Skull modularity of the European ground squirrel Spermophilus citellus (Linnaeus, 1766)
DOI:
https://doi.org/10.14720/abs.57.1.15542Keywords:
neurocranium, viscerocranium, ontogeny, allometry, Escoufier RV, morphological integration, geometric morphometricsAbstract
The skull is a complex structure that has frequently been studied for the patterns of morphological integration and modularity. The ventral side of the skull can be divided into two functional modules, the neurocranium composed of the braincase, eyes and ears, and the viscerocranium composed of the jaw apparatus. The aim of this study was to test the ventral cranium of the European ground squirrel Spermophilus citellus(Linnaeus, 1766) for this partitioning as sciurid skull is believed to be highly integrated without clear divisions into subunits. Additionally, I compared the degree of modularity between juveniles and adults. Hypothesized modularity was tested on 159 (43 juveniles and 116 adults)skulls by applying geometric morphometric method based on Escoufier RV coefficient. In adults, the results yielded strong support to the hypothesis that the viscerocranium and neurocranium are separate modules. In juveniles, two-module organization of the skull was also confirmed, but the hypothesized modules were much more integrated with each other. Although allometry can be a strong integrating factor, it had very little influence on the hypothesized modularity of the S. citellus skull. A permutation test for the difference in the degree of modularity between juveniles and adults was marginally significant. The change in the strength of integration between the viscerocranium and neurocranium in the S. citellus skull during ontogeny, with the higher level of modularity in adults than in juveniles, is probably a consequence of the transition from suckling to gnawing of food and greater specialisation of the two functional modules.
References
Bookstein, F.L., 1991. Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge University Press, Cambridge, 435 pp. DOI: https://doi.org/10.1017/CBO9780511573064
Cardini, A., Tongiorgi, P., 2003. Yellow-bellied marmots (Marmota flaviventris) ‘in the shape space’ (Rodentia, Sciuridae): sexual dimorphism, growth and allometry of the mandible. Zoomorphology, 122, 11-23. DOI: https://doi.org/10.1007/s00435-002-0063-y
Cheverud, J.M., 1995. Morphological integration in the saddleback tamarin (Saguinus fuscicollis) DOI: https://doi.org/10.1086/285728
cranium. American Naturalist, 145, 63-89.
Drake, A.G., Klingenberg, C.P., 2010. Large-scale diversification of skull shape in domestic dogs: disparity and modularity. American Naturalist, 175, 289-301. DOI: https://doi.org/10.1086/650372
Emerson, S.B., Bramble, D.M., 1993. Scaling, allometry and skull design. In: Hanken, J., Hall, B.K. (eds.): The Skull. The University of Chicago Press, Chicago, pp. 384-416.
Escoufier, Y., 1973. Le traitement des variables vectorielles. Biometrics, 29, 751-760. DOI: https://doi.org/10.2307/2529140
Fruciano, C., Franchini, P., Meyer, A., 2013. Resampling-based approaches to study variation in morphological modularity. PLoS ONE 8(7), e69376. DOI: https://doi.org/10.1371/journal.pone.0069376
Gonzalez, P.N., Hallgrímsson, B., Oyhenart, E.E., 2011. Developmental plasticity in covariance structure of the skull: effects of prenatal stress. Journal of Anatomy, 218, 243-257. DOI: https://doi.org/10.1111/j.1469-7580.2010.01326.x
González-José, R., Escapa, I., Neves, W.A., Cúneo, R., Pucciarelli, H.M., 2008. Cladistic analysis of continuous modularized traits provides phylogenetic signals in Homo evolution. Nature, 453, 775-778. DOI: https://doi.org/10.1038/nature06891
Goswami, A., Polly, P.D., 2010. Methods for studying morphological integration and modularity. In: Alroy, J., Hunt, G. (eds.): Quantitative Methods in Paleobiology, Paleontological Society Special Publications, 16. Yale University Printing and Publishing Services, New Haven, CT, pp. 213-243. Hallgrímsson, B., Brown, J.J.Y., Ford-Hutchinson, A.F., Sheets, H.D., Zelditch, M.L., Jirik, F.R., 2006. DOI: https://doi.org/10.1017/S1089332600001881
The brachymorph mouse and the developmental-genetic basis for canalization and morphological integration. Evolution and Development, 8, 61-73. DOI: https://doi.org/10.1111/j.1525-142X.2006.05075.x
Hallgrímsson, B., Jamniczky, H., Young, N.M., Rolian, C., Parsons, T.E., Boughner, J.C., Marcucio, R.S., 2009. Deciphering the palimpsest: studying the relationship between morphological inte- gration and phenotypic covariation. Evolutionary Biology, 36, 355-376. DOI: https://doi.org/10.1007/s11692-009-9076-5
Herring, S.W., 1993. Epigenetic and functional influences on skull growth. In: Hanken, J., Hall, B.K. (eds.): The Skull. The University of Chicago Press, Chicago, pp. 237-271.
