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Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Genetic structure of introduced American mink (Neovison vison) in Patagonia: colonisation insights and implications for control and management strategies

Mónica Mora A , Gonzalo Medina-Vogel B , Maximiliano A. Sepúlveda C , Daly Noll A D , Rocío Álvarez-Varas A D and Juliana A. Vianna A E
+ Author Affiliations
- Author Affiliations

A Departamento de Ecosistemas y Medio Ambiente, Facultad de Agronomía e Ingeniería Forestal, Pontificia Universidad Católica de Chile, Vicuña Mackenna 4860, Santiago 7820436, Chile.

B Centro de Investigación para la Sustentabilidad, Universidad Andrés Bello, República 440, Santiago Centro, Santiago 8320000, Chile.

C Gerencia de Áreas Silvestres Protegidas del Estado, Corporación Nacional Forestal, Paseo Bulnes 285, Santiago 8330407, Chile.

D Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Las Palmeras 3425, Ñuñoa, Santiago 7800003, Chile.

E Corresponding author. Email: jvianna@uc.cl

Wildlife Research 45(4) 344-356 https://doi.org/10.1071/WR18026
Submitted: 9 February 2018  Accepted: 23 April 2018   Published: 18 July 2018

Abstract

Context: Biological invasions have caused dramatic changes in native biodiversity and ecosystem function. Studies of genetic variation and evolutionary changes are useful for understanding population dynamics during biological invasions, and shed light on management, prevention and restoration strategies.

Aims: This study aimed to investigate the structure and genetic variability of American mink (Neovison vison), an invasive species in southern South America, introduced for fur farming in the 1930s.

Methods: Samples from 153 mink were obtained from 12 locations in southern Chile to sequence the mitochondrial DNA (mtDNA) control region and to genotype 11 polymorphic microsatellite loci.

Key results: The highest mtDNA diversity was detected in Puerto Cisnes, suggesting multiple introductions and/or the most probable area where mink was first introduced. The latter is also supported by microsatellite data, because a high percentage of individuals from different locations were assigned to this location. All other locations showed low or no mtDNA diversity, possibly due to founder effect. The results also indicate marked population structure, with three genetic clusters coincident with the main historical introduction points, with low dispersal among them.

Conclusions: The results suggest that control strategies for American mink in southern Chile should be concentrated on these three genetically differentiated management units, and particularly on source populations and locations with low effective population size and restricted connectivity.

Implications: Genetic approaches have been used for the management of numerous alien species worldwide. Recommendations delivered here for American mink control could also be implemented in other regions and for other invasive species with similar genetic diversity distribution and connectivity.

Additional keywords: conservation genetics, invasive species, molecular ecology, pest management, vertebrates.


References

Abdelkrim, J., Pascal, M., Calmet, C., and Samadi, S. (2005). Importance of assessing population genetic structure before eradication of invasive species: examples from insular Norway rat populations. Conservation Biology 19, 1509–1518.
Importance of assessing population genetic structure before eradication of invasive species: examples from insular Norway rat populations.Crossref | GoogleScholarGoogle Scholar |

Abdelkrim, J., Pascal, M., and Samadi, S. (2007). Establishing causes of eradication failure based on genetics: case study of ship rat eradication in Ste. Anne archipelago. Conservation Biology 21, 719–730.
Establishing causes of eradication failure based on genetics: case study of ship rat eradication in Ste. Anne archipelago.Crossref | GoogleScholarGoogle Scholar |

Aljanabi, S. M., and Martinez, I. (1997). Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research 25, 4692–4693.
Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques.Crossref | GoogleScholarGoogle Scholar |

Anistoroaei, R., Farid, A., and Christensen, K. (2006). Isolation and characterization of 79 microsatellite markers from the American mink (Mustela vison). Animal Genetics 37, 185–188.
Isolation and characterization of 79 microsatellite markers from the American mink (Mustela vison).Crossref | GoogleScholarGoogle Scholar |

Bandelt, H. J., Forster, P., and Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.
Median-joining networks for inferring intraspecific phylogenies.Crossref | GoogleScholarGoogle Scholar |

Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., and Bonhomme, F. (2001). GENETIX 4.02, logiciel sous Windows TM pour la genetique des populations. Lab Genome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, France

Belliveau, A. M., Farid, A., O’Connell, M., and Wright, J. M. (1999). Assessment of genetic variability in captive and wild American mink (Mustela vison) using microsatellite markers. Canadian Journal of Animal Science 79, 7–16.

