Phylogeographic footprints of the Strait of Gibraltar and Quaternary climatic fluctuations in the western Mediterranean: a case study with the greater white-toothed shrew Crocidura russula (Mammalia: Soricidae)
Cosson, Jean François; Hutterer, Rainer; Libois, Rolandet al.
Europe, Human assisted dispersal, mtDNA, North Africa, phylogeography, Quaternary history, speciation
Abstract :
[en] We used mitochondrial cyt b sequences to investigate the phylogenetic relationships of Crocidura russula (sensu lato) populations across the Strait of Gibraltar, western Europe, Maghreb, and the Mediterranean and Atlantic islands. This revealed very low genetic divergence between European and Moroccan populations. The application of a molecular clock previously calibrated for shrews suggested that the separation of European from Moroccan lineages occurred less than 60000 BP, which is at least 5 million years (Myr) after the reopening of the Strait of Gibraltar. This means that an overwater dispersal event was responsible for the observed phylogeographical structure. In contrast, genetic analyses revealed that Moroccan populations were highly distinct from Tunisian ones. According to the molecular clock, these populations separated about 2.2 million years ago (Ma), a time marked by sharp alternations of dry and humid climates in the Maghreb. The populations of the Mediterranean islands Ibiza, Pantellaria, and Sardinian were founded from Tunisian populations by overwater dispersal. In conclusion, overwater dispersal across the Strait of Gibraltar, probably assisted by humans, is possible for small terrestrial vertebrates. Moreover, as in Europe, Quaternary climatic fluctuations had a major effect on the phylogeographical structure of the Maghreb biota.
Disciplines :
Zoology
Author, co-author :
Cosson, Jean François
Hutterer, Rainer
Libois, Roland ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Zoogéographie - Département des sciences et gestion de l'environnement
Sarà, Maurizio
Taberlet, P.
Vogel, Peter
Language :
English
Title :
Phylogeographic footprints of the Strait of Gibraltar and Quaternary climatic fluctuations in the western Mediterranean: a case study with the greater white-toothed shrew Crocidura russula (Mammalia: Soricidae)
Alcover JA (1980) Note on the origin of the present mammalian fauna from the Balearic and Pityusic islands. Miscellánia Zoológica, 6, 141-149.
Alcover JA, Vesmanis I (1985) Sobre les restes subfossils de la musaranya de dents blanques Crocidum russula (Hermann, 1780) de la Grotta su Guanu, illa de Sardenya (Mammalia, Insectivora). Endins, 10, 63-70.
Alimen H (1975) Les «Isthmes» hispano-marocain et sicilo-tunisien aux temps acheuléens. L'Anthropologie, 79, 399-436.
Avise JC, Walker D, Johns GC (1998) Speciation and Pleistocene effects on the vertebrate phylogeography. Proceedings of the Royal Society of London. Series B, Biological Sciences, 265, 1707-1712.
Beerli P, Hotz H, Uzzell H (1996) Geologically dated sea barriers calibrate a protein clock for the Aegean water frogs. Evolution, 50, 1676-1687.
Blondel J, Aronson J (1999) Biology and Wildlife of the Mediterranean Region. Oxford University Press.
Bons J, Geniez P (1995) Contribution to the systematics of the lizard Acanthodactylus erythrurus (Sauria, Lacertidae) in Morocco. Herpetological Journal, 5, 271-280.
Bouzouggar A, Kozlowski JK, Otte M (2002) Study of the Aterian lithic assemblages from El Aliya cave in Tangier (Morocco). L'Anthropologie, 106, 207-248.
Bradley RD, Baker RJ (2001) A test of the genetic species concept: cytochrome-b sequences and mammals. Journal of Mammalogy, 82, 960-973.
Brown JH, Gibson AC (1983) Biogeography. Mosby Co, St. Louis.
