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Mammalian Biology

, Volume 78, Issue 4, pp 241–250 | Cite as

Geometric morphometrics on Greek house mouse populations (Mus musculus domesticus) with Robertsonian and all-acrocentric chromosomal arrangements

  • Maria KamilariEmail author
  • George Tryfonopoulos
  • Stella Fraguedakis-Tsolis
  • Basil Chondropoulos
Original Investigation

Abstract

This work aims to give the first comprehensive morphometric analysis of intraspecific variation for the different populations of the western house mouse (Mus musculus domesticus), in the Robertsonian (Rb) system of the N-NW Peloponnisos. Furthermore, we study all-acrocentric karyotype populations (2n = 40) of the species coming from several localities of Greece. We apply 2D shape analysis, i.e. landmark analysis and Elliptic Fourier Analysis, on the dorsal and ventral side of skull and the occlusal view of the first upper molar (M1), respectively. Although significant genetic divergence between typical and Rb populations and even ongoing speciation processes have been reported for this species, this was not the case for the Greek populations studied. However, our analyses herein reveal morphologically differentiated chromosome groups in N-NW Peloponnisos Rb system and a clear geographical discrimination of the all-acrocentric (2n = 40) populations for all characters studied. We suggest that in all-acrocentric (2n = 40) karyotype mice the geographical distance drives their differentiation while within the Rb system of N-NW Peloponnisos, karyotype is the key factor that acts on their phenotypic variation.