Bifolchi, A., Picard, D., Lemaire, C., Cormier, J. P., and Pagano, A. (2010). Evidence of admixture between differentiated genetic pools at a regional scale in an invasive carnivore. Conservation Genetics 11, 1–9.
Evidence of admixture between differentiated genetic pools at a regional scale in an invasive carnivore.Crossref | GoogleScholarGoogle Scholar |

Bonesi, L., and Palazon, S. (2007). The American mink in Europe: status, impacts, and control. Biological Conservation 134, 470–483.
The American mink in Europe: status, impacts, and control.Crossref | GoogleScholarGoogle Scholar |

Cornuet, J. M., and Luikart, G. (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014.

Crego, R. D., Jiménez, J. E., and Rozzi, R. (2015). Invasive expansion of the American mink (Neovison vison) in the Cape Horn Biosphere Reserve, Chile. Anales del Instituto de la Patagonia 43, 157–162.
Invasive expansion of the American mink (Neovison vison) in the Cape Horn Biosphere Reserve, Chile.Crossref | GoogleScholarGoogle Scholar |

Di Rienzo, A., Peterson, A. C., Garza, J. C., Valdes, A. M., Slatkin, M., and Freimer, N. B. (1994). Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the National Academy of Sciences of the United States of America 91, 3166–3170.
Mutational processes of simple-sequence repeat loci in human populations.Crossref | GoogleScholarGoogle Scholar |

Dlugosch, K. M., and Parker, I. M. (2008). Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology 17, 431–449.
Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions.Crossref | GoogleScholarGoogle Scholar |

Earl, D. A., and vonHoldt, B. M. (2012). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method.Crossref | GoogleScholarGoogle Scholar |

Evanno, G., Regnaut, S., and Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.
Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.Crossref | GoogleScholarGoogle Scholar |

Excoffier, L., and Lischer, H. E. L. (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar |

Fleming, M. A., Ostrander, E. A., and Cook, J. A. (1999). Microsatellite markers for American mink (Mustela vison) and ermine (Mustela erminea). Molecular Ecology 8, 1352–1355.
Microsatellite markers for American mink (Mustela vison) and ermine (Mustela erminea).Crossref | GoogleScholarGoogle Scholar |

Frankham, R., Ballou, J. D., and Briscoe, D. A. (2002). ‘Introduction to Conservation Genetics.’ (Cambridge University Press: Cambrigde, UK.)

Fraser, E. J., Macdonald, D. W., Oliver, M. K., Piertney, S., and Lambin, X. (2013). Using population genetic structure of an invasive mammal to target control efforts. Biological Conservation 167, 35–42.
Using population genetic structure of an invasive mammal to target control efforts.Crossref | GoogleScholarGoogle Scholar |

Genovesi, P. (2009). Invasive alien species in a changing world. Biodiversity (Nepean) 10, 3–4.
Invasive alien species in a changing world.Crossref | GoogleScholarGoogle Scholar |

Goudet, J. (1995). A program for estimating and testing gene diversities and differentiation statistics from codominant genetic markers. The Journal of Heredity 86, 485–486.
A program for estimating and testing gene diversities and differentiation statistics from codominant genetic markers.Crossref | GoogleScholarGoogle Scholar |

Grapputo, A., Boman, S., Lindström, L., Lyytinen, A., and Mappes, J. (2005). The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations. Molecular Ecology 14, 4207–4219.
The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations.Crossref | GoogleScholarGoogle Scholar |

Guillot, G., Mortier, F., and Estoup, A. (2005). GENELAND: a computer package for landscape genetics. Molecular Ecology Notes 5, 712–715.
GENELAND: a computer package for landscape genetics.Crossref | GoogleScholarGoogle Scholar |