Brown RP, Suárez NM, Pestano J (2002) The Atlas mountains as a biogeographical divide in North-West Africa: evidence from mtDNA evolution in the agamid lizard Agama impalearis. Molecular Phylogenetics and Evolution, 24, 324-332.
Castella V, Ruedi M, Excoffier L, Ibanez C, Arlettaz R, Hausser J (2000) Is the Gibraltar Strait a barrier to gene flow for the bat Myotis myotis (Chiroptera: Vespertillionidae)? Molecular Ecology, 9, 1761-1772.
Catalan J, Poitevin F, Fons R, Guerasimov S, Croset H (1988) Biologie évolutive des populations ouest-européennes de crocidures (Mammalia, Insectivora). III. Structures génétiques des populations continentales et insulaires de Crocidura russula (Hermann, 1780) et de Crocidura suaveolens (Pallas, 1811). Mammalia, 52, 387-400.
Catzeflis F (1984) Systématique biochimique, taxonomie et phylogénie des musaraignes d'Europe (Soricidae, Mammalia). PhD Thesis, University of Lausanne, Switzerland.
Cheylan G (1984) Les mammifères des îles de Provence et de Méditerranée occidentale: un exemple de peuplement insulaire non équilibré? Revue d'Ecologie-La Terre et la Vie, 39, 37-54.
Cheylan G (1990) Patterns of Pleistocene turnover, current distribution and speciation among Mediterranean mammals. In: Biogeography of Mediterranean Invasions (eds Groves RH, Di Castri F), pp. 227-262. Cambridge University Press, Cambridge.
Claussen M, Brovkin V, Ganopolski A, Kubatzki C, Petoukhov V (2003) Climate Change in northern Africa: the past is not the future. Climatic Change, 57, 99-118.
Claussen M, Gayler V (1997) The greening of the Sahara during the mid-Holocene: results of an interactive atmosphere-biome model. Global Ecology and Biogeography Letters, 6, 369-377.
Clément M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657-1659.
Collina-Girard J (2001) Atlantis off the Gibraltar Strait? Myth and geology. Comptes Rendus de l'Académie Des Sciences Serie, II. 333, 233-240.
Contoli L (1990) Ulteriori dati su Crocidura cossyrensis Contoli, 1989, con particolare riguardo a soecie congeneri dell'arena mediterranea (Mammalia, Soricidae). Hystrix, 2, 53-58.
Contoli L (1992) De Cossyrae crocidura (Crocidura cossyrensis Contoli, 1989). Atti Della Società Italiana Scienze Naturali e del Museo Civico di Storia Naturale di Milano, 132, 61-68.
Contoli L, Aloise G (2001) On the taxonomy and distribution of Crocidura cossyrensis and Crocidura russula (Insectivora, Soricidae) in Maghreb. Hystrix, 12, 11-18.
Contoli L, Benincasa-Stagni B, Marenzi AR (1989) Morfologia di Crocidura Wagler, 1832 (Mammalia, Soriciae) in Italia, Sardegna e Sicilia, con il metodo dei descrittori di Fourier: primi dati. Hystrix, 1, 113-129.
Corbet GB (1978) The Mammals of the Palaearctic Region: a Taxonomic Review. British Museum (Natural History), London.
Cosson JF, Pascal M, Bioret F (1996) Origine et répartition des musaraignes du genre Crocidura dans les îles bretonnes. Vie et Milieu-Life and Environment, 48, 233-244.
De Jong H (1998) In search of historical biogeographic patterns in the western Mediterranean terrestrial fauna. Biological Journal of the Linnean Society, 65, 99-164.
Dobson M (1998) Mammal distributions in the western Mediterranean: the role of human intervention. Mammal Review, 28, 77-88.
Dobson M, Wright A (2000) Faunal relationships and zoogeographical affinities of mammals in north-west Africa. Journal of Biogeography, 27, 417-424.