Keywords

Mus musculus domesticus Morphometrics Greece Rb system 

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References

  1. Angerbjorn, A., 1986. Gigantism in island populations of wood mice (Apodemus) in Europe. Oikos 47, 47–56.CrossRefGoogle Scholar
  2. Barciová, L., 2009. Advances in insectivore and rodent systematics due to geometric morphometrics. Mammal Rev. 39, 80–91.CrossRefGoogle Scholar
  3. Bergmann, C., 1847. Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Göttinger Studien. 3, 595–708.Google Scholar
  4. Bookstein, F.L., 1991. Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge University Press, New York.Google Scholar
  5. Bookstein, F.L., 1997. Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Med. Image Anal. 1, 225–243.PubMedCrossRefPubMedCentralGoogle Scholar
  6. Boursot, P., Din, W., Anand, R., Darviche, D., Dod, B., Vondeimling, F., Talwar, G.P., Bonhomme, F., 1996. Origin and radiation of the house mouse: mitochondrial DNA phylogeny. J. Evol. Biol. 9, 391–415.CrossRefGoogle Scholar
  7. Britton-Davidian, J., 1990. Genic differentiation in M. m. domesticus populations from Europe, the Middle-East and North-Africa – geographic patterns and colonization events. Biol. J. Linn. Soc. 41, 27–45.CrossRefGoogle Scholar
  8. Britton-Davidian, J., Catalan, J., Lopez, J., Ganem, G., Nunes, A.C., Ramalhinho, M.G., Auffray, J.C., Searle, J.B., Mathias, M.L., 2007. Patterns of genic diversity and structure in a species undergoing rapid chromosomal radiation: an allozyme analysis of house mice from the Madeira archipelago. Heredity 99, 432–442.PubMedCrossRefGoogle Scholar
  9. Cardini, A., O’Higgins, P., 2004. Patterns of morphological evolution in Marmota (Rodentia, Sciuridae): geometric morphometrics of the cranium in the context of marmot phylogeny, ecology and conservation. Biol. J. Linn. Soc. 82, 385–407.CrossRefGoogle Scholar
  10. Chondropoulos, B.P., Fraguedakis-Tsolis, S.E., Markakis, G., Giagia-Athanasopoulou, E., 1996. Morphometric variability in karyologically polymorphic populations of the wild Mus musculus domesticus in Greece. Acta Theriol. 41, 375–382.CrossRefGoogle Scholar
  11. Corti, M., Rohlf, F.J., 2001. Chromosomal speciation and phenotypic evolution in the house mouse. Biol. J. Linn. Soc. 73, 99–112.CrossRefGoogle Scholar
  12. Cucchi, T., 2008. Uluburun shipwreck stowaway house mouse: molar shape analysis and indirect clues about the vessel’s last journey. J. Archaeol. Sci. 35, 2953–2959.CrossRefGoogle Scholar
  13. D’ Anatro, A., Lessa, E.P., 2006. Geometric morphometric analysis of geographic variation in the Rio Negro tuco-tuco, Ctenomys rionegrensis (Rodentia: Ctenomyidae). Mammal. Biol. 71, 288–298.CrossRefGoogle Scholar
  14. Dallas, J.F., Bonhomme, F., Boursot, P., Britton-Davidian, J., Bauchau, V., 1998. Population genetic structure in a Robertsonian race of house mice: evidence from microsatellite polymorphism. Heredity 80, 70–77.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Dermitzakis, D.M.,1990. Paleogeography, geodynamic processes and event stratigraphy during the Late Cenozoic of the Aegean area. In: Proceedings of the International Symposium on: Biogeographical Aspects of Insularity. Academia Nazionale dei Lincei, 85, pp. 263–288.Google Scholar
  16. dos Reis, S.F., Duarte, L.C., Monteiro, L.R., Von Zuben, F.J., 2002. Geographic variation in cranial morphology in Thrichomys apereoides (Rodentia: Echimyidae). I. Geometric descriptors and patterns of variation in shape. J. Mammal. 83, 333–344.Google Scholar
  17. Ellison, G.T.H., Taylor, P.J., Nix, H.A., Bronner, G.N., McMahon, J.P., 1993. Climatic adaptation of body-size among pouched mice (Saccostomus campestris: Cricetidae) in the southern African subregion. Global Ecol. Biogeogr. 3, 41–47.CrossRefGoogle Scholar
  18. Erlinge, S., 1987. Why do European stoats Mustela erminea not follow Bergmann’s rule? Holarct. Ecol. 10, 33–39.Google Scholar
  19. Escudé, É., Renvoisé, É., Lhomme, V., Montuire, S., 2012. Why all vole molars (Arvicolinae, Rodentia) are informative to be considered as proxy for Quaternary paleoenvironmental reconstructions. J. Archaeol. Sci.,  https://doi.org/10.1016/j.jas.2012.03.003.CrossRefGoogle Scholar
  20. Ferris, S.D., Sage, R.D., Huang, C.M., Nielsen, J.T., Ritte, U., Wilson, A.C., 1983. Flow of mitochondrial DNA across a species boundary. Proc. Natl. Acad. Sci. U.S.A. 80, 2290–2294.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Ferson, S., Rohlf, F.J., Koehn, R.K., 1985. Measuring shapes variation of two-dimensional outlines. Syst. Zool. 34, 59–68.CrossRefGoogle Scholar