Harrington, L. A., and Macdonald, D. W. (2008). Spatial and temporal relationships between invasive American mink and native European polecats in the southern United Kingdom. Journal of Mammalogy 89, 991–1000.
Spatial and temporal relationships between invasive American mink and native European polecats in the southern United Kingdom.Crossref | GoogleScholarGoogle Scholar |

Hill, W. G. (1981). Estimation of effective population size from data on linkage disequilibrium. Genetical Research 38, 209–216.
Estimation of effective population size from data on linkage disequilibrium.Crossref | GoogleScholarGoogle Scholar |

Jaksic, F. M., Iriarte, J. A., Jiménez, J. E., and Martínez, D. R. (2002). Invaders without Frontiers: Cross-border Invasions of Exotic Mammals. Biological Invasions 4, 157–173.
Invaders without Frontiers: Cross-border Invasions of Exotic Mammals.Crossref | GoogleScholarGoogle Scholar |

Jiménez, J. E., Crego, R. D., Soto, G. E., Román, I., Rozzi, R., and Vergara, P. M. (2014). Potential impact of the alien American mink (Neovison vison) on Magellanic woodpeckers (Campephilus magellanicus) in Navarino Island, Southern Chile. Biological Invasions 16, 961–966.
Potential impact of the alien American mink (Neovison vison) on Magellanic woodpeckers (Campephilus magellanicus) in Navarino Island, Southern Chile.Crossref | GoogleScholarGoogle Scholar |

Jombart, T., and Collins, C. (2015). A tutorial for Discriminant Analysis of Principal Components (DAPC) using Adegenet 2.0.0. Available at http://adegenet.r-forge.r-project.org/files/tutorial-dapc.pdf [accessed June 2018].

Kimura, M., and Otha, T. (1978). Stepwise mutation model and distribution of allelic frequencies in a finite population. Proceedings of the National Academy of Sciences of the United States of America 75, 2868–2872.
Stepwise mutation model and distribution of allelic frequencies in a finite population.Crossref | GoogleScholarGoogle Scholar |

Korbie, D. J., and Mattick, J. S. (2008). Touchdown PCR for increased specificity and sensitivity in PCR amplification. Nature Protocols 3, 1452.
Touchdown PCR for increased specificity and sensitivity in PCR amplification.Crossref | GoogleScholarGoogle Scholar |

Lecis, R., Ferrando, A., Ruiz-Olmo, J., Mañas, S., and Domingo-Roura, X. (2008). Population genetic structure and distribution of introduced American mink (Mustela vison) in Spain, based on microsatellite variation. Conservation Genetics 9, 1149–1161.
Population genetic structure and distribution of introduced American mink (Mustela vison) in Spain, based on microsatellite variation.Crossref | GoogleScholarGoogle Scholar |

Luikart, G., Allendorf, F. W., Cornuet, J. M., and Sherwin, W. B. (1998). Distortion of allele frequency distributions provides a test for recent population bottlenecks. The Journal of Heredity 89, 238–247.
Distortion of allele frequency distributions provides a test for recent population bottlenecks.Crossref | GoogleScholarGoogle Scholar |

Martínez, D. R., Rau, J. R., Soriguer, R. C., and Beltran, J. F. (1999). Ecología espacial del visón americano introducido en el sur de Chile: Ámbito de hogar y descriptores de hábitat. Actas del II Taller Nacional Sobre Carnívoros, Región de Aysén, Chile.

Medina, G. (1997). A comparison of the diet and distribution of southern river otter (Lutra provocax) and mink (Mustela vison) in southern Chile. Journal of Zoology 242, 291–297.
A comparison of the diet and distribution of southern river otter (Lutra provocax) and mink (Mustela vison) in southern Chile.Crossref | GoogleScholarGoogle Scholar |

Medina-Vogel, G., Barros, M., Monsalve, R., and Pons, D. J. (2015). Assessment of the efficiency in trapping North American mink (Neovison vison) for population control in Patagonia. Revista Chilena de Historia Natural 88, 9.
Assessment of the efficiency in trapping North American mink (Neovison vison) for population control in Patagonia.Crossref | GoogleScholarGoogle Scholar |

O’Connell, M., Wright, J. M., and Farid, A. (1996). Development of PCR primers for nine polymorphic American mink Mustela vison microsatellite loci. Molecular Ecology 5, 311–312.

