. Craniometric variability of the river otter (Lutra lutra: Carnivora: Mustelidae) in Northern Eurasia, Trudy Zoologicheskogo instituta RAN. 2012. T. 316. No. 3. P. 203–222.

Bobrov V. V. Mammalian invasive species in Russia (survey of studies), Social'no-ekologicheskie tehnologii. 2015. No. 1-2. P. 21–30.

Boroneckaya O. I. Nikiforov A. I. Chikurova E. A. Ye. F. Liskun state museum of livestock – center for craniological research, Izvestiya Timiryazevskoy sel'skohozyaystvennoy akademii. 2017. No. 3. P. 70–83.

Chaschuhin V. A. Muskrat: causes and effects of biological invasion. M.: T-vo nauchnyh izdaniy KMK, 2007. 133 p.

Cox P. G., Kirkham J., Herre A. Masticatory biomechanics of the Laotian rock rat, Laonastes aenigmamus, and the function of the zygomaticomandibularis muscle, PeerJ. 1: e160. 2013. DOI: 10.7717/peerj.160

Dgebuadze Yu. Yu. Alien species in the Holarctic: some results and prospects of research, Rossiyskiy zhurnal biologicheskih invaziy. 2014. No. 1. P. 2–8.

Ge D., Yao L., Xia L., Zhang Z., Yang Q. Geometric morphometric analysis of skull morphology reveals loss of phylogenetic signal at the generic level in extant lagomorphs (Mammalia: Lagomorpha), Contributions to Zoology. 2015. Vol. 84 (4). P. 267–284.

Gelashvili D. B. Chuprunov E. V. Somov N. V. Marychev M. O. Nizhegorodcev A. A. Markelov I. N. Yakimov V. N. Group-theoretical analysis of symmetry transformations on the example of some hydrobionts, Zhurnal obschey biologii. 2018. T. 79. No. 3. P. 169–182.

Gelashvili D. B. Chuprunov E. V. Somov N. V. Marychev M. O. Nizhegorodcev A. A. Markelov I. N. Yakimov V. N. Pseudosymmetry in wildlife: monograph, Pod obsch. red. prof. D. B. Gelashvili i prof. E. V. Chuprunova. N. Novgorod: Izd-vo NNGU, 2016. 363 p.

Good P. Permutation, parametric and bootstrap tests of hypotheses. N.Y.: Springer, 2005. 315 p.

Hlyap L. A. Bobrov V. V. Varshavskiy A. A. Biological invasions in the territory of Russia: mammals, Rossiyskiy zhurnal biologicheskih invaziy. 2008. No. 2. P. 78–96.

Karaseva E. V. Telicyna A. Yu. Zhigal'skiy O. A. Methods for the study of rodents in the field. M.: Izd-vo LKI, 2008. 416 p.

Klingenberg C. P. A combined morphometric and phylogenetic analysis of an ecomorphological trend: pelagization in Antarctic fishes (Perciformes: Nototheniidae), Biological Journal of the Linnean Society. 1996. Issue 59. P. 143–177.

Klingenberg C. P. Morphological Integration and developmental modularity, Annu. Rev. Ecol. Evol. Syst. 2008. Issue 39. P. 115–132.

Klingenberg C. P., Barluenga M., Meyer A. Shape analysis of symmetric structures: Quantifying variation among individuals and asymmetry, Evolution. 2002. Vol. 56. Issue 10. P. 1909–1920.

Klingenberg C. P., McIntyre G. S. Geometric morphometrics of developmental instability: Analyzing patterns of fluctuating asymmetry with procrustes methods, Evolution. 1998. Vol. 52. Issue 5. P. 1363–1375.

Lalis A., Evin A., Denys C. Morphological identification of sibling species: the case of West African Mastomys (Rodentia: Muridae) in sympatry, C. R. Biologies. 2009. Vol. 332. P. 480–488.

Lebedev V. S. Lisovskiy A. A. The geographical variability of the metric signs of the skull and the taxonomic structure of the hamsters Cricetulus of the Barabensis group (Rodentia, Cricetidae), Zoologicheskiy zhurnal. 2008. T. 87. No. 3. P. 361–374.

