Phylogeographic differentiation in Sorex araneus: morphology in relation to geography and karyotype

Phylogeographic differentiation in Sorex araneus: morphology in relation to geography and karyotype

Polly P.D.

P. 073-084

Findings of gene flow across hybrid zones between karyotypic races of the common shrew, Sorex araneus Linnaeus, 1758, have contributed to the debate over the role of chromosomal changes in speciation. The correlation between chromosomal and morphological evolution was examined here across the full geographic range of the species. Previous studies on selected karyotypic races yielded ambiguous results: some found significant differences between races, but others concluded that local variation was more important than karyotype for morphological structuring. Forty three samples, representing 24 karyotypic races and three species were studied here. Geometric morphometrics were used to determine whether karyotypic, geographic or population-level structuring was present in the size and shape of molars, skulls and mandibles. Significant structuring was found in all traits among populations, among karyotypic races, among phylogenetic groups of karyotypic races and among species, greatest among populations (FST ranged from 0.08 to 0.11) and groups (FST 0.04 to 0.15). Within S. araneus structuring was greater in skull centroid size and molar shape than in skull or mandible shape. Large-scale east-to-west clines were found in molar and skull shape. The skull cline is probably associated with changes in the frequency of the upper fifth antemolar. Mandible shape was not highly differentiated between karyotypic races compared to molar shape, but it was better at discriminating among karyotypic groups and species. It is likely that fossil specimens can be determined to the level of karyotypic group, but not to a specific karyotypic race.DOI: 10.15298/rusjtheriol.6.1.11