Peel, D., Ovenden, J. R., and Peel, S. L. (2004). NeEstimator: software for estimating effective population size, Version 1.3. Queensland Government, Department Primary Industries and Fisheries, Brisbane.

Piry, S., Alapetite, A., Cornuet, J. M., Paetkau, D., Baudouin, L., and Estoup, A. (2004). GENECLASS2: a software for genetic assignment and first-generation migrant detection. The Journal of Heredity 95, 536–539.
GENECLASS2: a software for genetic assignment and first-generation migrant detection.Crossref | GoogleScholarGoogle Scholar |

Pritchard, J. K., Stephens, M., and Donnelly, P. J. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.

Pudovkin, A. I., Zaykin, D. V., and Hedgecock, D. (1996). On the potential for estimating the effective number of breeders from heterozygote excess in progeny. Genetics 144, 383–387.

Rannala, B., and Mountain, J. L. (1997). Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences of the United States of America 94, 9197–9201.
Detecting immigration by using multilocus genotypes.Crossref | GoogleScholarGoogle Scholar |

Raymond, M., and Rousset, F. (1995). An exact test for population differentiation. Evolution 49, 1280–1283.
An exact test for population differentiation.Crossref | GoogleScholarGoogle Scholar |

Rozzi, R., and Sherriffs, M. (2003). El visón (Mustela vison Schreber, Carnivora: Mustelidae), un nuevo mamífero exótico para la isla Navarino. Anales del Instituto de la Patagonia 31, 97–104.

SAG (2011). Legislación La Ley de Caza y su Reglamento, 12va edn. Unidad comunicación y prensa, Servicio Agrícola y Ganadero, Subdepartamento de Vida Silvestre DIPROREN, Santiago, Chile. [In Spanish]

Sandoval, R. J., and Schlatter, R. (1994). Estudio ecológico del visón asilvestrado (Mustela vison, Schreber) en la XI Región. Veterinary Degree (DVM) Thesis, Universidad Austral de Chile. [In Spanish]

Sandoval, R., Bahamonde, A., Lagos, C., and Calderón, J. (2014). Control del visón (Neovison vison) mediante remoción no selectiva de individuos en Monumento Natural Dos Lagunas: I Informe de Avance. Informe Técnico SAG-CONAF. Región de Aysén, Chile. [In Spanish]

Schuelke, M. (2000). An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18, 233–234.
An economic method for the fluorescent labeling of PCR fragments.Crossref | GoogleScholarGoogle Scholar |

Schüttler, E., Klenkea, R., McGehee, S., Rozzi, R., and Jax, K. (2009). Vulnerability of ground-nesting waterbirds to predation by invasive American mink in the Cape Horn Biosphere Reserve, Chile. Biological Conservation 142, 1450–1460.
Vulnerability of ground-nesting waterbirds to predation by invasive American mink in the Cape Horn Biosphere Reserve, Chile.Crossref | GoogleScholarGoogle Scholar |

Shimatani, Y., Fukue, Y., Kishimoto, R., and Masuda, R. (2010). Genetic variation and population structure of the feral American mink (Neovison vison) in Nagano, Japan, revealed by microsatellite analysis. Mammal Study 35, 1–7.
Genetic variation and population structure of the feral American mink (Neovison vison) in Nagano, Japan, revealed by microsatellite analysis.Crossref | GoogleScholarGoogle Scholar |

Stevens, R. T., Kennedy, M. L., and Kelley, V. R. (2005). Genetic structure of American mink (Mustela vision) populations. The Southwestern Naturalist 50, 350–355.
Genetic structure of American mink (Mustela vision) populations.Crossref | GoogleScholarGoogle Scholar |

