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Genetic footprints of a rapid and large-scale range expansion: the case of cyclic common vole in Spain

Heredity volume 130, pages 381–393 (2023)Cite this article

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Abstract

In the Anthropocene, many species are rapidly shifting their ranges in response to human-driven habitat modifications. Studying patterns and genetic signatures of range shifts helps to understand how species cope with environmental disturbances and predict future shifts in the face of global environmental change. We investigated the genetic signature of a contemporary wide-range expansion observed in the Iberian common vole Microtus arvalis asturianus shortly after a colonization event. We used mtDNA and microsatellite data to investigate patterns of genetic diversity, structure, demography, and gene flow across 57 localities covering the historical range of the species and the newly colonized area. The results showed a genetic footprint more compatible with a true range expansion (i.e. the colonization of previously unoccupied areas), than with a model of “colonization from within” (i.e. local expansions from small, unnoticed populations). Genetic diversity measures indicated that the source population was likely located at the NE of the historical range, with a declining gradient of genetic diversity towards the more recently invaded areas. At the expansion front, we observed the greatest gene flow and smallest pairwise differences between nearby localities. Both natural landscape features (rivers) and recent anthropogenic barriers (roads, railways) explained a large proportion of genetic variance among populations and had a significant impact on the colonization pathways used by voles.

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Fig. 1: Sampling sites and main rivers in the study area.
Fig. 2: Genetic clusters and migration networks.
Fig. 3: Haplotype network, patterns of spatial genetic differentiation and demographic changes over time.
Fig. 4: Map showing the spatial distribution of genetic diversity parameters based on STR and mtDNA markers.

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Acknowledgements

We are very grateful to students and friends for their help during the fieldwork, with special thanks to Iván García, Xurxo Piñeiro, Fernando Arce, Julián Núñez, and Vega Santos. Thanks to lab technicians, specially to María Santoro. Samples from Campo Azálvaro were kindly provided by Juan Antonio Fargallo (MNCN, CSIC), who also provided insightful comments on the manuscript. Thanks are also due to GREFA for the support and cooperation the landowners who allowed us access to their properties, and the communities and mayors from the villages of Villalar de Los Comuneros, Boada de Campos, San Martín de Valderaduey and Fuentes de Nava. This work was supported by I + D National Plan Projects of the Spanish Ministry of Economy, Industry and Competitiveness (CGL2011-30274, CGL2015-71255-P, CGL2013-42451-P) co-funded by the European Regional Development Fund (FEDER, EU), and the Fundación BBVA Research Project TOPIGEPLA (2014 call). J Martínez-Padilla was funded by ARAID foundation and currently by Science and Education Ministry (PID2019-104835GB-100). Julio Domínguez was supported by a predoctoral grant: “Programa Talento Formación” funded by Fondo Social Europeo (FSE) and Castilla La Mancha regional government (JCCM) (ref: SBPLY/16/180501/000205). Julio Domínguez was also supported by Margarita Salas fellowship funded by NextGenerationEU, Ministry of Universities and Recovery, Transformation and ResiliencePlan, through a call from Castilla-La Mancha University. We thank three anonymous reviewers for their constructive feedback.

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Authors and Affiliations

  1. IREC, Instituto de Investigación en Recursos Cinegéticos (CSIC-UCLM-JCCM), Ronda de Toledo 12, 13071, Ciudad Real, Spain

    Julio C. Domínguez, María Calero-Riestra, Javier Viñuela & Jesús T. García

  2. IPE, Pyrenean Institute of Ecology (CSIC), 22700, Avda. Nuestra Señora de la Victoria 16, Jaca, Spain

    Julio C. Domínguez, María Calero-Riestra & Jesús Martínez-Padilla

  3. Department of Biology, Geology and Environmental Science, University of Tennessee at Chattanooga, Chattanooga, TN, USA

    Fernando Alda

  4. Terrestrial Ecology Group (TEG)-Departamento de Ecología, and Centro de Investigación en Biodiversidad y Cambio Global, Universidad Autónoma de Madrid, c/ Darwin, 2, 28049, Madrid, Spain

    Pedro P. Olea, Jesús Herranz, Juan José Oñate & Ana Santamaría

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  1. Julio C. Domínguez
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Contributions

JTG, JCD, JVM, PPO, JMP, JJO and JH conceived the study. All authors collected samples. JCD and MCR performed the lab work. JCD, MCR and JTG analysed the genetic data. JCD and JTG led the writing and the rest of authors contributed to edit and review the manuscript.

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Correspondence to Julio C. Domínguez.

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Genetic footprints of a rapid and large-scale range expansion: the case of cyclic common vole in Spain. Supplemental Material

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Domínguez, J.C., Alda, F., Calero-Riestra, M. et al. Genetic footprints of a rapid and large-scale range expansion: the case of cyclic common vole in Spain. Heredity 130, 381–393 (2023). https://doi.org/10.1038/s41437-023-00613-w

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