Literature
  • Andersson A.-C. 2004. Postglacial population history of the common shrew (Sorex araneus) in Fennoscandia: molecular studies of recolonization, sex-biased gene flow, and the formation of chromosome races // Comprehensive Summaries of Uppsala Dissertations of the Faculty of Science and Technology. Vol.986. Acta Universitatis Upsaliensis, Uppsala.
  • Andersson A.-C., Narain Y., Tegelström H. & Fredga K. 2004. No apparent reduction of gene flow in a hybrid zone between the West and North European karyotypic groups of the common shrew, Sorex araneus // Molecular Ecology. Vol.13. P.1205-1215.
  • Balloux F., Brünner H., Lugon-Moulin N., Hausser J. & Goudet J. 2003. Microsatellites can be misleading: an empirical and simulation study // Evolution. Vol.54. P.1414-1422.
  • Banaszek A., Smakulska J., Fedyk S., Jadwiszczak K.A. & Chętnicki W. 2003. Morphometric differentiation of shrews (Sorex araneus L., 1758) from the hybrid zone between the Guzowy Młyn and Łęgucki Młyn chromosome races in Poland // Mammalia. Vol.68. P.217-224.
  • Bannikova A.A., Bulatova N.S., Krysanov E.Y. & Kramerov D.A. 2003. DNA polymorphism within Sorex araneus and two congeneric species as inferred from inter-SINE-PCR // Mammalia. Vol.68. P.263-274.
  • Bengtsson O. & Frykman I. 1990. Karyotype evolution: evidence from the common shrew (Sorex araneus L.) // Journal of Evolutionary Biology. Vol.3. P.85-101.
  • Bookstein F.L. 1991. Morphometric Tools for Landmark Data. Cambridge: Cambridge University Press.
  • Brünner H., Lugon-Moulin N., Balloux F., Fumagalli L. & Hausser J. 2002. A taxonomical re-evaluation of the Valais chromosome race of the common shrew Sorex araneus (Insectivora: Soricidae) // Acta Theriologica. Vol.47. P.245-275.
  • Caumul R. & Polly P.D. 2005. Comparative phylogenetic and environmental components of morphological variation: skull, mandible and molar shape in marmots (Marmota, Rodentia) // Evolution. Vol.59. P.2460-2472.
  • Churchfield S. 1990. The Natural History of Shrews. Ithaca, New York: Comstock Publishing Associates.
  • Corbet G.B., Southern H.N. 1977. The Handbook of British Mammals. Oxford: Blackwell Scientific Publications.
  • Dryden I.L & Mardia K.V. 1998. Statistical Analysis of Shape. New York: John Wiley & Sons.
  • Fivaz F., Basset P., Lugon-Moulin N. & Hausser J. 2003. Postglacial recolonization of the Valais (Switzerland) by the shrew Sorex antinorii: Is dispersal sex-biased? A preliminary study // Mammalia. Vol.68. P.253-362.
  • Fredga K. 1996. The chromosome races of Sorex araneus in Scandinavia // Hereditas. Vol.125. P.123-135.
  • Frykman I. & Bengtsson B.O. 1984. Genetic differentiation in Sorex. III. Electrophoretic analysis of a hybrid zone between two karyotypic races in Sorex araneus // Hereditas. Vol.100. P.259-270.
  • Frykman I., Simonsen V. & Bengtsson B.O. 1983. Genetic differentiation in Sorex. I. Electrophoretic analysis of the karyotypic races of Sorex araneus in Sweden // Hereditas. Vol.99. P.279-292.
  • Halkka L., Söderlund V., Skarén U. & Heikkilä J. 1987. Chromosomal polymorphism and racial evolution of Sorex araneus L. in Finland // Hereditas. Vol.106. P.257-275.
  • Hausser J. & Jammot D. 1974. Etude biométrique des mâchoires chez les Sorex du groupe araneus en Europe continentale (Mammalia, Insectivora) // Mammalia. Vol.38. P. 324-343.
  • Hausser J. 1994. The Sorex of the araneus-arcitcus group (Mammalia: Soricidae): do they actually speciate? // Merrit J.F., Kirkland G.L., Jr. & Rose R.K. (eds.). Advances in the Biology of Shrews. Carnegie Museum of Natural History Special Publication. Vol.8. P.295-306.
  • Hausser J., Hutterer R. & Vogel P. 1990. Sorex araneus Linnaeus, 1758 - Waldspitzmaus. // Niethammer J. & Krapp F. (eds.). Handbuch der Säugetiere Europas. Wiesbaden: AULA-Verlag. P.237-278.
  • Homolka M. 1980. Biometrischer Vergleich zweier Populationen Sorex araneus // Acta Scientiarum Naturalium Academiae Scientiarum Bohemicae Brno. Vol.14. P.1-34.
  • Ivanitskaya E. 1994. Comparative cytogenetics and systematics of Sorex: a cladistic approach // Merrit J.F., Kirkland G.L., Jr. & Rose R.K. (eds.), Advances in the Biology of Shrews. Carnegie Museum of Natural History Special Publication. Vol.8. P.313-323.
  • Lande R. 1992. Neutral theory of quantitative genetic variance in an island model with local extinction and colonization // Evolution. Vol.46. P.381-389.
  • Linnaeus C. 1758. Systema Naturae. 10th Edition. Stockholm: Laurentii Salvii.
  • Lougon-Moulin N., Balloux F., & Hausser J. 2000. Genetic differentiation of common shrew Sorex araneus populations among different alpine valleys revealed by microsatellites // Acta Theriologica. Vol.45. Suppl.1. P.103-117.
  • Manly B.F.J. 1991. Randomization, Bootstrap and Monte Carlo Methods in Biology. New York: Chapman and Hall.
  • Ochocińska D. & Taylor J.R.E. 2003. Bergmann's rule in shrews: geographical variation of body size in Palearctic Sorex species // Biological Journal of the Linnean Society. Vol.78. P.365-381.
