Skip to main content

Origin and introduction history of the least weasel (Mustela nivalis) on Mediterranean and Atlantic islands inferred from genetic data

Biological Invasions volume 19, pages 399–421 (2017)Cite this article

An Erratum to this article was published on 10 December 2016

Abstract

Introduced mammalian predators have negatively affected native biota and ecological processes in ecosystems across the globe. The least weasel (Mustela nivalis) is a Holarctic mustelid carnivore that has been considered one of the world’s worst invasive alien species. It has been introduced to several islands in the Mediterranean Sea and Atlantic Ocean, and here we present a genetic analysis of these insular populations, based on mitochondrial DNA and microsatellites and building upon a previous Western Palearctic phylogeographic study, with the aim of inferring their origin and introduction history. This is essential information for ecological and evolutionary studies of those populations and our understanding of their impacts on the islands’ biodiversity. Among the Mediterranean insular populations, a substantial mitochondrial subdivision between weasels in Sicily-Corsica and Malta-Sardinia-Balearics is best explained by a dual colonization originating from the Eastern Mediterranean. Given the correspondence between the observed genetic partition and the differential geographic distribution of Greek and Phoenician settlements and influence during the last millennium BC in those islands, we propose that weasels may have been introduced into the first group of islands by the Greeks and into the second group by the Phoenicians. There is strong support that the commercial and demographic expansions of Phoenicians and Greeks allowed the colonization of the western Mediterranean islands by the house mouse, and texts from Classical Antiquity show evidence that weasels were used for rodent control. Thus, weasels may have been intentionally introduced to the islands, with the aim of controlling commensal rodents. Besides indicating Eastern Mediterranean origins for weasels in Mediterranean islands, the mitochondrial data also revealed an unanticipated close genealogical connection between some of these populations and those from the Azores and São Tomé. The latter island populations showed no affinities with weasels from mainland Portugal, contrary to what might have been expected given that these Atlantic islands were settled by the Portuguese. The microsatellite data also supported the relationship between weasels in Atlantic and in Mediterranean islands. Considering geographic proximity and historical information, the most parsimonious explanation for the origin of the Atlantic weasels appears to be introduction from the Balearic Islands to the Azores and from there to São Tomé.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Abi-Said M, Amr ZS (2012) Camera trapping in assessing diversity of mammals in Jabal Moussa Biosphere Reserve, Lebanon. Vertebr Zool 62:145–152

    Google Scholar 

  • Abramov AV, Baryshnikov GF (2000) Geographic variation and intraspecific taxonomy of weasel Mustela nivalis (Carnivora, Mustelidae). Zoosystematica Rossica 8:365–402

    Google Scholar 

  • Abulafia D (1991) The Problem of the kingdom of Majorca (1229/76–1343) 2. Economic identity. Mediterr Hist Rev 6:35–61

    Article  Google Scholar 

  • Antonioli F, Lo Presti V, Gasparo Morticelli M, Bonfiglio L, Mannino MA, Palombo MR, Sannino G, Ferranti L, Furlani S, Lambeck K, Canese S, Catalano R, Chiocci FL, Mangano G, Scicchitano G, Tonielli R (2016) Timing of the emergence of the Europe–Sicily bridge (40–17 cal ka BP) and its implications for the spread of modern humans. In: Harff J, Bailey G, Lüth F (eds) Geology and archaeology: submerged landscapes of the continental shelf. The Geological Society, London, Special Publication 411, pp 111–144

  • Atkinson IA (2001) Introduced mammals and models for restoration. Biol Conserv 99:81–96

    Article  Google Scholar 

  • Avise JC (2009) Phylogeography: retrospect and prospect. J Biogeogr 36:3–15

    Article  Google Scholar 

  • Ballard RD, Stager LE, Master D, Yoerger D, Mindell D, Whitcomb LL, Singh H, Piechota D (2002) Iron age shipwrecks in deep water off Ashkelon, Israel. Am J Archaeol 106:151–168

    Article  Google Scholar 

  • Bandelt H, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Barboza du Bocage JV (1895) A doninha da ilha de S. Tomé. J Sci Math Phys Nat Segunda Sér 4:24–27