  22. Förster, D.W., Gündüz, I., Nunes, A.C., Gabriel, S., Ramalhinho, M.G., Mathias, M.L., Britton-Davidian, J., Searle, J.B., 2009. Molecular insights into the coloniza-tion and chromosomal diversification of Madeiran house mice. Mol. Ecol. 18, 4477–4494.PubMedCrossRefGoogle Scholar
  23. Fraguedakis-Tsolis, S.E., Chondropoulos, B.P., Stamatopoulos, C.V., Giokas, S., 2009. Morphological variation of the five vole species of the genus Microtus (Mammalia, Rodentia, Arvicolinae) occurring in Greece. Acta Zool. 90, 254–264.CrossRefGoogle Scholar
  24. Gündüz, I., Rambau, R.V., Tez, C., Searle, J.B., 2005. Mitochondrial DNA variation in the western house mouse (Mus musculus domesticus) close to its site of origin: studies in Turkey. Biol. J. Linn. Soc. 84, 473–485.CrossRefGoogle Scholar
  25. Hallgrimsson, B., Lieberman, D.E., Liu, W., Ford-Hutchinson, A.F., Jirik, F.R., 2007. Epigenetic interactions and the structure of phenotypic variation in the cranium. Evol. Dev. 9, 76–91.PubMedCrossRefGoogle Scholar
  26. Hauffe, H.C., Fraguedakis-Tsolis, S., Mirol, P.M., Searle, J.B., 2002. Studies of mito-chondrial DNA, allozyme and morphometric variation in a house mouse hybrid zone. Genet. Res. 80, 117–129.PubMedCrossRefGoogle Scholar
  27. Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G., Jarvis, A., 2005. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978.CrossRefGoogle Scholar
  28. Iwata, H., Ukai, Y., 2002. SHAPE: a computer program package for quantitative evaluation of biological shapes based on elliptic Fourier descriptors. J. Hered. 93, 384–385.PubMedCrossRefGoogle Scholar
  29. Kamilari, M., Sfenthourakis, S., 2009. A morphometric approach to the geographic variation of the terrestrial isopod species Armadillo tuberculatus (Isopoda: Oniscidea). J. Zool. Syst. Evol. Res. 47, 219–226.CrossRefGoogle Scholar
  30. Klingenberg, C.P., Leamy, L.J., Routman, E.J., Cheverud, J.M., 2001. Genetic architecture of mandible shape in mice: effects of quantitative trait loci analyzed by geometric morphometrics. Genetics 157, 785–802.PubMedPubMedCentralGoogle Scholar
  31. Kuhl, F.P., Giardina, C.R., 1982. Elliptic Fourier features of a closed contour. Comput. Graph. Image Proc. 18, 236–258.CrossRefGoogle Scholar
  32. 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. Am. Nat. 153, 201–214.PubMedCrossRefPubMedCentralGoogle Scholar
  33. Ledevin, R., Michaux, J.R., Deffontaine, V., Henttonen, H., Renaud, S., 2010. Evolutionary history of the bank vole Myodes glareolus: a morphometric perspective. Biol. J. Linn. Soc. 100, 681–694.CrossRefGoogle Scholar
  34. Lomolino, M.V., 2005. Body size evolution in insular vertebrates: generality of the island rule. J. Biogeogr. 32, 1683–1699.CrossRefGoogle Scholar
  35. Marriner, N., Morhange, C., 2007. Geoscience of ancient Mediterranean harbours. Earth Sci. Rev. 80, 137–194.CrossRefGoogle Scholar
  36. Marriner, N., Morhange, C., Carayon, N., 2008. Ancient Tyre and its harbours: 5000 years of human-environment interactions. J. Archaeol. Sci. 35, 1281–1310.CrossRefGoogle Scholar
  37. McLellan, T., Endler, J.A., 1998. The relative success of some methods for measuring and describing the shape of complex objects. Syst. Biol. 47, 264–281.CrossRefGoogle Scholar
  38. Meiri, S., Dayan, T., 2003. On the validity of Bergmann’s rule. J. Biogeogr. 30, 331–351.CrossRefGoogle Scholar
  39. Meiri, S., Dayan, T., Simberloff, D., 2004. Carnivores, biases and Bergmann’s rule. Biol. J. Linn. Soc. 81, 579–588.CrossRefGoogle Scholar
  40. Michaux, J., Cucchi, T., Renaud, S., Garcia-Talavera, F., Hutterer, R., 2007. Evolution of an invasive rodent on an archipelago as revealed by molar shape analysis: the house mouse in the Canary Islands. J. Biogeogr. 34, 1412–1425.CrossRefGoogle Scholar
  41. Millien, V., 2006. Morphological evolution is accelerated among island mammals. PLoS Biol. 4, e321.PubMedPubMedCentralCrossRefGoogle Scholar
  42. Mitsainas, G.P., Giagia-Athanasopoulou, E.B., 2005. Studies on the Robertsonian chromosomal variation of Mus musculus domesticus (Rodentia, Muridae) in Greece. Biol. J. Linn. Soc. 84, 503–513.CrossRefGoogle Scholar
  43. Morgan, C.C., Verzi, D.H., 2006. Morhological diversity of the humerus of the south American subterranean rodent Ctenomys (Rodentia, Ctnomyidae). J. Mammal. 87, 1252–1260.CrossRefGoogle Scholar
  44. Munoz˜-Munoz,˜ F., Sans-Fuentes, M.A., Lopez-Fuster, M.J., Ventura, J., 2011. Evolutionary modularity of the mouse mandible: dissecting the effect of chromosomal reorganizations and isolation by distance in a Robertsonian system of Mus musculus domesticus. J. Evol. Biol. 24, 1763–1776.CrossRefGoogle Scholar
