The genetic structure of the European black pine (Pinus nigraArnold) is shaped by its recent Holocene demographic history

Fragmentation acting over geological times confers wide, biogeographical scale, 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 major European forest tree and to resolve its demographic history, we describe and model its spatial genetic structure and gene genealogy. We then test which Pleistocene event, whether recent or ancient, could explain its widespread but patchy geographic distribution using population genetic data, environmental data and realistic demographic timed scenarios. The taxon of interest is a conifer forest tree, Pinus nigra (Arnold), the European black pine, whose populations are located in the mountains of southern Europe and North Africa, most frequently at mid-elevation. We used a set of different genetic markers, both neutral and potentially adaptive, and either bi-parentally or paternally inherited, and we sampled natural populations across the entire range of the species. We analysed the data using frequentist population genetic methods as well as Bayesian inference methods to calibrate realistic, demographic timed scenarios. Species with geographically fragmented distribution areas are expected to display strong 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 are best explained as resulting from late Pleistocene or early Holocene fragmentation of one ancestral population into seven genetic lineages, which we found to be the main biogeographical contributors of the natural black pine forests of today. 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 subspecies and name these seven lineages using regionally accepted subspecies-level names. Highlights The European black pine, Pinus nigra (Arnold), has a weak spatial genetic structure. Gene flow among populations is frequent and populations are often of admixed origin. Current genealogies result from recent, late Pleistocene or Holocene events. Seven modern genetic lineages emerged from divergence and demographic contractions. These seven lineages warrant a revision of subspecies taxonomic nomenclature.