    Google Scholar 

  • Bar-Oz G, Dayan T (2001) Weasels from the Hellenistic period of Israel. Isr J Zool 47:271–274

    Article  Google Scholar 

  • Barrett-Hamilton GEH (1900) III.—Note on the weasel, Putorius (Ictis) nivalis, Linn., and some of its subspecies. Ann Mag Nat Hist Ser 7 5:41–50

    Google Scholar 

  • Barrett-Hamilton GEH (1904) XXXVIII.—Note on an undescribed weasel from the Atlas Mountains, and on the occurrence of a weasel in the Azores. Ann Mag Nat Hist Ser 13:323–325

    Google Scholar 

  • Bastrop R, Jürss K, Sturmbauer C (1998) Cryptic species in marine polychaete and their independent introduction from North America to Europe. Mol Biol Evol 15:97–103

    Article  CAS  PubMed  Google Scholar 

  • Bate DMA (1905) On the mammals of Crete. Proc Zool Soc Lond 75:315–323

    Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier. http://kimura.univ-montp2.fr/genetix/

  • Bellard CG (1995) The first colonization of Ibiza and Formentera (Balearic Islands, Spain): some more islands out of the stream? World Archaeol 26:442–455

    Article  Google Scholar 

  • Berglund H, Järemo J, Bengtsson G (2009) Endemism predicts intrinsic vulnerability to nonindigenous species on islands. Am Nat 174:94–101

    Article  PubMed  Google Scholar 

  • Bikai PM, Bikai PM (1990) A Phoenician fable. Archaeology 43:20–23

    Google Scholar 

  • Bonanno A (2005) Malta: Phoenician. Midsea Books Ltd, Malta

    Google Scholar 

  • Bosch-Gimpera P (1944) The Phokaians in the Far West: an historical reconstruction. Class Q 38:53–59

    Article  Google Scholar 

  • Bover P, Alcover JA (2008) Extinction of the autochthonous small mammals of Mallorca (Gymnesic Islands, Western Mediterranean) and its ecological consequences. J Biogeogr 35:1112–1122

    Article  Google Scholar 

  • Cabrera P (1998) Greek trade in Iberia: the extent of interaction. Oxf J Archaeol 17:191–206

    Article  Google Scholar 

  • Carpenter R (1958) Phoenicians in the West. Am J Archaeol 62:35–53

    Article  Google Scholar 

  • Cavalli-Sforza LL, Edwards AW (1967) Phylogenetic analysis. Models and estimation procedures. Am J Hum Genet 19:233–257

    CAS  PubMed  PubMed Central  Google Scholar 

  • Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733

    Article  Google Scholar 

  • Cooper WE Jr, Pérez-Mellado V (2012) Historical influence of predation pressure on escape by Podarcis lizards in the Balearic Islands. Biol J Linn Soc 107:254–268

    Article  Google Scholar 

  • Courchamp F, Chapuis JL, Pascal M (2003) Mammal invaders on islands: impact, control and control impact. Biol Rev 78:347–383

    Article  PubMed  Google Scholar 

  • Cristescu ME (2015) Genetic reconstructions of invasion history. Mol Ecol 24:2212–2225

    Article  PubMed  Google Scholar 

  • Cucchi T, Vigne JD (2006) Origin and diffusion of the house mouse in the Mediterranean. Hum Evol 21:95–106

    Article  Google Scholar 

  • Davies A (1964) Prince Henry the Navigator. Trans Pap (Institute of British Geographers) 35:119–127

    Article  Google Scholar 

  • De Marinis AM, Masseti M (2003) The weasel (Mustela nivalis) on the Mediterranean islands. Mamm Biol 68:181–186

    Google Scholar 

  • Diamond JM (1989) Nine hundred kiwis and a dog. Nature 338:544

    Article  Google Scholar 

  • Dixon CJ (2006) A means of estimating the completeness of haplotype sampling using the Stirling probability distribution. Mol Ecol Notes 6:650–652