  45. Nachman, M.W., Searle, J.B., 1995. Why is the house mouse karyotype so variable. Trends Ecol. Evol. 10, 397–402.PubMedCrossRefGoogle Scholar
  46. Navarro, M., Britton-Davidian, J., 1989. Genetic-structure of insular Mediterranean populations of the house mouse. Biol. J. Linn. Soc. 36, 377–390.CrossRefGoogle Scholar
  47. Niethhammer, J., Krapp, F., 1978. Handbuch der saugetiere Europas, Band I. Rodentia I. Akademiche Verlagsgesellschaft, Wiesbaden, Germany.Google Scholar
  48. Piálek, J., Hauffe, H.C., Searle, J.B., 2005. Chromosomal variation in the house mouse. Biol. J. Linn. Soc. 84, 535–563.CrossRefGoogle Scholar
  49. Rajabi-Maham, H., Orth, A., Bonhomme, F., 2008. Phylogeography and postglacial expansion of Mus musculus domesticus inferred from mitochondrial DNA coalescent, from Iran to Europe. Mol. Ecol. 17, 627–641.PubMedCrossRefGoogle Scholar
  50. Renaud, S., Auffray, J.C., 2010. Adaptation and plasticity in insular evolution of the house mouse mandible. J. Zool. Syst. Evol. Res. 48, 138–150.CrossRefGoogle Scholar
  51. Rohlf, F.J., Archie, J.W., 1984. A comparison of Fourier methods for the description of wing shape in mosquitoes (Diptera: Culicidae). Syst. Zool. 33, 302–317.CrossRefGoogle Scholar
  52. Rohlf, F.J., 2004. TPSSplin. https://doi.org/life.bio.sunysb.edu/morph/
  53. Rohlf, F.J., 2010. TPSDig; TPSRelw. https://doi.org/life.bio.sunysb.edu/morph/
  54. Ryan, A.W., Montgomery, W.I., Duke, E.J., 2000. Microgeographic distribution of house mouse, Mus domesticus, mitochondrial DNA types on farland in North-East Ireland. Biol. Environ. Proc. R. Irish Acad. 100, 159–163.Google Scholar
  55. Saïd, K., Britton-Davidian, J., 1991. Genetic differentiation and habitat partition of Robertsonian house mouse populations (Mus musculus domesticus) of Tunisia. J. Evol. Biol. 4, 409–427.CrossRefGoogle Scholar
  56. Sans-Fuentes, M.A., Ventura, J., Lopez-Fuster, M.J., Corti, M., 2009. Morphological variation in house mice from the Robertsonian polymorphism area of Barcelona. Biol. J. Linn. Soc. 97, 555–570.CrossRefGoogle Scholar
  57. Schneider, C.A., Rasband, W.S., Eliceiri, K.W., 2012. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods, 671.PubMedPubMedCentralCrossRefGoogle Scholar
  58. Scotland, R.W., Olmstead, R.G., Bennett, J.R., 2003. Phylogeny reconstruction: the role of morphology. Syst. Biol. 52, 539–548.PubMedCrossRefGoogle Scholar
  59. Sundell, J., Norrdahl, K., 2002. Body size-dependent refuges in voles: an alternative explanation of the Chitty effect. Ann. Zool. Fenn. 39, 325–333.Google Scholar
  60. Tichy, H., Vucak, I., 1987. Chromosomal polymorphism in the house mouse (Musdomesticus) of Greece and Yugoslavia. Chromosoma 95, 31–36.PubMedCrossRefGoogle Scholar
  61. Tryfonopoulos, G., Chondropoulos, B., Fraguedakis-Tsolis, S., 2005a. Allozymic polymorphism among 14 populations of the house mouse, Mus musculus domesticus, from Greece. Biochem. Genet. 43, 11–24.PubMedCrossRefGoogle Scholar
  62. Tryfonopoulos, G.A., Chondropoulos, B.R., Fraguedakis-Tsolis, S.E., 2005b. Mitochondrial DNA polymorphisms of the house mouse Mus musculus domesticus from Greece, focusing on the Robertsonian chromosomal system of north-west Peloponnese. Biol. J. Linn. Soc. 84, 643–651.CrossRefGoogle Scholar
  63. Whittaker, R., 1998. Island Biogeography: Ecology, Evolution, and Conservation. Oxford University Press, UK.Google Scholar
  64. Wiens, J.J., 2004. The role of morphological data in phylogeny reconstruction. Syst. Biol. 53, 653–661.PubMedCrossRefGoogle Scholar
  65. Winking, H., Gropp, A., Bulfield, G., 1981. Robertsonian chromosomes in mice from North-eastern Greece. Mouse News Lett. 64, 69–70.Google Scholar
  66. Yom-Tov, Y., Geffen, E., 2006. Geographic variation in body size: the effects of ambient temperature and precipitation. Oecologia 148, 213–218.CrossRefGoogle Scholar
  67. Zalewski, A., Harrison, D.J., Fuller, A.K., Proulx, G., 2004. Geographical and seasonal variation in food habits and prey size of European pine martens. In: Harrison, D.J., Fuller, A.K., Proulx, G. (Eds.), In Martens and Fishers (Martes) in Human-altered Environments. Springer Science & Business Media: Springer-Verlag, New York, USA, pp. 77–98.Google Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2013

Authors and Affiliations

  • Maria Kamilari
    • 1
    Email author
  • George Tryfonopoulos
    • 1
  • Stella Fraguedakis-Tsolis
    • 1
  • Basil Chondropoulos
    • 1
  1. 1.Section of Animal Biology, Department of BiologyUniversity of PatrasPatrasGreece

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