Tchaicka, L., Eizirik, E., De Oliveira, T. G., Cândido, J. F., and Freitas, T. R. O. (2007). Phylogeography and population history of the crab-eating fox (Cerdocyon thous). Molecular Ecology 16, 819–838.
Phylogeography and population history of the crab-eating fox (Cerdocyon thous).Crossref | GoogleScholarGoogle Scholar |

Vaghefi, N., Nelson, S. C., Kikkert, J. R., and Pethybridge, S. J. (2017). Genetic structure of Cercospora beticola populations on Beta vulgaris in New York and Hawaii. Scientific Reports 7, 1726.
Genetic structure of Cercospora beticola populations on Beta vulgaris in New York and Hawaii.Crossref | GoogleScholarGoogle Scholar |

Valenzuela, A. E., Sepúlveda, M. A., Cabello, J. L., and Anderson, C. B. (2016). El visón americano en Patagonia: un análisis histórico y socioecológico de la investigación y el manejo. Mastozoología Neotropical 23, 289–304.

Van Oosterhout, C., Hutchinson, W., Wills, D. P. M., and Shipley, P. (2004). MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data.Crossref | GoogleScholarGoogle Scholar |

Vergara, G., and Valenzuela, J. (2014). Presencia de visón americano (Neovison vison, Schreber 1777) en Chiloé, Chile: ¿inicio de una invasión biológica? Ecosistemas (Madrid) 24, 29–31.
Presencia de visón americano (Neovison vison, Schreber 1777) en Chiloé, Chile: ¿inicio de una invasión biológica?Crossref | GoogleScholarGoogle Scholar |

Weir, B. S., and Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.

Wirgin, I., Maceda, L., Waldman, J., and Mayack, D. T. (2015). Genetic variation and population structure of American mink Neovison vison from PCB-contaminated and non-contaminated locales in eastern North America. Ecotoxicology (London, England) 24, 1961–1975.
Genetic variation and population structure of American mink Neovison vison from PCB-contaminated and non-contaminated locales in eastern North America.Crossref | GoogleScholarGoogle Scholar |

Yamaguchi, N., and Macdonald, D. W. (2003). The burden of co-occupancy: intraspecific resource competition and spacing patterns in American mink, Mustela vison. Journal of Mammalogy 84, 1341–1355.
The burden of co-occupancy: intraspecific resource competition and spacing patterns in American mink, Mustela vison.Crossref | GoogleScholarGoogle Scholar |

Zalewski, A., Piertney, S., Zalewska, H., and Lambin, X. (2009). Landscape barriers reduce gene flow in an invasive carnivore: geographical and local genetic structure of American mink in Scotland. Molecular Ecology 18, 1601–1615.
Landscape barriers reduce gene flow in an invasive carnivore: geographical and local genetic structure of American mink in Scotland.Crossref | GoogleScholarGoogle Scholar |

Zalewski, A., Michalska-Parda, A., Bartoszewicz, M., Kozakiewicz, M., and Brzeziński, M. (2010). Multiple introductions determine the genetic structure of an invasive species population: American mink Neovison vison in Poland. Biological Conservation 143, 1355–1363.
Multiple introductions determine the genetic structure of an invasive species population: American mink Neovison vison in Poland.Crossref | GoogleScholarGoogle Scholar |

Zalewski, A., Michalska-Parda, A., Ratkiewicz, M., Kozakiewicz, M., Bartoszawicz, M., and Brzezin, M. (2011). High mitocondrial DNA diversity of an introduced alien carnivore: comparison of feral and ranch American mink Neovison vison in Poland. Diversity & Distributions 17, 757–768.
High mitocondrial DNA diversity of an introduced alien carnivore: comparison of feral and ranch American mink Neovison vison in Poland.Crossref | GoogleScholarGoogle Scholar |

Zalewski, A., Zalewska, H., Lunneryd, S. G., André, C., and Mijusinski, G. (2016). Reduced genetic diversity and increased structure un American mink on the Swedish Coast following invasive species control. PLoS One 11, e0157972.
Reduced genetic diversity and increased structure un American mink on the Swedish Coast following invasive species control.Crossref | GoogleScholarGoogle Scholar |