    Article  Google Scholar 

  • Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449

    Article  CAS  PubMed  Google Scholar 

  • Dubey S, Cosson JF, Magnanou E, Vohralík V, Benda P, Frynta D, Hutterer R, Vogel V, Vogel P (2007) Mediterranean populations of the lesser white-toothed shrew (Crocidura suaveolens group): an unexpected puzzle of Pleistocene survivors and prehistoric introductions. Mol Ecol 16:3438–3452

    Article  CAS  PubMed  Google Scholar 

  • Dutton J (1994) Introduced mammals in São Tomé and Príncipe: possible threats to biodiversity. Biodivers Conserv 3:927–938

    Article  Google Scholar 

  • Eales J, Thorpe RS (2010) Revealing the geographic origin of an invasive lizard: the problem of native population genetic diversity. Biol Invasions 12:77–86

    Article  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Evian SBD (2011) Egypt and the levant in the iron age I–IIA: the ceramic evidence. Tel Aviv 38:94–119

    Article  Google Scholar 

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Faure E, Kitchener AC (2009) An archaeological and historical review of the relationships between felids and people. Anthrozoos 22:221–238

    Article  Google Scholar 

  • Fernandes CA, Ginja C, Pereira I, Tenreiro R, Bruford MW, Santos-Reis M (2008) Species-specific mitochondrial DNA markers for identification of non-invasive samples from sympatric carnivores in the Iberian peninsula. Conserv Genet 9:681–690

    Article  CAS  Google Scholar 

  • Ficetola GF, Bonin A, Miaud C (2008) Population genetics reveals origin and number of founders in a biological invasion. Mol Ecol 17:773–782

    Article  CAS  PubMed  Google Scholar 

  • Fitzpatrick BM, Fordyce JA, Niemiller ML, Reynolds RG (2012) What can DNA tell us about biological invasions? Biol Invasions 14:245–253

    Article  Google Scholar 

  • Frank F (1985) Zur Evolution und Systematik der kleinen Wiesel (Mustela nivalis Linnaeus, 1766). Z Säugetierkd 50:208–225

    Google Scholar 

  • Frutuoso G (1873) Saudades da Terra. Typ Funchalense, Funchal

    Google Scholar 

  • Gabriel SI, Mathias ML, Searle JB (2015) Of mice and the ‘Age of Discovery’: the complex history of colonization of the Azorean archipelago by the house mouse (Mus musculus) as revealed by mitochondrial DNA variation. J Evol Biol 28:130–145

    Article  CAS  PubMed  Google Scholar 

  • Godman FDC (1870) Natural history of the Azores, or Western Islands. John Van Voorst, London

    Google Scholar 

  • Guiller A, Bellido A, Madec L (1998) Genetic distances and ordination: the land snail Helix aspersa in North Africa as a test case. Syst Biol 47:208–227

    Article  CAS  PubMed  Google Scholar 

  • Guinand B (1996) Use of a multivariate model using allele frequency distributions to analyse patterns of genetic differentiation among populations. Biol J Linn Soc 58:173–195

    Article  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  • Hanke M, Wink M (1994) Direct DNA sequencing of PCR-amplified vector inserts following enzymatic degradation of primer and dNTPs. Biotechniques 17:858–860

    CAS  PubMed  Google Scholar 

  • Harrison DL, Lewis RE (1964) A note on the occurrence of the weasel (Mustela nivalis Linnaeus, 1766) (Carnivora: Mustelinae) in Lebanon. Z Säugetierkd 29:179–181

    Google Scholar 

  • Hays WS, Conant S (2007) Biology and impacts of Pacific Island invasive species. 1. A worldwide review of effects of the small Indian mongoose, Herpestes javanicus (Carnivora: Herpestidae). Pac Sci 61:3–16

    Article  Google Scholar 

  • Hinten G, Harriss F, Rossetto M, Braverstock PR (2003) Genetic variation and island biogeography: microsatellite and mitochondrial DNA variation in island populations of the Australian bush rat, Rattus fuscipes greyii. Conserv Genet 4:759–778