Maga A. M., Navarro N., Cunningham M. L., Cox T. C. Quantitative trait loci affecting the 3D skull shape and size in mouse and prioritization of candidate genes in-silico, Frontiers in Physiology. 2015. Vol. 6. Article 92. DOI: 10.3389/fphys.2015.00092

Morpho-phenetic analysis of populations of the American mink (Neovison vison) of the Caspian-Baltic watershed, Rossiyskiy zhurnal biologicheskih invaziy. 2012. No. 4. P. 36–56.

Muskrat: morphology, systematics, ecology. M.: Nauka, 1993. 542 p.

Oleynikov A. Yu. Placement of native and introduced semi-aquatic mammals on Sikhote-Alin, Rossiyskiy zhurnal biologicheskih invaziy. 2013. No. 2. P. 35–50.

Pavlinov I. Ya. Nanova O. G. Spasskaya N. N. To the study of morphological variety of dimensional signs of the skull of mammals. 1. Value different forms of group variability, Zhurnal obschey biologii. 2008. T. 69. No. 5. P. 344–354.

Pozdnyakov A. A. Morphological variability of animals (methods, study results using different taxa as an example), Soobschestva i populyacii zhivotnyh: ekologicheskiy i morfologicheskiy analiz. Novosibirsk; M.: Tovarischestvo nauchnyh izdaniy KMK, 2010. P. 133–157.

Puzachenko A. Yu. Invariants and dynamics of morphological diversity (on the example of the skull of mammals): Avtoref. dip. … d-ra biol. nauk. M., 2013. 48 p.

Puzachenko A. Yu. Quantitative regulations of the morphological diversity of the skull of mammals, Sbornik trudov Zoologicheskogo muzeya MGU im. M. V. Lomonosova. 2016. T. 54. P. 229–268.

Quintela F. M., Fornel R., Freitas T. R. O. Geographic variation in skull shape of the water rat Scapteromys tumidus (Cricetidae, Sigmodontinae): isolation-by-distance plus environmental and geographic barrier effects?, Anais da Academia Brasileira de Ciê. 2016. Vol. 88 (1 Suppl.). P. 451–466. DOI: 10.1590/0001-3765201620140631

Stevens R. D., Willing M. R. Community structure, abundance, and morphology, OIKOS. 2000. Vol. 88. P. 48–56.

Tumanov I. L. Factors of the morphological diversity of craniometric features of the American mink (Neovison vison), Rossiyskiy zhurnal biologicheskih invaziy. 2014. No. 4. P. 30–54.

Vasil'ev A. G. Bol'shakov V. N. Malafeev Yu. M. Valyaeva E. A. Evolutionary-ecological processes in muskrat populations during acclimatization in the conditions of the North, Ekologiya. 1999. No. 6. P. 433–441.

Vasil'ev A. G. Bol'shakov V. N. Sineva N. V. Remote morphogenetic consequences of muskrat acclimatization in Western Siberia, Doklady Akademii nauk. 2014. T. 455. No. 4. P. 478–480.

Vasil'ev A. G. Bol'shakov V. N. Vasil'eva I. A. Sineva N. V. Consequences of the introduction of muskrats in Western Siberia: the morphofunctional aspect, Rossiyskiy zhurnal biologicheskih invaziy. 2016. No. 4. P. 2–13.

Vasil'eva I. A. Vasil'ev A. G. Bol'shakov V. N. Morphological divergence of rocky voles of the subgenus Aschizomys (Rodentia, Cricetidae), Zoologicheskie issledovaniya, Pod red. I. Ya. Pavlinova, M. V. Kalyakina. M.: Izd-vo Mosk. un-ta, 2008. P. 210–255.

Zaharov V. M. Zhdanova N. P. Kirik E. F. Shkil' F. N. Ontogenesis and population: an assessment of the stability of development in natural populations, Ontogenez. 2001. T. 32. No. 6. P. 404–421.

Zaharov V. M. Ontogenesis and population (developmental stability and population variability), Ekologiya. 2001. No. 3. P. 177–191.

Zelditch M. L., Swiderski D. L., Sheets H. D., & Fink W. L. Introduction, Geometric Morphometrics for Biologists. 2004. P. 1–20.

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