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Type: Articles
Published: 2006-06-23
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A new endemic species of the subgenus Mus (Rodentia, Mammalia) on the Island of Cyprus

CNRS- Muséum National d’Histoire Naturelle- Département Ecologie et Gestion de la Biodiversité-UMR 5197 « Archéozoologie, histoire des sociétés humaines et de peuplements animaux ». Bât. d’Anatomie comparée-55 rue Buffon, France
Génome, Populations, Interactions, Adaptation », UMR 5171 CNRS-IFREMER-UM2, CC063, Université Montpellier 2, 34095 Montpellier cedex 05, France
Institut des Sciences de l’Evolution CC064, Université Montpellier 2, 34095 Montpellier cedex 5, France
Paléoenvironnements et Paléobiosphère », UMR 5125 CNRS Université Lyon 1, Bât. Géode, 2 rue Dubois, Campus de la Doua, 69622 Villeurbanne, France
NRAP - CBAE UMR 5059 CNRS, 163 rue A. Broussonnet, 34090 MONTPELLIER Cedex
Institut des Sciences de l’Evolution CC064, Université Montpellier 2, 34095 Montpellier cedex 5, France
Ministry of the Interior, Nicosia, 1453 Cyprus
Génome, Populations, Interactions, Adaptation », UMR 5171 CNRS-IFREMER-UM2, CC063, Université Montpellier 2, 34095 Montpellier cedex 05, France
CNRS- Muséum National d’Histoire Naturelle- Département Ecologie et Gestion de la Biodiversité-UMR 5197 « Archéozoologie, histoire des sociétés humaines et de peuplements animaux ». Bât. d’Anatomie comparée-55 rue Buffon, France
Mammalia Rodent insular syndrome Landmarks Fourier analysis DNA

Abstract

The house mouse (Mus musculus domesticus) and the short-tailed mouse of the eastern Mediterranean area (M. macedonicus) were thought to live sympatrically on Cyprus Island. Recently, a phylogenetic survey has shown that the non-commensal mouse of Cyprus was an unknown sister species of European wild mice. Here, we describe this new species of the genus Mus (Rodentia, Mammalia), namely Mus cypriacus sp. n., based on 19 specimens trapped in the southern part of Cyprus. These animals were first compared to Eurasian species of mice using both molecular genetics (complete D-loop sequences and nuclear gene intron) and cytogenetics to state on its systematic status. Then classical and geometric morphometric analyses on both cranial and dental characters have been performed to compare Mus cypriacus with circum-Mediterranean species and provide diagnositic morphological characters. Genetic data strongly support a sister species relationship of the new species to M. macedonicus, the closest mainland taxon. Morphometric analyses provide satisfying criteria for diagnosis of this species relative to other Mediterranean species. The most obvious phenotypic characteristics are its long tail and the allometric gigantism and shape robustness of its cranial and dental characters compared to other Mediterranean mice. The molecular clock and the history of the murine settlement on Cyprus are congruent and suggest that the common ancestor of M. cypriacus and M. macedonicus arrived on Cyprus during the Middle Pleistocene by a founder event on natural raft. The remoteness of Cyprus through time has prevented introgression from the mainland gene pool, and favoured phenotypic adaptation to competition release, leading to the allopatric speciation of M. cypriacus.

References

  1. Adler, G.H. & Levins, R. (1994) The island syndrome in rodent populations. The Quarterly Review of Biology, 64, 473–490.

    Atchley, W.R., Ruttledge, J.J. & Cowley, D.E. (1982) A multivariate statistical analysis of direct and correlated response to selection in the rat. Evolution, 36, 677–678.

    Auffray, J.C., Alibert, P., Latieule, C. & Dod, B. (1996) Relative warp analysis of skull shape across the hybrid zone of the house mouse (Mus musculus) in Denmark. Journal of Zoology, 240, 441–455.

    Auffray, J-C., Marshall, J.T., Bonhomme, F. & Thaler, L. (1990) Focus on the nomenclature of european species of Mus. Mouse Genome, 88, 7–8.

    Auffray, J.-C., Orth, A., Catalan, J., Gonzalez, J.-P., Desmarais, E. & Bonhomme, F. (2003) Phylogenetic position and description of subgenus Mus (Rodentia, Mammalia) from Thailand. Zoologica Scripta, 32, 119–127.