    Article  CAS  Google Scholar 

  • Ho SYW, Shapiro B, Phillips MJ, Cooper A, Drummond AJ (2007) Evidence for time dependency of molecular rate estimates. Syst Biol 56:515–522

    Article  PubMed  Google Scholar 

  • Holder MT, Sukumaran J, Lewis PO (2008) A justification for reporting the majority-rule consensus tree in Bayesian phylogenetics. Syst Biol 57:814–821

    Article  PubMed  Google Scholar 

  • Holland LA (1937) Herodotus I, 94: a Phocaean Version of an Etruscan Tale. Am J Archaeol 41:377–382

    Article  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    Article  PubMed  PubMed Central  Google Scholar 

  • Huelsenbeck JP, Larget B, Alfaro ME (2004) Bayesian phylogenetic model selection using reversible jump Markov chain Monte Carlo. Mol Biol Evol 21:1123–1133

    Article  CAS  PubMed  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Jarman MR (1996) Human influence in the development of the Cretan mammalian fauna. In: Reese DS (ed) Pleistocene and Holocene fauna of Crete and its first settlers. Monographs in World Archaeology 28. Prehistory Press, Madison, pp 211–229

  • Johnson JR, Thomson RC, Micheletti SJ, Shaffer HB (2011) The origin of tiger salamander (Ambystoma tigrinum) populations in California, Oregon, and Nevada: introductions or relicts? Conserv Genet 12:355–370

    Article  Google Scholar 

  • Jombart T, Pontier D, Dufour AB (2009) Genetic markers in the playground of multivariate analysis. Heredity 102:330–341

    Article  CAS  PubMed  Google Scholar 

  • Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543

    Article  CAS  Google Scholar 

  • Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Kasparek M (1988) On the occurrence of the Weasel, Mustela nivalis, in Turkey. Zool Middle East 2:8–11

    Article  Google Scholar 

  • Keller SR, Taylor DR (2008) History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection. Ecol Lett 11:852–866

    Article  PubMed  Google Scholar 

  • Kelley JE Jr (1979) Non-Mediterranean influences that shaped the Atlantic in the early Portolan charts. Imago Mundi 31:18–35

    Google Scholar 

  • King RJ, Di Cristofaro J, Kouvatsi A, Triantaphyllidis C, Scheidel W, Myres NM, Lin AA, Eissautier A, Mitchell M, Binder D, Semino O, Novelletto A, Underhill PA, Chiaroni J (2011) The coming of the Greeks to Provence and Corsica: Y-chromosome models of archaic Greek colonization of the western Mediterranean. BMC Evol Biol 11:69

    Article  PubMed  PubMed Central  Google Scholar 

  • Kreiser BR, Mitton JB, Woodling JD (2000) Single versus multiple sources of introduced populations identified with molecular markers: a case study of a freshwater fish. Biol Invasions 2:295–304

    Article  Google Scholar 

  • Kruskal JB (1964) Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1–27

    Article  Google Scholar 

  • Lanfear R, Calcott B, Ho SY, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701

    Article  CAS  PubMed  Google Scholar 

  • Langella O (1999) Populations 1.2.30. CNRS UPR9034. http://bioinformatics.org/populations/

  • Lebarbenchon C, Poitevin F, Montgelard C (2006) Genetic variation of the weasel (Mustela nivalis) in Corsica based on mitochondrial control region sequences. Mamm Biol 71:164–171

    Google Scholar 

  • Lebarbenchon C, Poitevin F, Arnal V, Montgelard C (2010) Phylogeography of the weasel (Mustela nivalis) in the western-Palaearctic region: combined effects of glacial events and human movements. Heredity 105:449–462

    Article  CAS  PubMed  Google Scholar 

  • Lehmann EV, Nobis G (1979) Subfossile Mauswiesel, Mustela nivalis Linné, 1766 aus Enkomia-Alasia auf Zypern. Bonn Zool Beitr 30:32–38

    Google Scholar 

  • Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116

    Article  Google Scholar 

  • Lowe S, Browne M, Boudjelas S, De Poorter M (2004) 100 of the World’s worst invasive alien species. A selection from the global invasive species database. The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN)

