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

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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.

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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.

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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

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  1. Mónica Rodrigues
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Correspondence to Mónica Rodrigues.

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

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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

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