    Barome, P.O., Monnerot, M. & Gautun, J.C. (2000) Phylogeny of the genus Acomys (Rodentia, Muridae) based on the cytochrome b mitochodrial gene: implications on taxonomy and phylogeography. Mammalia, 64, 423–438.

    Bate, D.M.A. (1903a) The mammals of Cyprus. Proceedings of the Zoological Society of London, 2, 341–348.

    Bate, D.M.A. (1903b) On an Extinct Species of Genet (Genetta plesictoides, sp.n.) from the Pleistocene of Cyprus. Proceedings of the Zoological Society of London, 2, 121–124.

    Bibb, M.J., Van Etten, R.A., Wright, C.T., Walberg, M.W. & Clayton, D.A. (1981) Sequence and Gene Organisation of mouse Mitochondrial DNA. Cell, 26, 167–180.

    Blondel, J. (1986) Biogéographie évolutive. 221 pp.

    Blosat, B., Hadjisterkotis, E. & Papamichael, C. (1996) Endemic snakes of Cyprus. Game Fund, Ministry of Interior, Nicosia, 6 pp.

    Boekschoten, G.J. & Sondaar, P.Y. (1972) On the fossil mammalia of Cyprus, p. 306–308. In: Proceedings of the Kononklijke Nederlandse Akad. van Wetenschappen. Vol. ser. B 75, Amsterdam

    Bonhomme, F., Catalan, J., Britton-Davidian, J., Chapman, V.M., Moriwaki, K., Nevo, E. & Thaler, L. (1984) Biochemical Diversity and Evolution in the Genus Mus. Biochemical Genetics, 22, 275–303.

    Bonhomme, F., Orth, A., Cucchi, T., Hadjisterkotis, E., Vigne, J.-D. & Auffray, J.-C. (2004) Découverte d'une nouvelle espèce de souris sur l'île de Chypre. Comptes Rendus Biologies, 327, 501–507.

    Bookstein, F.L. (1991) Morphometric tools for landmark data. Geometry and biology. Cambridge Press, pp. 435.

    Boursot, P., Auffray, J.-C., Britton-Davidian, J. & Bonhomme, F. (1993) The evolution of House mouse. Annual review of ecology and systematics, 24, 119–152.

    Bulatova, N. & Kotenkova., E. (1990) Variants of the Y-chromosome in sympatric

    taxa of Mus in southern USSR. Bollettino di Zoologia, 57, 357–360.

    Cherry, J.F. (1990) The first Colonization of the Mediterranean Islands: A review of Recent Research. Journal of Mediterranean Archaeology, 3, 145–221.

    Chevret, P., Jenkins, P. & Catzeflis, C. (2003) Evolutionary systematics of the Indian mouse Mus famulus Bonhote, 1898: molecular (DNA/DNA hybridization and 12S rRNA sequences) and morphological evidence. Zoological Journal of the Linnean Society, 137, 385–401.

    Cowell, J.K. (1984) A photographic representation of the variability of G-banded structure of the chromosomes of the mouse karyotype. Chromosoma, 89, 194–320.

    Crampton, J.S. (1995) Elliptic Fourier shape analysis of fossil bivalves: some practical considerations. Lethaia, 28, 179–186.

    Cucchi, T. (2005) Le commensalisme murin et les premières sociétés méditerranéennes, p. 307. Thesis. Muséum National d'Histoire Naturelle, Paris

    Cucchi, T., Vigne, J.-D. & Auffray, J.-C. (2005) First occurrence of the house mouse (Mus musculus domesticus SCHWARTZ & SCHWARTZ, 1943) in Western Mediterranean: a zooarchaeological revision of sub-fossil house mouse occurrences. Biological Journal of the Linnean Society, 84, 429–445.

    Cucchi, T., Vigne, J.-D., Auffray, J.-C., Croft, P. & Peltenburg, E. (2002) Introduction involontaire de la souris domestique (Mus musculus domesticus) à Chypre dès le Néolithique précéramique ancien (fin IXe et VIIIe millénaire av. J.-C.). English abridged version. Comptes Rendus Palevol, 1, 235–241.

    Darviche, D. & Orsini, P. (1982) Critères de différenciation morphologique et biométrique de deux espèces de souris sympatriques: Mus spretus et Mus musculus domesticus. Mammalia, 46, 205–217.

    Ferson, S., Rohlf, F.J. & Koehn, R.K. (1985) Measuring shape variation of two dimensional outlines. Systematic Zoology, 34, 59–68.