  • Malkin I (2011) A small Greek world: networks in the Ancient Mediterranean. Oxford University Press, New York

    Book  Google Scholar 

  • Marmi J, López-Giráldez F, Macdonald DW, Calafell F, Zholnerovskaya E, Domingo-Roura X (2006) Mitochondrial DNA reveals a strong phylogeographic structure in the badger across Eurasia. Mol Ecol 15:1007–1020

    Article  CAS  PubMed  Google Scholar 

  • Masseti M (1995) Quaternary biogeography of the Mustelidae family on the Mediterranean islands. Hystrix 7:17–34

    Google Scholar 

  • Masseti M (2009) Carnivores of Syria. ZooKeys 31:229–252

    Article  Google Scholar 

  • Mathias ML, Santos-Reis M, Petrucci-Fonseca F, Libois R, Fons R, Ferraz de Carvalho G, Oom MM, Collares-Pereira M (1998) Mammals from the Azores islands (Portugal): an updated overview. Mammalia 62:397–407

    Article  Google Scholar 

  • McDevitt AD, Zub K, Kawalko A, Oliver MK, Herman JS, Wojcik JM (2012) Climate and refugial origin influence the mitochondrial lineage distribution of weasels (Mustela nivalis) in a phylogeographic suture zone. Biol J Linn Soc 106:57–69

    Article  Google Scholar 

  • Medina FM, Bonnaud E, Vidal E, Tershy BR, Zavaleta ES, Donlan CJ, Keitt BS, Le Corre M, Horwath SV, Nogales M (2011) A global review of the impacts of invasive cats on island endangered vertebrates. Glob Change Biol 17:3503–3510

    Article  Google Scholar 

  • Miller GS (1912) Catalogue of the Mammals of Western Europe (Europe exclusive of Russia) in the collection of the British Museum. Trustees of the British Museum, London

    Google Scholar 

  • Miró M, Santos M (2014) The Greek presence on the east coast of the Iberian Peninsula: colonial establishments and rhythms of trade with Iberian societies. Catalan Hist Rev 7:9–28

    Google Scholar 

  • Montgomery WI, Montgomery SS, Reid N (2015) Invasive alien species disrupt spatial and temporal ecology and threaten extinction in an insular, small mammal community. Biol Invasions 17:179–189

    Article  Google Scholar 

  • Moore JW (2010) Madeira, sugar, and the conquest of nature in the “first” sixteenth century, part II: from Regional Crisis to Commodity Frontier, 1506–1530. Review (Fernand Braudel Center) 33:1–24

    Google Scholar 

  • Muirhead JR, Gray DK, Kelly DW, Ellis SM, Heath DD, MacIsaac HJ (2008) Identifying the source of species invasions: sampling intensity vs. genetic diversity. Mol Ecol 17:1020–1035

    Article  CAS  PubMed  Google Scholar 

  • Muñoz-Fuentes V, Green AJ, Sorenson MD, Negro JJ, Vila C (2006) The ruddy duck Oxyura jamaicensis in Europe: natural colonization or human introduction? Mol Ecol 15:1441–1453

    Article  PubMed  CAS  Google Scholar 

  • Negbi O (1992) Early Phoenician presence in the Mediterranean islands: a reappraisal. Am J Archaeol 96:599–615

    Article  Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Article  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nye TMW, Lio P, Gilks WR (2006) A novel algorithm and web-based tool for comparing two alternative phylogenetic trees. Bioinformatics 22:117–119

    Article  CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research - an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Pike G (1971) The animal bones from the Xenixija tombs. In: Evans JD (ed) The Prehistoric Antiquities of the Maltese Islands: a Survey. University of London, The Athlone Press, London, pp 239–241

    Google Scholar 

  • Pinya S, Carretero MA (2011) The Balearic herpetofauna: a species update and a review on the evidence. Acta Herpetol 6:59–80

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Puillandre N, Dupas S, Dangles O, Zeddam JL, Capdevielle-Dulac C, Barbin K, Torres-Leguizamon M, Silvain JF (2008) Genetic bottleneck in invasive species: the potato tuber moth adds to the list. Biol Invasions 10:319–333

