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Molecular and morphological insights into the origin of the invasive greater white-toothed shrew (Crocidura russula) in Ireland

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Abstract

Identifying routes of invasion is a critical management strategy in controlling the spread of invasive species. This is challenging however in the absence of direct evidence. Therefore, indirect methodologies are used to infer possible invasion sources and routes, such as comparisons of genetic and morphological data from populations from invasive ranges and putative source areas. The greater white-toothed shrew (Crocidura russula) was first discovered in Ireland from skeletal remains in the pellets of birds of prey collected in 2007 and is it is now sufficiently established that the species has a detrimental impact on Ireland’s small mammal community. In this study, we address the uncertain origin(s) of the Irish population of C. russula. The cytochrome b gene of mitochondrial DNA was analysed from 143 individuals from throughout its range within a phylogenetic and approximate Bayesian computation framework. These analyses revealed that the Irish population stemmed from Europe as opposed to North Africa. Additionally, mandibles from 523 individuals from Ireland and 28 other European populations were subjected to multivariate and distance-based analyses, which demonstrated an association between the Irish population and those in France, Switzerland and Belgium. When the genetic and morphological analyses were considered together, an origin stemming from France was deemed the most likely scenario for the source of the invasive Irish population. This study has demonstrated the importance of utilising a multidisciplinary approach when attempting to identify the origins and invasion routes of invasive species.

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Acknowledgments

This work was part of L.M.G.’s M.Sc. in Evolutionary Biology in University College Dublin (UCD) and A.D.M.’s Government of Ireland Postdoctoral Fellowship awarded by the Irish Research Council (Grant No.: PD/2011/2093). Laboratory work was partly funded by UCD and A.D.M. was provided with further funding from the Heritage Council, Ireland (Grant No.: R02511); a Heredity fieldwork grant awarded by the Genetics Society; and the Vincent Wildlife Trust for fieldwork. JP is currently supported by Project “Genomics and Evolutionary Biology” co-financed by North Portugal Regional Operational Programme 2007/2013 (ON.2 – O Novo Norte), under the National Strategic Reference Framework (NSRF), through the European Regional Development Fund (ERDF). Samples from Molène and Groix (Brittany) were obtained in the framework of an ATM project (“Biodiversités”, 2011) from the Museum National d’Histoire Naturelle in Paris. We are extremely grateful to Damien McDevitt, Ruth Carden and Ilaria Coscia for assistance during fieldwork in Ireland and to Tom White for providing samples. Thanks to Carlotta Sacchi and Danielle Dunlea for assistance in the lab. Thanks to Sylvian Dubey, Anna Bannikova and Jean-Francois Cosson for discussions on cyt b primers for Crocidura russula and to Ilaria Coscia for advice on ABC. We are further grateful to Jean-Francois Cosson for providing raw sequence data from his 2005 publication. Thanks to Alan Kelly and Barry McMahon for information on Irish agricultural imports, Juan Rofes for information on fossil records of C. russula in Europe, and to the editor and reviewer for comments on the manuscript. We dedicate this paper to two great scientists who’ve taught us so much about small mammals in general, our co-author Michel Pascal, and Peter Vogel, who both unfortunately left us during this project.

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    Authors and Affiliations

    1. School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland

      Laura M. Gargan, Jon M. Yearsley & Allan D. McDevitt

    2. Institut de Systématique, Évolution et Biodiversité, Centre National de la Recherche Scientifique/Muséum National d’Histoire Naturelle, 45 Rue Buffon, 75005, Paris, France

      Raphaël Cornette

    3. School of Biological Sciences, Queen’s University Belfast, Belfast, BT9 7BL, Northern Ireland, UK

      W. Ian Montgomery

    4. Institute of Global Food Security, Queen’s University Belfast, Belfast, BT9 5BN, Northern Ireland, UK

      W. Ian Montgomery

    5. InBIO Laboratório Associado, CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus Agrãrio de Vairão, 4485-661, Vairão, Portugal

      Joana Paupério & Paulo C. Alves

    6. Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, Rua do Campo Alegre s/n, 4169-007, Porto, Portugal

      Paulo C. Alves

    7. Wildlife Biology Program, College of Forestry and Conservation, University of Montana, 32 Campus Drive, Missoula, MT, 59801, USA

      Paulo C. Alves

    8. School of Biological, Earth and Environmental Sciences, Environmental Research Instiitute, University College Cork, Distillery Fields, North Mall, Cork, Ireland

      Fidelma Butler

    9. Équipes Gestion des Populations Invasives, INRA, Station SCRIBE, Campus de Beaulieu, 35042, Rennes Cedex, France

      Michel Pascal

    10. Archéozoologie et Archéobotanique, Sociétés, Pratiques et Environnements, Département d’Ecologie et Gestion de la Biodiversité, Centre National de la Recherche Scientifique/Muséum National d’Histoire Naturelle, 57 rue Cuvier, Case postale 55, 75231, Paris Cedex 5, France

      Anne Tresset

    11. Département d’Ecologie et de Gestion de la Biodiversité, Centre National de la Recherche Scientifique/Muséum National d’Histoire Naturelle, 57 rue Cuvier, Case postale 55, 75231, Paris Cedex 5, France

      Anthony Herrel

    12. Evolutionary Morphology of Vertebrates, Ghent University, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium

      Anthony Herrel

    13. Birdwatch Ireland, Midlands Office, Crank House, Banagher, Co. Offaly, Ireland

      John Lusby

    14. Quercus, School of Biological Sciences, Queen’s University Belfast, Belfast, BT9 7BL, Northern Ireland, UK

      David G. Tosh

    15. Department of Ecology and Evolution, Corson Hall, Cornell University, Ithaca, NY, 14853-2701, USA

      Jeremy B. Searle

    16. School of Environment and Life Sciences, University of Salford, Salford, M5 4WT, UK

      Allan D. McDevitt

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    1. Laura M. Gargan
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    2. Raphaël Cornette
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    3. Jon M. Yearsley
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    4. W. Ian Montgomery
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    8. Michel Pascal
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    9. Anne Tresset
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    12. David G. Tosh
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    14. Allan D. McDevitt
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    Correspondence to Allan D. McDevitt.

    Additional information

    Laura M. Gargan and Raphaël Cornette have contributed equally to this work.

    Michel Pascal: Deceased.

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    Gargan, L.M., Cornette, R., Yearsley, J.M. et al. Molecular and morphological insights into the origin of the invasive greater white-toothed shrew (Crocidura russula) in Ireland. Biol Invasions 18, 857–871 (2016). https://doi.org/10.1007/s10530-016-1056-y

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