    Foster, J.B. (1964) Evolution of Mammals on Islands. Nature, 202, 234–235.

    Gass, I.G. (1968) Is the Troodos Massif of Cyprus a fragment of Mesozoïc Ocean Floor ? Nature, 220, 39–42.

    Gerasimov, S., Nikolov, H., Mihailova, V., Auffray, J.-C. & Bonhomme, F. (1990) Morphometric stepwise discriminant analysis of the five genetically determined European taxa of the genus Mus. Biological Journal of the Linnean Society, 41, 47–64.

    Guénet, J.L. & Bonhomme, F. (2003) Wild mice: an ever-increasing contribution to a popular mammalian model. Trends in Genetics, 19, 24–31.

    Hadjisterkotis, E., Masala, B. & Reese, D. (2000) The origin and extinction of the large Pleistocene Mammals of Cyprus. Biogeographia Anatolia, 21, 593–606.

    Harrison, D.L. & Bates, P.J.J. (1991) The mammals of Arabia. Harrison Zoological Museum Publications, Sevenoaks, pp. 354.

    Held, S.O. (1989) Colonization Cycles on Cyprus. 1: The biogeographic and palaeontological foundation of early prehistoric settlement. Rep. Dpt Antiquities Cyprus,

    Isaev, M. (1992) EFAWin: Windows shell for elliptic Fourier. Institut of Maths Problems of Biology, Pushchino

    Ivanitskaya, E., Gorlov, I., Gorlova, O. & Nevo, E. (1996) Chromosome markers for Mus macedonicus (Rodentia, Muridae) from Israel. Hereditas, 124, 145–150.

    Kry”tufek, B. & Vohralik, V. (2001) Mammals of Turkey and Cyprus. Knjiznica Annales Majora, Koper, pp. 140.

    Kuhl, F.P. & Giardina, C.R. (1982) Elliptic Fourier features of a closed contour. Computer Graphics and Image Processing, 18, 259–278.

    Lee, M.R. & Elder, F.F.B. (1980) Yeast stimulation of bone marrow mitosis for cytogenetic investigations. Cytogenetics & Cell Genetics, 26, 36–40.

    Libois, R. & Fons, R. (1990) Le mulot des îles d'Hyères : un cas de gigantisme insulaire. Vie et Milieu, 40, 217–222.

    Lidicker, W.Z. (1966) Ecological observations on a feral house mouse population declining to extinction. Ecological monographs, 36, 28–50.

    Lomolino, M.V. (1985) Body size of Mammals on islands: the island rule reexamined. The American Naturalist, 125, 310–316.

    Macholan, M. (1996a) Morphometric analysis of European house mice. Acta Theriologica, 41, 255–275.

    Macholan, M. (1996b) Multivariate morphometric analysis of European species of the genus Mus (Mammalia, Muridae). Z. Säugetierkunde, 61, 304–319.

    Marcus, L.F. (1993) Some aspects of multivariate statistics for morphometrics. In: Marcus, L.F., Bello, E. & Garcia-Valdecasas, A. (Eds.) Contributions to morphometrics. Museo Nacional de Ciencas Naturales, Madrid, pp. 95–130.

    Markvong, A., Marshall, J.T. & Gropp, A. (1973) Chromosomes of rats and mice of Thailand. Natural History Bulletin of the Siam Society, 25, 23–32.

    Marshall, J.T. & Sage, R.D. (1981) Taxonomy of the house mouse. Symposia of the Zoological Society of London, 47, 15–25.

    Masseti, M. (2002) Uomini e (non solo) topi. Gli animali domestici e la fauna antropocora. Firenze University Press, Università degli Studi di Firenze, pp. 337.

    McCallum, J.E. & Robertson, A.H.F. (1990) Pulsed uplift of the Troodos Massif - evidence from the Plio-Pleistocene Mesaoria basin. In: Malpas, J., Moores, E.M., Panayiotou, A. & C., X. (Eds.) Ophiolites, Oceanic Crustall Analogues. Proceedings of the Symposium Troodos 1987. Geology Survey Department, Ministry of Agriculture, Natural Resources and Environmenrt, Nicosia, pp. 733.

    Michaux, J. (1971) Données nouvelles sur les Muridae (Rodentia) Néogènes d'Europe sud-occidentale. Evolution et rapports avec les formes actuelles. Paléobiologie continentale, 2, 67.