    Article  Google Scholar 

  • Rigsby KJ (1987) Phocians in Sicily: Thucydides 6.2. Class Q 37:332–335

    Article  Google Scholar 

  • Rodrigues AF (2015) Megalithic constructions discovered in the Azores, Portugal. Archaeol Discov 3:51–61

    Article  Google Scholar 

  • Rodrigues M, Santos-Reis M, Elmeros M, Fernandes CA (2012) Microsatellite markers for genetic studies in the weasel (Mustela nivalis). Eur J Wildl Res 58:507–510

    Article  Google Scholar 

  • Rodrigues AF, Martins NO, Ribeiro N, Joaquinito A (2015) Early Atlantic navigation: pre-Portuguese presence in the Azores Islands. Archaeol Discov 3:104–113

    Article  Google Scholar 

  • Rodrigues M, Bos AR, Hoath R, Schembri PJ, Lymberakis P, Cento M, Ghawar W, Ozkurt SO, Santos-Reis M, Merilä J, Fernandes C (2016) Taxonomic status and origin of the Egyptian weasel (Mustela subpalmata) inferred from mitochondrial DNA. Genetica 144:191–202

    Article  PubMed  Google Scholar 

  • Roller DW (2006) Through the pillars of Herakles: Greco-Roman exploration of the Atlantic. Routledge, New York

    Google Scholar 

  • Romano V, Cali F, Ragalmuto A, D’Anna RP, Flugy A, De Leo G, Giambalvo O, Lisa A, Fiorani O, Di Gaetano C, Salerno A, Tamouza R, Charron D, Matullo G, Piazza A (2003) Autosomal microsatellite and mtDNA genetic analysis in Sicily (Italy). Ann Hum Genet 67:42–53

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Ruffino L, Vidal E (2010) Early colonization of Mediterranean islands by Rattus rattus: a review of zooarcheological data. Biol Invasions 12:2389–2394

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Santos C, Lima M, Montiel R, Angles N, Pires L, Abade A, Aluja MP (2003) Genetic structure and origin of peopling in the Azores islands (Portugal): the view from mtDNA. Ann Hum Genet 67:433–456

    Article  CAS  PubMed  Google Scholar 

  • Sax DF, Brown JH (2000) The paradox of invasion. Glob Ecol Biogeogr 9:363–371

    Article  Google Scholar 

  • Sax DF, Stachowicz JJ, Brown JH, Bruno JF, Dawson MN, Gaines SD, Grosberg RK, Hastings A, Holt RD, Mayfield MM, O’Connor MI, Rice WR (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22:465–471

    Article  PubMed  Google Scholar 

  • Shackleton JC, van Andel TH, Runnels CN (1984) Coastal paleogeography of the central and western Mediterranean during the last 125,000 years and its archaeological implications. J Field Archaeol 11:307–314

    Google Scholar 

  • Shaw JW (1989) Phoenicians in southern Crete. Am J Archaeol 93:165–183

    Article  Google Scholar 

  • Sheffield SR, King CM (1994) Mustela nivalis. Mammalian Species 454:1–10

    Article  Google Scholar 

  • Short J (1998) The extinction of rat-kangaroos (Marsupialia: Potoroidae) in New South Wales, Australia. Biol Conserv 86:365–377

    Article  Google Scholar 

  • Sidorovich VE, Pikulik MM (1997) Toads Bufo spp. in the diets of mustelid predators in Belarus. Acta Theriol 42:105–108

    Article  Google Scholar 

  • Simberloff D, Gibbons L (2004) Now you see them, now you don’t!—population crashes of established introduced species. Biol Invasions 6:161–172

    Article  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Stöver BC, Müller KF (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinform 11:7

    Article  Google Scholar 

  • Suarez AV, Tsutsui ND (2008) The evolutionary consequences of biological invasions. Mol Ecol 17:351–360

    Article  PubMed  Google Scholar 

  • Sukumaran J, Holder MT (2010) DendroPy: a Python library for phylogenetic computing. Bioinformatics 26:1569–1571