Edwards SV (1997) Relevance of microevolutionary processes to higher level molecular systematics. In: Avian Molecular Evolution and Systematics (ed. Mindell DP), pp. 251-278. Academic Press, New York.
Edwards SV, Beerli P (2000) Perspectives: gene divergence, population divergence, and the variance in coalescence times in phylogeographic studies. Evolution, 54, 1839-1854.
Ellerman JR, Morrison-Scott TCS (1966) Checklist of Palearctic and Indian Mammals, 1758-1946. 2d Trustees British Museum (Natural History). London.
Faure H (1987) Il quadro cronologico delle fasi pluviali e glaciali dell'Africa. In: Storia Generale dell'Africa. Metodologia e Preistoria dell'Africa (ed. Ki-Zerbo J), pp. 400-409. Jaca Book Milano.
Flemming N, Bailey G, Courtillot V et al. (2003) Coastal and marine palaeo-environments and human dispersal points across the Africa-Eurasia boundary. In: Maritime Heritage (eds Brebbia CA, Gambin T), pp. 13. Wessex Institute of Technology, Southampton, UK and University of Malta, Malta.
Fumagalli L, Taberlet P, Stewart DT, Gielli L, Hausser J, Vogel P (1999) Molecular phylogeny and evolution of Sorex shrews (Soricidae: Insectivora) inferred from mitochondrial DNA sequence data. Molecular Phylogenetics and Evolution, 11, 222-235.
Gantenbein B, Largiadèr CR (2003) The phylogeographic importance of the Strait of Gibraltar as a gene flow barrier in terrestrial arthropods: a case study with the scorpion Buthus occitanus as a model organism. Molecular Phylogenetics and Evolution, 28, 119-130.
Genoud M, Hutterer R (1990) Crocidura russula (Hermann, 1780) - Hausspitzmaus. In: Handbuch der Säugetiere Europas (eds Niethammer J, Krapp F), pp. 429-452. Aula-Verlag, Wiesbaden.
Geraads D (1995) Rongeurs et Insectivores (Mammalia) du Pliocène final de Ahl Oughlam (Casablanca, Maroc). Geobios, 28, 99-115.
Guiller A, Coutellec-Vreto MA, Madec L, Deunff J (2001) Evolutionary history of the land snail Helix aspersa in the western Mediterranean: preliminary results inferred from mitochondrial DNA sequences. Molecular Ecology, 10, 81-87.
Harris DJ, Sá-Sousa P (2002) Molecular phylogenetics of the Iberian wall lizard (Podarcis): is Podarcis hispanica a species complex? Molecular Phylogenetics and Evolution, 23, 75-81.
Heaney LR (1986) Biogeography of mammals in SE Asia: estimates of rates of colonisation, extinction and speciation. Biological Journal of the Linnean Society, 28, 127-165.
Hewitt GM (1996) Some genetic consequencies of ice ages and their role in divergence and speciation. Biological Journal of the Linnean Society, 58, 247-276.
Hewitt GM (1999) Post-glacial recolonisation of European biota. Biological Journal of the Linnean Society, 68, 87-112.
Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature, 405, 907-913.
Hewitt GM (2001) Speciation, hybrid zones and phylogeography - or seen genes in space and time. Molecular Ecology, 10, 537-549.
Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London. Series B, Biology Sciences, 359, 183-195.
Hsü KJ, Montader L, Bernouilli D et al. (1977) History of the Mediterranean salinity crisis. Nature, 267, 399-403.
Hutterer R (1993) Order Insectivora. In: Mammal Species of the World, A Taxonomic and Geographic Reference (eds Wilson DE, Reeder DM), pp. 69-130. Smithsonian Institution Press, Washington, D.C.
Jamet P (1991) Flore et faune du Sahara depuis 18 000 BP. Actes Congres National Des Societés Savantes, 116, 55-69.
Johns GC, Avise C (1998) A comparative summary of genetic distances in the vertebrates from the mitochondrial cytochrome b gene. Molecular Biology and Evolution, 15, 1481-1490.