    Michaux, J., Filippucci, M.G., Libois, M.G., Fons, R. & Matagne, R.F. (1996a) Biogeography and taxonomy of Apodemus sylvaticus (the woodmouse) in the Tyrrhenian region: enzymatic variations and mitochondrial DNA restriction pattern analysis. Heredity, 76, 267–277.

    Michaux, J., Libois, M.G. & Fons, R. (1996b) Différenciation génétique et morphologique du mulot, Apodemus sylvaticus, dans le bassin méditerranéen occidental. Vie et Milieu, 46, 193–203.

    Michaux, J.R., Goüy de Bellocq, J., Sarà, M. & Morand, S. (2002) Body size increase in insular rodent populations: a roole for predators. Global Ecology & Biogeography, 11, 427–436.

    Michaux, J.R., Libois, R. & Fons, R. (1996c) Différenciation génétique et morphologique du mulot, Apodemus sylvaticus, dans le bassin méditerranéen occidental. Vie Milieu, 46, 193–203.

    Moores, E.M., Robinson, P.T., Malpas, J. & Xenophontos, C. (1984) A Model for the Origin of the Troodos Massif, Cyprus, and other Mideast Ophiolites. Geology, 12, 500–503.

    Morgan, G.S. & Woods, C.A. (1986) Extinction and the zoogeography of West Indian land mammals. Biological Journal of the Linnean Society, 28, 167–203.

    Nagamine, C., Nishioka, Y., Moriwaki, K., Boursot, P., Bonhomme, F. & Lau, Y.F.Q. (1992) The musculus-type Y chromosome of the laboratory mouse is of Asian origin. Mammalian Genome, 3, 84–91.

    Ohtsuka, H., Oyanagi, M., Mafune, Y., Miyashita, N., Shiroishi, T., Moriwaki, K., Kominami, R. & Saitou, N. (1996) The presence/absence polymorphism and evolution of the p53 pseudogene in the genus Mus. Molecular phylogentics and evolution, 5, 548–556.

    Orsini, P., Bonhomme, F., Britton-Davidian, J., Croset, H., Gerasimov, S. & Thaler, L. (1983) Le complexe d'espèces du genre Mus en Europe centrale et orientale. II: Critères d'identifications, répartitions et caractéristiques écologiques. Zeitschrift für Säugetierkunde, 48, 86–95.

    Orsini, P. & Cheylan, G. (1988) Les rongeurs de Corse: modification de taille en relation avec l'isolement en milieu insulaire. Bulletin d'Ecologie, 19, 411–416.

    Patton, J.L., Yang, S.Y. & Myers, P. (1975) Genetic and Morphologic divergence among introduced rat populations (Rattus rattus) of the Galapagos archipelago, Ecuador. Systematic Zoology, 24, 296–310.

    Pergams, O.R.W. & Ashley, M.V. (1999) Rapid morphological change in Channel island deer mice. Evolution, 53, 1573–1581.

    Pergams, O.R.W. & Ashley, M.V. (2001) Microevolution in island rodents. Genetica, 112–113, 245–256.

    Praeger, E.M., Boursot, P. & Sage, R.D. (1997) New assays for Y chromosome and p53 pseudogene clines among East Holstein house mice. Mammalian Genome, 8, 279–281.

    Renaud, S. (1999) Size and shape variability in relation to species differences and climatic gradient in the African rodent Oenomys. Journal of Biogeography, 26, 857–865.

    Renaud, S. (2005) First upper molar and mandibule shape of wood mice (Apodemus sylvaticus) from northern Germany: ageing, habitat and insularity. Mammalian Biology. Zeitschrift für Säugetierkunde, 70, 157–170.

    Renaud, S., Michaux, J., Jaeger, J.J. & Auffray, J.C. (1996) Fourier analysis applied to Stephanomys (Rodentia, Muridae) molars: non progressive evolutionnary pattern in a gradual lineage. Paleobiology, 22.2, 255–265.

    Renaud, S. & Michaux, J.R. (2003) Adaptative latitudinal trends in the mandible shape of Apodemus wood mice. Journal of Biogeography, 30, 1617–1628.

    Renaud, S. & Millien, V. (2001) Intra- and interspecific morphological variation in the field mouse species Apodemus argenteus and A. speciosus in the Japanese archipelago: the role of insular isolation and biogeographic gradients. Biological Journal of the Linnean Society, 74, 557–669.

