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Accessible Unlicensed Requires Authentication Published by De Gruyter July 17, 2015

Molecular evidence supports recent anthropogenic introduction of the Algerian hedgehog Atelerix algirus in Spain, Balearic and Canary islands from North Africa

Mourad Khaldi, Alexis Ribas, Ghania Barech, Jean-Pierre Hugot, Meryam Benyettou, Lila Albane, Antoni Arrizabalaga and Violaine Nicolas
From the journal Mammalia

Abstract

The Algerian hedgehog, Atelerix algirus, is recorded from North Africa, the Balearic, Canary and Maltese islands, and into parts of the Mediterranean coastal regions of Spain. The lack of an archeozoological record in Europe, Balearic, Maltese or Canary Islands has led several authors to postulate recent introductions by humans, but few studies actually investigated this hypothesis. We used both mitochondrial and nuclear genes to test it. To this aim, we widely sampled the Algerian hedgehog in North Africa (Algeria, Morocco and Tunisia), continental Spain (Catalonia), and Balearic and Canary islands. Our mitochondrial and nuclear data are consistent and show low genetic diversity across the geographical range of the Algerian hedgehog. Our results suggest the recent colonisation of Spain, Balearic and Canary Islands by this species (Holocene), probably mediated by humans. Several subspecies, mainly based on pelage variations, have been described either from mainland or island populations, but our data do not show any genetic discontinuity, suggesting that subspecific recognition may be unwarranted.

Acknowledgments

This work was funded by the ANR projects PEX04-MOHMIE. Molecular analyses were supported by the Service de Systématique Moléculaire of the French National Museum of Natural History (UMS 2700, Paris, France) and the network “Bibliothèque du Vivant” funded by the CNRS, the Muséum National d’Histoire Naturelle, the INRA, and the CEA (Genoscope). In the field, we benefited from the help of A. Lalis, E. Stoetzel, A. Delapré, C. Denys, S. Cahill and F. Llimona. MK thanks particularly Prof. I. Doadrio and Dr. F. Alda from Spain for their help. The authors wish to thank all those who provided samples for this study in Algeria, Morocco, Tunisia and Spain.

References

Alcover, J.A. 2002. Atelerix algirus (Lereboullet, 1842). In: (L.J. Palomo and I.J. Gisbert, eds.) Atlas de los Mamiferos terrestres de España. Dirección General de Conservación de la Naturaleza – SECEM – SECUM, Madrid, Spain. pp. 58–61.Search in Google Scholar

Alcover, J.A. 2007. Atelerix algirus (Lereboullet, 1842). In: (L.J. Palomo, J. Gisbert and J.C. Blanco, eds.) Atlas y Libro Rojo de los mamíferos terrestres de España. Dirección General para la Biodiversidad – SECEM – SECEMU, Madrid, Spain. pp. 83–85.Search in Google Scholar

Alcover, J.A., E. Ballesteros and J.J. Fornos. 1993. Historia natural de I’arxipelag de Cabrera. Editorial Moll., Palma de Mallorca, Spain. pp. 778.Search in Google Scholar

Amori, G., R. Hutterer, B. Kryštufek, N. Yigit, G. Mitsain and L.J. Palomo. 2008. Atelerix algirus. The IUCN Red List of Threatened Species. Version 2014.2. Available at: . Accessed on 29 October 2014.Search in Google Scholar

Bandelt, H.J., P. Forster and A. Rohl. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16: 37–48.Search in Google Scholar

Bannikova, A.A., V.S. Lebedev, A.V. Abramov and V.V. Rozhnov. 2014. Contrasting evolutionary history of hedgehogs and gymnures (Mammalia: Erinaceomorpha) as inferred from a multigene study. Biol. J. Linn. Soc. 112: 499–519.Search in Google Scholar

Bellakhdar, J. 1978. Médecine traditionnelle et toxicologie ouest-sahariennes: contribution a l’étude de la pharmacopée marocaine. Editions techniques nord-africaines, Rabat. pp. 357.Search in Google Scholar

Blondel, J. and J. Aronson. 1999. Biology and wildlife of the Mediterranean Region. Oxford University Press, Oxford, UK. pp. 328.Search in Google Scholar

Borg, J.J. 2005. Technical Appendix 7: Mammalia baseline survey on the Xaghra l-Hamra Golf Course Proposal. Malta Tourism Authority, Malta. pp. 40.Search in Google Scholar

Brandy, L.D. and J.J. Jaeger. 1980. Les échanges de faunes terrestres entre l’Europe et l’Afrique nord-occidentale au Messinien. C.R. Acad. Sci. Paris 291 (Série D): 465–468.Search in Google Scholar