Jolly D, Harrisson SP, Damnati B, Bonnefille R (1998) Simulated climate and biomes of Africa during the late Quaternary: comparison with pollen and lake status data. Quaternary Science Reviews, 17, 629-657.
Kowalski K (1991) L'histoire de la faune de rongeurs de la zone aride de l'ancien monde pendant le Quaternaire. In: Le Rongeur et l'Espace (eds Le Berre M, Le Guelte L), pp. 167-175. Chabaud, Paris.
Krijgsman W (2002) The Mediterranean: Mare Nostrum of Earth sciences. Earth and Planetary Science Letters, 205, 1-12.
Libois RM, Michaux JR, Ramalhinho MG, Maurois C, Sarà M (2001) On the origin and systematics of the North African wood mouse (Apodemus sylvaticus) populations. A comparative study of mtDNA restriction patterns. Canadian Journal of Zoology, 79, 1503-1511.
Lo Brutto S, Arculeo M, Sarà M (2004) Mitochondrial simple sequence repeats (SSR) and 12S-rRNA gene reveal two distinct lineages of Crocidura russula (Mammalia, Soricidae). Heredity, 92, 527-533.
Maddison DR (1991) The discovery and importance of multiple islands of most-parsimonious trees. Systematic Zoology, 40, 315-328.
Madec L, Bellido A, Guiller A (1996) Statistical and biogeographical significances of patterns of morphological and biochemical variation in the land snail Helix aspersa. Comptes Rendus de l'Academie Des Sciences Paris Série, III. 319, 225-229.
Michaux JR, Magnanou E, Paradis E, Nieberding C, Libois R (2001) Mitochondrial phylogeography of the woodmouse (Apodemus sylvaticus) in the western Palearctic region. Molecular Ecology, 12, 685-697.
Molina O, Brown RP, Suarez NM, Pestano JJ (2003) The origin of the osorian shrew (Crocidura osorio) from Gran Canaria resolved using mtDNA. Italian Journal of Zoology, 70, 179-181.
Nehren R (1992) Zur Prähistorie der Maghrebländer (Marokko - Algerien - Tunesien). 1. Teil. Mainz, Philipp von Zabern.
Nichols R (2001) Gene trees and species trees are not the same. Trends in Ecology and Evolution, 16, 358-364.
Palmer M, Cambefort Y (2000) Evidence for reticulate paleogeography: beetle diversity linked to connection-disjunction cycles of the Gibraltar Strait. Journal of Biogeography, 27, 403-416.
Poitevin F, Catalan J, Fons R, Croset H (1986) Biologie évolutive des populations ouest-européennes de crocidures. 1. Critères d'identification et répartition biogéographique de Crocura russula (Hermann, 1780) et Crocidura suaveolens (Pallas, 1811). Revue d'Ecologie-la Terre et la Vie, 41, 299-314.
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817-819.
Prüser F, Mossakowski D (1998) Low substitution rates in mitochondrial DNA in Mediterranean carabid species. Insect Molecular Biology, 7, 121-128.
Quezel P, Barbero M (1993) Variations climatiques au Sahara et en Afrique sèche depuis le Pliocene: enseignements de la flore et de la végétation actuelles. Revue d'Ecologie-la Terre et la Vie, 24, 191-202.
Reumer JWF, Meylan A (1986) New developments in vertebrate cytotaxonomy IX. Chromosome numbers in the order Insectivora (Mammalia). Genetica, 70, 119-151.
Robinson M, Gouy M, Gautier C, Mouchiroud D (1998) Sensitivity of the relative-rate test to taxonomic sampling. Molecular Biology and Evolution, 15, 1091-1098.
Rozas J, Rozas R (1999) DNASP version 3: an integrated program for molecular population genetics and molcular evolution analysis. Bioinformatics, 15, 174-175.