Ivanović, A., Kalezić, M.L., 2010. Testing the hypothesis of morphological integration on a skull of a vertebrate with a biphasic life cycle: a case study of the alpine newt. Journal of Experimental Zoology Part B Molecular and Developmental Evolution, 314B, 527-538. DOI: https://doi.org/10.1002/jez.b.21358
Jojić, V., Blagojević. J., Ivanović, A., Bugarski-Stanojević, V., Vujošević, M., 2007. Morphological integration of the mandible in yellow-necked field mice: the effects of B chromosmes. Journal of Mammalogy, 88, 689-695. DOI: https://doi.org/10.1644/06-MAMM-A-019R1.1
Jojić, V., Blagojević, J., Vujošević, M., 2011. B chromosomes and cranial variability in yellow-necked field mice (Apodemus flavicollis). Journal of Mammalogy, 92, 396-406. DOI: https://doi.org/10.1644/10-MAMM-A-158.1
Jojić V., Blagojević J., Vujošević M., 2012. Two-module organization of the mandible in the yellow- necked mouse: a comparison between two different morphometric approaches. Journal of Evo- lutionary Biology, 25, 2489-2500. DOI: https://doi.org/10.1111/j.1420-9101.2012.02612.x
Klenovšek, T., Kryštufek, B., 2013. An ontogenetic perspective on the study of sexual dimorphism, phylogenetic variability, and allometry of the skull of European ground squirrel, Spermophilus citellus (Linnaeus, 1766). Zoomorphology, 132(4), 433-445. DOI: https://doi.org/10.1007/s00435-013-0196-1
Klingenberg, C.P., 2008. Morphological integration and developmental modularity. Annual Review of Ecology, Evolution and Systematics, 39, 115-132. DOI: https://doi.org/10.1146/annurev.ecolsys.37.091305.110054
Klingenberg, C.P., 2009. Morphometric integration and modularity in configurations of landmarks: Tools for evaluating a-priori hypotheses. Evolution and Development, 11, 405-421. DOI: https://doi.org/10.1111/j.1525-142X.2009.00347.x
Klingenberg, C.P., 2011. MorphoJ: an integrated software package for geometric morphometrics. DOI: https://doi.org/10.1111/j.1755-0998.2010.02924.x
Molecular Ecology Resources, 11, 353-357.
Klingenberg, C.P., 2013. Cranial integration and modularity: insights into evolution and development from morphometric data. Hystrix, 24, 43-58.