Cabrera, Á. 1928. Las formas geográficas de Aethechinus algirus. Bol. Real. Soc. Esp. Hist. Nat. 28: 453–455.Search in Google Scholar

Camps-Fabrer, H. and M. Peyron. 2000. Hérisson. Hadrumetum – Hidjaba. 22. Available at: . Accessed on 19 December 2014.Search in Google Scholar

Cheylan, G. 1991. Patterns of Pleistocene turnover, current distribution and speciation among Mediterranean mammals. In: (R.H. Groves and F. Di Castri, eds.) Biogeography of Mediterranean Invasions. Cambridge University Press, Cambridge, UK. pp. 227–262.Search in Google Scholar

Corbet, G.B. 1988. The family Erinaceidae: a synthesis of its taxonomy, phylogeny, ecology and zoogeography. Mammal Rev. 18: 117–172.Search in Google Scholar

Cosson, J.F., R. Hutterer, R. Libois, M. Sará, P. Taberlet and P. Vogel. 2005. Phylogeographical 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). Mol. Ecol. 14: 1151–1162.Search in Google Scholar

Dobson, M. 1998. Mammal distributions in the western Mediterranean: the role of human intervention. Mammal Rev. 28: 77–88.Search in Google Scholar

Dobson, M. and A. Wright. 2000. Faunal relationships and zoogeographical affinities of mammals in north-west Africa. J. Biogeogr. 27: 417–424.Search in Google Scholar

Duggen, S., K. Hoernle, P. van den Bogaard, L. Rüpke and J.P. Morgan. 2003. Deep roots of the Messinian salinity crisis. Nature 422: 602–606.Search in Google Scholar

Ellerman, J.R. and T.C.S. Morrison-Scott. 1951. Checklist of Palaearctic and Indian Mammals, 1758 to 1946. British Museum (Natural History), London, UK. pp. 810.Search in Google Scholar

Excoffier, L. and H.E.L. Lischer. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Res. 10: 564–567.Search in Google Scholar

Flot, J.F. 2010. Seqphase: a web tool for interconverting phase input/output files and fasta sequence alignments. Mol. Ecol. Res. 10: 162–166.Search in Google Scholar

García-Mudarra, J.L., C. Ibáñez and J. Juste. 2009. The Straits of Gibraltar: barrier or bridge to Ibero-Moroccan bat diversity? Biol. J. Linn. Soc. 96: 434–450.Search in Google Scholar

Gippoliti, S. and G. Amori. 2006. Ancient introductions of mammals in the Mediterranean Basin and their implications for conservation. Mammal Rev. 36: 37–48.Search in Google Scholar

Happold, D.C.D. 2013. Atelerix algirus Algerian Hedgehog. In: (M. Happold and D.C.D. Happold, eds.) Mammals of Africa, Volume IV: hedgehogs, shrews and bats. Bloomsbury Publishing, London, UK. pp. 33–34.Search in Google Scholar

Heim de Balsac, H. 1936. Le Hérisson d’Algérie, Aethechinus algirus, relique pliocène en France. Bull. Mus. Hist. Nat., Paris 8: 322–326.Search in Google Scholar

Husemann, M., T. Schmitt, F.E. Zachos, W. Ulrich and J.C. Habel. 2014. Palaearctic biogeography revisited: evidence for the existence of a North African refugium for Western Palaearctic biota. J. Biogeogr. 41: 81–94.Search in Google Scholar

Hutterer, R. 1983. Über den Igel (Erinaceus algirus) der Kanarischen Inseln. Z Säugetierk 48: 257–265.Search in Google Scholar

Hutterer, R. 2005. Order Erinaceomorpha. In: (D.E. Wilson and D.M. Reeder, eds.) Mammal species of the world: a taxonomical and geographical reference. 3rd edition. The John Hopkins University Press, Baltimore, MD. pp. 212–219.Search in Google Scholar

Irwin, D.M., T.D. Kocher and A.C. Wilson. 1991. Evolution of the cytochrome b gene of mammals. J. Mol. Evol. 32: 128–144.Search in Google Scholar

Jaeger, J.J., B. Coiffait, H. Tong and C. Denys. 1987. Rodent extinctions following Messinian faunal exchanges between western Europe and northern Africa. Mém. Soc. Géol. France 150: 153–158.Search in Google Scholar

Johnson, L., G.X. Pons and F.X. Roig-Munar. 2012. L’eriçó africà, Atelerix algirus (Lereboullet, 1842) (Erinaceidae), i els passos de bestiar canadencs del Cap de Cavalleria (Es Mercadal, Menorca). Boll. Soc. Hist. Nat. Balears 55: 139–148.Search in Google Scholar