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  PubMed  Google Scholar 

  • Thomas O (1895) On the long-lost Putorius africanus, Desm., and its occurrence in Malta. Proc Zool Soc Lond 63:128–131

    Google Scholar 

  • Thomas O (1901) On the mammals of the Balearic Islands. Proc Zool Soc Lond 70:35–44

    Article  Google Scholar 

  • Tikhonov A, Cavallini P, Maran T, Kranz A, Herrero J, Giannatos G, Stubbe M, Conroy J, Kryštufek B, Abramov A, Wozencraft C, Reid F, McDonald R (2008) Mustela nivalis. The IUCN Red List of Threatened Species. Version 2015.2. www.iucnredlist.org

  • Tomás G, Seco L, Seixas S, Faustino P, Lavinha J, Rocha J (2002) The peopling of São Tomé (Gulf of Guinea): origins of slave settlers and admixture with the Portuguese. Hum Biol 74:397–411

    Article  PubMed  Google Scholar 

  • Towns DR, Atkinson IA, Daugherty CH (2006) Have the harmful effects of introduced rats on islands been exaggerated? Biol Invasions 8:863–891

    Article  Google Scholar 

  • Traveset A, Nogales M, Alcover JA, Delgado JD, López-Darias M, Godoy D, Igual JM, Bover P (2009) A review on the effects of alien rodents in the Balearic (Western Mediterranean Sea) and Canary Islands (Eastern Atlantic Ocean). Biol Invasions 11:1653–1670

    Article  Google Scholar 

  • Tsutsui ND, Suarez AV, Holway DA, Case TJ (2001) Relationships among native and introduced populations of the Argentine ant (Linepithema humile) and the source of introduced populations. Mol Ecol 10:2151–2161

    Article  CAS  PubMed  Google Scholar 

  • Valenzuela A, Alcover JA (2013) Radiocarbon evidence for a prehistoric deliberate translocation: the weasel (Mustela nivalis) of Mallorca. Biol Invasions 15:717–722

    Article  Google Scholar 

  • van Andel TH (1989) Late Quaternary sea-level changes and archaeology. Antiquity 63:733–745

    Article  Google Scholar 

  • van Dommelen P (1997) Colonial constructs: colonialism and archaeology in the Mediterranean. World Archaeol 28:305–323

    Article  Google Scholar 

  • van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • van Sister JL (2012) Cultural exchange on Malta and Gozo: a study of the Aegyptiaca on Malta and Gozo from the Phoenician and Punic periods. Bachelor thesis, Leiden University

  • Vázquez-Domínguez E, Suárez-Atilano M, Booth W, González-Baca C, Cuarón AD (2012) Genetic evidence of a recent successful colonization of introduced species on islands: Boa constrictor imperator on Cozumel Island. Biol Invasions 14:2101–2116

    Article  Google Scholar 

  • Veale AJ, Hannaford OD, Russell JC, Clout MN (2012) Modelling the distribution of stoats on New Zealand offshore islands. New Zeal J Ecol 36:38–47

    Google Scholar 

  • Vella NC (2005) Review of ‘The archaeology of Punic Malta’. J Roman Archaeol 18:436–450

    Article  Google Scholar 

  • Vigne JD (1992) Zooarchaeology and the biogeographical history of the mammals of Corsica and Sardinia since the last ice age. Mamm Rev 22:87–96

    Article  Google Scholar 

  • Villesen P (2007) FaBox: an online toolbox for fasta sequences. Mol Ecol Notes 7:965–968

    Article  CAS  Google Scholar 

  • Wright CA (1875) On the specific identity of the weasel found in Malta. Proc Zool Soc Lond 43:312–313

    Google Scholar 

  • Xia X (2013) DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution. Mol Biol Evol 30:1720–1728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7

    Article  CAS  PubMed  Google Scholar 

  • Yannouli E (2003) Non-domestic carnivores in Greek prehistory: a review. Br School Athens Stud 9:175–192

    Google Scholar 

  • Zima J, Cenevová E (2002) Coat colour and chromosome variation in central European populations of the weasel (Mustela nivalis). Folia Zool 51:265–274