Rzebik-Kowalska B (1988) Studies on the genus Crocidura (Insectivora, Mammalia) in Algeria. Acta Zoologica Cracoviensia, 31, 176-192.
Sanmartín I (2003) Dispersal vs. vicariance in the Mediterranean: historical biogeography of the Palearctic Pachydeminae (Coleoptera, Scarabaeoidea). Journal of Biogeography, 30, 1883-1897.
Sarà M, Vogel P (1996) Geographic variation of the greater white-toothed shrew (Crocidura russula Hermann, 1780 Mammalia, Soricidae). Biological Journal of the Linnean Society, 116, 377-392.
Sarà M, Zanca L (1992) Metric discrimination and distribution of the species of Crocidura occurring in Tunisia. Acta Theriologica, 37, 103-116.
Straus LG (2001) Africa and Iberia in the Pleistocene. Quaternary International, 75, 91-102.
Street A, Gasse F (1981) Recent developments in research into the Quaternary climatic history of the Sahara. In: Sahara: Ecological Change and Early Economic History (ed. Allen JA), pp. 7-28. MENAS Press, London.
Sue JP, Bertini A, Combourieu-Nebout N et al. (1995) Structure of the west Mediterranean vegetation and climate since 5.3 Ma. Acta Zoologica Cracoviensia, 38, 3-16.
Swofford DL (1998) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.0b1. Sinauer Associates, Sunderland, Massachusetts.
Taberlet P, Fumagalli L (1996) Owl pellets as a source of DNA for genetic studies of small mammals. Molecular Ecology, 5, 301-305.
Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology, 7, 453-464.
Tchernov E (1996) Rodent faunas, chronostratigraphy and paleobiogeography of the southern Levant during the Quaternary. Acta Zoologica Cracoviensia, 39, 513-530.
Vigne JD (1992) Zooarchaeology and the biogeographical history of the mammals of Corsica and Sardinia, since the last ice age. Mammal Review, 22, 87-96.
Vigne JD, Alcover JA (1985) Incidence des relations historiques entre l'homme et l'animal dans la composition actuelle du peuplement amphibien, reptilien et mammalien des îles de Méditerranée occidentale. Actes 110ème Congrès national des Socié tés savantes, Montpellier, Sciences, fasc. 28, 79-91.
Vogel P, Cosson JF, Lopez Jurado LF (2003) Taxonomic status and origin of the shrews (Soricidae) from the Canary Islands inferred from mtDNA comparison with the European Crocidura species. Molecular Phylogenetics and Evolution, 27, 271-282.
Vogel P, Maddaleha T (1987) Note sur la répartition altitudinale et la fréquence de la musaraigne musette (Crocidura russula yebalensis) au Maroc. Mammalia, 51, 465-467.
Vogel P, Maddalena T, Catzeflis F (1986) A contribution to the taxonomy and ecology of shrews from Crete and Turkey (Crocidura zimmermanni and C. suaveolens). Acta Theriologica, 31, 537-545.
Vogel P, Maddalena T, Sarà M (1992) The taxonomic status of Crocidura cossyrensis Contoli, 1989 and its relationship to African and European Crocidura russula (Mammalia, Insectivora). Israel Journal of Zoology, 38, 424.
Vogel P, Maddalena T, Sarà M (2004) Crocidura cossyrensis Contoli, 1989 (Mammalia, Soricidae) karyotype, biochemical genetics and hybridization experiments. Revue Suisse de Zoologie, 111, 925-934.
Vogel P, Maddalena T, Schembri PJ (1990) Cytotaxonomy of shrews of the genus Crocidura from Mediterranean islands. Vie et Milieu-Life and Environment, 40, 124-129.
Zardoya R, Doadrio I (1998) Phylogenetics relationships of Iberian cyprinids: systematics and biogeographical implications. Proceedings of the Royal Society of London. Series B, Biological Sciences, 265, 1365-1372.