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Contrasting levels of hybridization across the two contact zones between two hedgehog species revealed by genome-wide SNP data

Heredity volume 129, pages 305–315 (2022)Cite this article

Subjects

Abstract

Hybridization and introgression have played important roles in the history of various species, including lineage diversification and the evolution of adaptive traits. Hybridization can accelerate the development of reproductive isolation between diverging species, and thus valuable insight into the evolution of reproductive barrier formation may be gained by studying secondary contact zones. Hedgehogs of the genus Erinaceus, which are insectivores sensitive to changes in climate, are a pioneer model in Pleistocene phylogeography. The present study provides the first genome-wide SNP data regarding the Erinaceus hedgehogs species complex, offering a unique comparison of two secondary contact zones between Erinaceus europaeus and E. roumanicus. Results confirmed diversification of the genus during the Pleistocene period, and detected a new refugial lineage of E. roumanicus outside the Mediterranean basin, most likely in the Ponto-Caspian region. In the Central European zone, the level of hybridization was low, whereas in the Russian-Baltic zone, both species hybridise extensively. Asymmetrical gene flow from E. europaeus to E. roumanicus suggests that reproductive isolation varies according to the direction of the crosses in the hybrid zones. However, no loci with significantly different patterns of introgression were detected. Markedly different pre- and post-zygotic barriers, and thus diverse modes of species boundary maintenance in the two contact zones, likely exist. This pattern is probably a consequence of the different age and thus of the different stage of evolution of reproductive isolating mechanisms in each hybrid zone.

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Fig. 1: Species ranges and localities of the 70 samples used in the present study.
Fig. 2: The estimated phylogeny of the genus Erinaceus, Atelerix and Hemiechinus inferred with MrBayes (Ronquist and Huelsenbeck 2003).
Fig. 3: Clustering analysis produced in Admixture (Alexander et al. 2009) for the highest supported number of clusters (six), represented by different colours, and ordered according to lineage/species membership.
Fig. 4: Principal component analysis (PCA) plot representing genetic variation of hedgehog populations.

Data availability

The data that supports findings of this study are publically available in Dryad under reference: 10.5061/dryad.2547d7wnt. Scripts used to process genomic data, produced plots and graphs are publicly available on GitHub: https://github.com/eliasok/hedgehog_RAD and https://github.com/IgnasiLucas/hedgehog.

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Acknowledgements

We thank Lukáš Choleva and Bianka Baying for assisting us with the preparation of the Illumina libraries, and Jindřich Brejcha for creating the sampling map. For language proofreading, we thank Science Unleashed. The project was funded by the Grant Agency of Charles University in Prague, project no. 538218 (KE, ML, BČB), Czech University of Life Sciences CIGA 20185006 (BČB) and IGA 20223108 (BČB), Spanish Ministry of Economy and Competitivity RYC-2012-11872 (JILL) and Russian Foundation for Basic Research N20-04-00081a (AB, KZ).

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  1. These authors contributed equally: Pavel Hulva, Barbora Černá Bolfíková

Authors and Affiliations

  1. Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic

    Kristýna Eliášová, Miroslava Loudová & Pavel Hulva

  2. Department of Animal Science and Food Processing, Faculty of Tropical AgriSciences, Czech University of Life Sciences Prague, Prague, Czech Republic

    Kristýna Eliášová & Barbora Černá Bolfíková

  3. Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Valencia, Spain

    J. Ignacio Lucas Lledó

  4. Evolutionary Adaptive Genomics, University of Potsdam, Potsdam, Germany

    José Horacio Grau

  5. Center for Species Survival, Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC, USA

    José Horacio Grau

  6. Lomonosov Moscow State University, Moscow, Russia

    Anna A. Bannikova & Katerina I. Zolotareva

  7. EMBL, Genomics Core Facility, Heidelberg, Germany

    Vladimír Beneš

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Contributions

BČB and PH conceived the study; BČB, PH, KE and JILL designed the study; ML, PH and KE performed the laboratory work; KE, JILL, JHG and BČB analysed the data; BČB, KE, PH, JILL, ML, VB, AB, KZ contributed to samples/reagents/materials; KE, BČB and PH drafted the manuscript, and all authors contributed to the final version.

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Correspondence to Kristýna Eliášová.

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Eliášová, K., Lucas Lledó, J.I., Grau, J.H. et al. Contrasting levels of hybridization across the two contact zones between two hedgehog species revealed by genome-wide SNP data. Heredity 129, 305–315 (2022). https://doi.org/10.1038/s41437-022-00567-5

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