Juste, J., R. Bilgin, J. Munoz and C. Ibanez. 2009. Mitochondrial DNA signatures at different spatial scales: from the effects of the Straits of Gibraltar to population structure in the meridional serotine bat (Eptesicus isabellinus). Heredity 103: 178–187.Search in Google Scholar

Kahmann, H. and I. Vesmanis. 1978. Zur Kenntnis des Wanderigels (Erinaceus algirus Lereboullet, 1842) auf der Insel Formentera (Pityusen) und im nordafrikanischen Verbreitungsgebiet. Spixiana 1: 105–135.Search in Google Scholar

Kocher, T.D., W.K. Thomas, A. Meyer, S.V. Edwards, S. Paabo, F.X. Villablanca and A.C. Wilson. 1989. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Natl. Acad. Sci. USA 86: 6196–6200.Search in Google Scholar

Krijgsman, W., F.J. Hilgen, I. Raffi, F.J. Sierro and D.S. Wilson. 1999. Chronology, causes and progression of the Messinian salinity crisis. Nature 400: 652–655.Search in Google Scholar

Lapini, L. 1999. Atelerix algirus (Lereboullet, 1842). In: (A.J. Mitchell-Jones, G. Amori, W. Bogdanowicz, B. Kryštufek, P.J.H. Reijnders, F. Spitzenberger, M. Stubbe, J. Thissen, B.M.V. Vohralík and J. Zima, eds.) The atlas of European mammals. T & AD Poyser Natural History, London. pp. 34–35.Search in Google Scholar

Leberg, P.L. 2002. Estimating allelic richness: effects of sample size and bottlenecks. Mol. Ecol. 11: 2445–2449.Search in Google Scholar

Long, J.L. 2003. Introduced mammals of the world: their history, distribution and influence. CSIRO Publishing, Oxford, UK. pp. 612.Search in Google Scholar

Malec, F. and G. Storch. 1972. Deer Wanderigel, Erinaceus algirus Duvernoy & Lereboullet, 1842, von Malta und seine Beziehungen zum nordakrikanischen Herkunftsgebiet. Säugetierk Mitteil 20: 146–151.Search in Google Scholar

Masseti, M. 2010. Mammals of the Macaronesian islands (the Azores, Madeira, the Canary and Cape Verde islands): redefinition of the ecological equilibrium. Mammalia 74: 3–34.Search in Google Scholar

Morales, A. and J. Rofes. 2008. Early evidence for the Algerian hedgehog in Europe. J. Zool. 274: 9–12.Search in Google Scholar

Posada, D. and K.A. Crandall. 2001. Intraspecific gene genealogies: trees grafting into networks. Trends Ecol. Evol. 16: 37–45.Search in Google Scholar

Saint Girons, M.C. 1969. Notes sur les Mammifères de France. VIII. Données sur la morphologie et la répartition de Erinaceus europaeus et Erinaceus algirus. Mammalia 33: 206–218.Search in Google Scholar

Saint Girons, M.C. 1984. Le Hérisson Erinaceaus europaeus. In: (A. Fayard, ed.) Atlas des Mammifères sauvages de France. S.F.E.P.M, Paris, France. pp. 24.Search in Google Scholar

Sanchez, A., M. Bullejos, M. Burgos, C. Hera, R. Jimenez and R. Diaz de la Guardia. 1996. High sequence identity between the SRY HMG box from humans and insectivores. Mamm. Genome 7: 536–538.Search in Google Scholar

Seddon, J.M., F. Santucci, N.J. Reeve and G.M. Hewitt. 2001. DNA footprints of European hedgehogs, Erinaceus europaeus and E. concolor: Pleistocene refugia, postglacial expansion and colonization routes. Mol. Ecol. 10: 2187–2198.Search in Google Scholar

Stephens, M. and P. Scheet. 2005. Accounting for decay of linkage disequilibrium in haplotype inference and missing data imputation. Am. J. Hum. Genet. 76: 449–462.Search in Google Scholar

Stephens, M., N.J. Smith and P. Donnelly. 2001. A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 68: 978–989.Search in Google Scholar

Stoetzel, E. 2013. Late Cenozoic micromammal biochronology of northwestern Africa. Palaeogeogr. Palaeocl. 392: 359–381.Search in Google Scholar

Received: 2014-12-19
Accepted: 2015-6-5
Published Online: 2015-7-17
Published in Print: 2016-5-1

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