  • Okulova N.M., Balakirev A.E. & Orlov V.N. 2004. [Craniometrical characteristics of some Sorex araneus (Insectivora) chromosomal races] // Zoologicheskii Zhurnal. Vol.83. P.1476-1487 [in Russian, with English summary]..
  • Polly P.D. 2001. On morphological clocks and paleophylogeography: Towards a timescale for Sorex hybrid zones // Genetica. Vol.112/113. P.339-357.
  • Polly P.D. 2003. Paleophylogeography of Sorex araneus: molar shape as a morphological marker for fossil shrews // Mammalia. Vol.68. P.233-243.
  • Polyakov A.V., Onischenko S.S., Ilyashenko V.B., Searle J.B. & Borodin P.M. 2002. Morphometric difference between the Novosibirsk and Tomsk chromosome races of Sorex araneus in a zone of parapatry // Acta Theriologica. Vol.47. P.381-387.
  • Polyakov A.V., Panov V.V., Ladygina T.Yu., Bochkarev M.N., Rodionova M.I. & Borodin P.M. 2001. Chromosomal evolution of the common shrew Sorex araneus L. from the southern Urals and Siberia in the postglacial period // Russian Journal of Genetics. Vol.37. P.351-357.
  • Ratkiewicz M., Banaszek A., Jadwiszczak K., Chętnicki W. & Fedyk S. 2003. Genetic diversity, stability of population structure and barriers to gene flow in a hybrid zone between two Sorex araneus chromosome races // Mammalia. Vol.68. P.275-283.
  • Ratkiewicz M., Fedyk S., Banaszek A., Chętnicki W., Szałaj K., Gielly L. & Taberlet P. 2002. The evolutionary history of the two karyotypic groups of the common shrew, Sorex araneus, in Poland // Heredity. Vol.88. P.235-242.
  • Reinwaldt E. 1961. Über Zahnanomalien und die Zahnformel der Gattung Sorex Linné // Arkiv för Zoologi. Vol.13. P.533-539.
  • Rohlf F.J. 1990. Rotational fit Procrustes methods // Rohlf F.J. & Bookstein F.L. (eds.). Proceedings of the Michigan Morphometrics Workshop, University of Michigan Museum of Zoology Special Publication. Vol.2. P.227-236.
  • Rohlf F.J. & Slice D. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks // Systematic Zoology. Vol.39. P.40-49.
  • Schmidt E. 1967. Unregelmässigkeiten der Zahl der Alveolen and den oberen einspitzigen Zähnen bei der Waldspitzmaus. // Acta Theriologica. Vol.12. P.665-689.
  • Searle J.B. 1984. Three new karyotypic races of the Common shrew Sorex araneus (Mammalia: Insectivora) and a phylogeny // Systematic Zoology. Vol.33. P.184-194.
  • Searle J.B. 1985. Isozyme variation in the common shrew (Sorex araneus) in Britain in relation to karyotype // Heredity. Vol.55. P.175-180.
  • Searle J.B., Hübner R., Wallace B.M.N. & Garagna S. 1990. Robertsonian variation in wild mice and shrews // Chromosomes Today. Vol.10. P.253-263.
  • Searle J.B. & Thorpe R.S. 1987. Morphometric variation of the Common shrew (Sorex araneus) in Britain in relation to karyotype and geography // Journal of Zoology. Vol.212. P.373-377.
  • Searle J.B. & Wójcik J.M. 1998. Chromosomal evolution: the case of Sorex araneus // Wójcik J.M. & Wolsan M. (eds.). Evolution of Shrews. Białowieża: Mammal Research Institute, Polish Academy of Sciences. P.173-218.
  • Skarén U. 1964. Variation in two shrews, Sorex unguiculatus Dobson and S. a. araneus L. // Annales Zoologici Fennici. Vol.1. P.94-124.
  • Sulkava S., Vahtola M. & Fredga K. 1985. Structure of the upper tooth-row of Sorex araneus in Scandinavia // Acta Zoologica Fennica. Vol.173. P.237-239.
  • Spitze K. 1993. Population structure in Daphnia obtusa: quantitative genetic and allozymic variation // Genetics. Vol.135. P.367-374.
  • Weir B.S. & Cockerham C.C. 1984. Estimating F-statistics for the analysis of population structure // Evolution. Vol.38. P.1358-1370.
  • White M.J.D. 1978. Modes of Speciation. San Francisco: W.H. Freeman and Company.
  • Wójcik J.M. 1993. Chromosome races of the common shrew Sorex araneus in Poland: a model of karyotype evolution // Acta Theriologica. Vol.38. P.315-338.
  • Wójcik J.M., Bogdanowicz W., Pucek Z., Wójcik A.M. & Zalewska H. 2000. Morphometric variation of the common shrew Sorex araneus in Poland in relation to karyotype // Acta Theriologica. Vol.45. Suppl.1. P.161-172.
  • Wójcik J.M., Borodin P.M., Fedyk S., Fredga K., Hausser J., Mishta A., Orlov V.N., Searle J.B., Volobouev V.T. & Zima J. 2003. The list of the chromosome races of the common shrew Sorex araneus (updated 2002) // Mammalia. Vol.67. P.169-178.
  • Wójcik J.M. & Wójcik A.M. 1994. Protein variation in the common shrew (Sorex araneus L.) in Poland in relation to karyotype // Folia Zoologica. Vol.43. Suppl.1. P.53-61.
  • Wójcik J.M., Wójcik A.M. & Sikorski M.D. 2003. Morphometric variation in the common shrew, Sorex araneus, in different habitats // Mammalia. Vol.67. P.225-231.
  • Wright S. 1951. The genetic structure of populations // Annals of Eugenics. Vol.15. P.323-354.
  • Zima J., Slivková L. & Tomáškova L. 2003. New data on karyotypic variation in the common shrew, Sorex araneus, from the Czech Republic: an extension of the range of the Laska race // Mammalia. Vol.67. P.209-215.