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Recent, Late Pleistocene fragmentation shaped the phylogeographic structure of the European black pine (Pinus nigra Arnold)

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Abstract

Fragmentation acting over geological times confers wide, biogeographical scale and genetic diversity patterns to species, through demographic and natural selection processes. To test the effects of historical fragmentation on the genetic diversity and differentiation of a widespread forest tree, Pinus nigra Arnold, the European black pine, and to resolve its demographic history, we described and modelled its spatial genetic structure and gene genealogy. We then tested which Pleistocene event, whether recent or ancient, could explain its widespread but patchy geographic distribution. We used a set of different genetic markers, both neutral and potentially adaptive, and either bi-parentally or paternally only inherited, and we sampled natural populations across the entire species range. We analysed the data using both frequentist population genetic and Bayesian inference methods to calibrate realistic, demographic timed scenarios. We also considered how habitat suitability might have affected demography by correlating climate variables at different recent Pleistocene ages with genetic diversity estimates. Species with geographically fragmented distribution areas are expected to display significant among-population genetic differentiation and low within-population genetic diversity. Contrary to these expectations, we show that the current diversity of Pinus nigra and its weak genetic spatial structure result from the Late Pleistocene or Early Holocene fragmentation of one ancestral population into six distinct genetic lineages. Gene flow among the different lineages is strong across forests and many current populations are admixed between lineages. We propose to modify the currently accepted international nomenclature made of five sub-species and name these six lineages using regionally accepted sub-species-level names.

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Acknowledgements

We thank O. Gilg, F. Rei, N. Turion and D. Vauthier (INRA UEFM, Avignon, France), J. Rousselet (INRA Orléans, France), S.C. Gonzalez-Martinez (INRA Bordeaux, France), E. Kakouris (Cyprus Forest Department, Nicosia, Cyprus), F. Krouchi (University of Tizi Ouzou, Algeria), G. Huber (Bavarian Office for Forest Seeding and Planting, Teisendorf, Germany), Carmen García-Barriga (National Institute for Agronomy, Madrid, Spain) and H. Sbay (Forest Research Centre, Rabat, Morocco) for the sample collection. Collection of material was made before the Nagoya Protocol on Access to Genetic Resources and the Fair and Equitable Sharing of Benefits Arising from their Utilization to the Convention on Biological Diversity was legally implemented by signatory countries.

Data archiving statement

Raw DNA sequence and genotyping data are to be archived in the Open Access archive Zenodo (https://zenodo.org/).

Funding

This study was made possible by the financial support of the French Forest Service (Office National des Forêts) and the project “Programme global de conservation des populations françaises de pin de Salzmann”. We also acknowledge the support for Sanger DNA sequencing from the French “Bibliothèque du Vivant” project and for SSR genotyping from the French Ministry of Agriculture—Irstea project 2015-339 “Déterminants de la vulnérabilité du pin laricio à la maladie des bandes rouges”. G. Giovannelli was financially supported by Aix-Marseille Université (Ecole Doctorale ED251), France, and the short-term scientific mission programme of the COST Action FP1202, while working on her PhD.

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Correspondence to Bruno Fady.

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Communicated by Z. Kaya

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Scotti-Saintagne, C., Giovannelli, G., Scotti, I. et al. Recent, Late Pleistocene fragmentation shaped the phylogeographic structure of the European black pine (Pinus nigra Arnold). Tree Genetics & Genomes 15, 76 (2019). https://doi.org/10.1007/s11295-019-1381-2

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  • DOI: https://doi.org/10.1007/s11295-019-1381-2

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