    Google Scholar 

Download references

Acknowledgments

We thank Jean-François Noblet, Wissem Ghawar (Institut Pasteur de Tunis), Maurizio Gattabria (Museo Civico di Zoologia di Roma), Federico Striglioni and Gino Damiani (Parco Nazionale del Gran Sasso e Monti della Laga) and Parco Nazionale d’Abruzzo, Lazio e Molise for providing samples, Fátima Sobral and Ana Simões Nunes (DGV) for kindly providing access to an automated sequencer, and Arlindo Carvalho (São Tomé and Príncipe General-Directorate for the Environment) for the permit to collect and export samples. We also thank Associate Editor Marc Rius and three anonymous reviewers for their helpful comments and suggestions. This study was financed by Portuguese National Funds through Fundação para a Ciência e a Tecnologia (FCT), within the project UID/BIA/00329/2013. MR, RFL and CF acknowledge financial support from Fundação para a Ciência e Tecnologia (FCT, MCTES, Portugal) through, respectively, the PhD fellowship SFRH/BD/60595/2009, the post-doctoral grant SFRH/BPD/91494/2012 and the Ciência 2007 contract C2007-UL-342-CBA1. JM acknowledges support from the Academy of Finland (Grants 200940, 108601 and 118673). ARB acknowledges financial support from the American University in Cairo through a faculty research grant. PJS thanks the Malta Environment and Planning Authority for granting permits to work on the protected Maltese weasel, and Dr. Katrin Fenech and Dr. Nicholas C. Vella for information on the Phoenicians in Malta. SOO acknowledges support from the Turkish National Science Foundation (TUBITAK) through the project 110T930.

Author information

Authors and Affiliations

  1. CE3C – Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, 1749-016, Lisbon, Portugal

    Mónica Rodrigues, Ricardo F. de Lima, Margarida Santos-Reis & Carlos Fernandes

  2. Ecological Genetics Research Unit, Department of Biosciences, University of Helsinki, PO Box 65, 00014, Helsinki, Finland

    Mónica Rodrigues & Juha Merilä

  3. The American University in Cairo, PO Box 74, New Cairo, 11835, Egypt

    Arthur R. Bos

  4. Naturalis Biodiversity Centre, PO Box 9517, 2300 RA, Leiden, The Netherlands

    Arthur R. Bos

  5. Department of Biology, University of Malta, Msida, 2080, Malta

    Patrick J. Schembri

  6. Associação Monte Pico, Monte Café, São Tomé, São Tomé and Príncipe

    Ricardo F. de Lima

  7. Natural History Museum of Crete, University of Crete, 71409, Iraklion, Crete, Greece

    Petros Lymberakis

  8. Consorci per a la Recuperació de la Fauna de les Illes Balears (COFIB), Santa Eugènia, Spain

    Lluís Parpal

  9. SROPU Bird Observation and Protection Station of Rome, 00165, Rome, Italy

    Michele Cento

  10. Office National de la Chasse et de la Faune Sauvage, CNERA-PAD, 01330, Birieux, France

    Sandrine Ruette

  11. Faculty of Education, Ahi Evran University, Kırşehir, Turkey

    Sakir O. Ozkurt

Authors
  1. Mónica Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Arthur R. Bos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Patrick J. Schembri
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ricardo F. de Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Petros Lymberakis
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lluís Parpal
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michele Cento
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sandrine Ruette
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sakir O. Ozkurt
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Margarida Santos-Reis
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Juha Merilä
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Carlos Fernandes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mónica Rodrigues.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

An erratum to this article is available at http://dx.doi.org/10.1007/s10530-016-1347-3.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 214 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rodrigues, M., Bos, A.R., Schembri, P.J. et al. Origin and introduction history of the least weasel (Mustela nivalis) on Mediterranean and Atlantic islands inferred from genetic data. Biol Invasions 19, 399–421 (2017). https://doi.org/10.1007/s10530-016-1287-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-016-1287-y

Keywords

  • Least weasel
  • Mediterranean islands
  • Azores
  • São Tomé Island
  • Genetic markers
  • Introduced species