    Rohlf, F.J. (1998a) NTSYS-pc. Numerical Taxonomy and Multivariate Analysis system. Ecology & Evolution, State University at Stony brook, New York

    Rohlf, F.J. (1998b) Numerical taxonomy and multivariate analysis system. 2.02j (Ed.). Exeter Software, New York

    Rohlf, F.J. (2004) TpsDig 1.40-Thin Plate Spline Digitizer. Ecology & Evolution, State University at Stony brook, New York

    Rohlf, F.J. (2005) TpsRelw 1.41-Thin Plate Spline Relative Warp. Ecology & Evolution, State University at Stony brook, New York

    Rohlf, F.J. & Archie, J.W. (1984) A comparison of Fourier methods for the description of wing shape in mosquitoes (Diptera: Culcidae). Systematic Zoology, 33.3, 302–317.

    Rohlf, F.J. & Slice, D.E. (1990) Extensions of the Procrustes method for the optimal surimpostion of landmarks. Systematic Zoology, 39, 40–59.

    Seabright, J. (1971) A rapid technique for human chromosomes. The Lancet, 2, 971–972.

    Sen, S. & Sharma, T. (1983) Role of constitutive heterochromatin in evolutionary divergence: results of chromosome banding and condensation inhibition studies in Mus musculus, Mus booduga and Mus dunni. Evolution, 37, 628–636.

    Simmons, A.H. (1991) Humans, Islands, Colonization and Pleistocene Extinctions in the Mediterranean: the view from Akrotiri Aetokremnos, Cyprus. Antiquity, 65, 857–869.

    Simmons, A.H. (1999) Faunal extinction in an Island society. Pygmy Hippopotamus Hunters of Cyprus. New-York, Klumer Academic/Plenum publishers, 381 pp.

    Suzuki, H., Shimada, T., Terashima, M., Tsuchiya, K. & Aplin, K. (2004) Temporal, spatial, and ecological modes of evolution of Eurasian Mus based on mitochondrial and nuclear gene sequences. Molecular Phylogenetics and Evolution, 33, 626–646.

    Tanooka, H., Sasaki, H., Shiroishi, T. & Moriwaki, K. (2001) p53 pseudogene dating: Identification of the origin of laboratory mice. Gene, 270, 153–159.

    Thaler, L. (1973) Nanisme et gigantisme insulaire. La Recherche, 37, 741–750.

    Tucker, K.P., Lee, B.K. & Eicher, E.M. (1989) Y chromosome evolution in the subgenus Mus (Genus Mus). Genetics, 122, 169–179.

    Tyrberg, T. (1998) Pleistocene Birds of the Palearctic: A Catalogue. Nuttall Ornithological Club, Cambridge, 720 pp.

    Van Valen, L. (1973) Pattern and the Balance of Nature. Evolution Theory, 1, 31–49.

    Van Vugt, N., de Bruijn, H., van Kolfschoten, M. & Langereis, C.G. (2000) Magneto- and cyclostratigraphy and mammal-fauna's of the Pleistocene lacustrine Megalopolis Basin, Peloponnesos, Greece. In: Van Vugt, N. (Ed.). Geologica Ultraiectina, Orbital forcing in late Neogene lacustrine basins from Mediterranean. A magnetostratigraphic and cyclostratigraphic study, pp. 69–92.

    Vigne, J.-D. (1999) The large "true" Mediterranean as a model for the Holocene human impact on the European vertebrate fauna? Recent data and new reflections. In: Benecke, N. (Ed.) The Holocene history of the european vertebrate fauna.Modern aspects of research (Workshop, 6th-9th April 1998, Berlin). Deutsches Archaologisches Institut, Eurasian-Abteilung, Berlin, pp. 295–322.

    Vigne, J.-D., Cheylan, G., Granjon, L. & Auffray, J.-C. (1993a) Evolution ostéométrique de Rattus et de Mus musculus domesticus sur de petites îles: comparaison de populations médiévales et actuelles des îles Lavezzi (Corse) et de Corse. Mammalia, 57.1, 85–98.

    Vigne, J.-D. & Cucchi, T. (2005) Premières navigations au Proche-Orient : les informations indirectes de Chypre. Paléorient, 31, 195–204.

    Vigne, J.-D., Granjon, L., Auffray, J.-C. & Cheylan, G. (1993b) Les micrommamifères. In: Vigne, J.-D. (Ed.) L'île Lavezzi, Homme, animaux, archéologie et marginalité (XIIIe-XXe siècles, Bonifacio, Corse). CNRS, Paris, pp. 133–154.