Klingenberg, C.P., Badyaev, A.V., Sowry, S.M., Beckwith, N.J. 2001. Inferring developmental modular- ity from morphological integration: analysis of individual variation and asymmetry in bumblebee wings. American Naturalist, 157, 11-23. DOI: https://doi.org/10.1086/317002
Klingenberg, C.P., Leamy, L.J., 2001. Quantitative genetics of geometric shape in the mouse mandible. Evolution, 55, 2342-2352. DOI: https://doi.org/10.1111/j.0014-3820.2001.tb00747.x
Klingenberg, C.P., Leamy, L.J., Cheverud, J.M., 2004. Integration and modularity of quantitative trait locus effects on geometric shape in the mouse mandible. Genetics, 166, 1909-1921. DOI: https://doi.org/10.1093/genetics/166.4.1909
Klingenberg, C.P., Zaklan, S.D., 2000. Morphological integration between developmental com- partments in the Drosophila wing. Evolution 54: 1273-1285. DOI: https://doi.org/10.1111/j.0014-3820.2000.tb00560.x
Leamy, L.J., Routman, E.J., Cheverud, J.M., 1999. Quantitative trait loci for early- and late developing skull characters in mice: a test of the genetic independence model of morphological integration. American Naturalist, 153, 201-214. DOI: https://doi.org/10.1086/303165
Marroig, G., Cheverud, J.M., 2001. A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of New World monkeys. Evolution, 55, 2576-2600. DOI: https://doi.org/10.1111/j.0014-3820.2001.tb00770.x
Monteiro, L.R., Lessa, L.G., Abe, A.S., 1999. Ontogenetic Variation in Skull Shape of Thrichomys apereoides (Rodentia: Echimyidae). Journal of Mammalogy, 80, 102-111. DOI: https://doi.org/10.2307/1383212
Olson, E.C., Miller, R.L. 1958: Morphological Integration. University of Chicago Press, Chicago, 376 pp.
Ramos-Lara, N., Koprowski, J.L., Kryštufek, B., Hoffmann, I.E., in press. Spermophilus citellus (Rodentia: Sciuridae). Mammalian Species.
Rohlf, F.J., 2010. TpsDig2, Version 2.16. Ecology & Evolution. SUNY at Stony Brook.
Rohlf, F.J., Slice, D.E., 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39, 40-59. DOI: https://doi.org/10.2307/2992207
Roth, V.L., 1996. Cranial Integration in the Sciuridae. American Zoologist, 36, 14-23. DOI: https://doi.org/10.1093/icb/36.1.14
Ružić, A., 1966. Određivanje uzrasnih kategorija u populaciji tekunice Citellus citellus. Arhiv bioloških nauka, XVIII, 1/1966, Beograd.
SPSS Statistics, 2008. Version 17.0. IBM Corporation.
Sun, Z., Lee, E., Herring, S.W., 2004. Cranial sutures and bones: growth and fusion in relation to masticatory strain. Anatomical Record Part A, 276A, 150-161. DOI: https://doi.org/10.1002/ar.a.20002
Swiderski, D.L., Zelditch, M.L., 2010. Morphological diversity despite isometric scaling of lever arms. Evolutionary Biology, 37, 1-18. DOI: https://doi.org/10.1007/s11692-010-9081-8
Willmore, K.E., Leamy, L., Hallgrímsson, B., 2006. Effects of developmental and functional interactions on mouse cranial variability through late ontogeny. Evolution and Development, 8(6), 550-567. DOI: https://doi.org/10.1111/j.1525-142X.2006.00127.x
Young, R.L., Badyaev, A.V., 2007. Evolution of ontogeny: linking epigenetic remodeling and genetic adaptation in skeletal structures. Integrative and Comparative Biology, 47, 234-244. DOI: https://doi.org/10.1093/icb/icm025
Zelditch, M.L., Mezey, J.G., Sheets, H.D., Lundrigan, B.L., Garland, T.Jr., 2006. Developmental regulation of skull morphology II: ontogenetic dynamics of covariance. Evolution and Deve- lopment, 8, 46-60. DOI: https://doi.org/10.1111/j.1525-142X.2006.05074.x
Downloads
Published
Issue
Section
License
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.