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

Abstract

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. 2 0• Seven modern genetic lineages emerged from divergence and demographic contractions.• These seven lineages warrant a revision of subspecies taxonomic nomenclature. Abstract 2 5Fragmentation 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 3 0 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 midelevation. We used a set of different genetic markers, both neutral and potentially adaptive, and either 3 5bi-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 amongpopulation genetic differentiation and low within-population genetic diversity. Contrary to these 4 0expectations, 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 4 5accepted international nomenclature made of five subspecies and name these seven lineages using regionally accepted subspecies-level names.

Portuguese Pinus nigra J.F. Arnold populations: genetic diversity, structure and relationships inferred by SSR markers

“…According to Giovannelli et al (2017), such SSR markers are highly informative and valuable for population genetic studies and can be interesting to resolve the complex taxonomy of the P. nigra. Giovannelli et al (2019) recently reported the need for revising the infraspecific taxonomy of this pine species based on the integration of molecular data with its demographic history resulting from geological events. Regarding the wide and patchy distribution of P. nigra, it was expected a strong genetic differentiation among populations and a low within-population genetic diversity (Giovannelli et al 2019;Scotti-Saintagne et al 2019).…”

“…Giovannelli et al (2019) recently reported the need for revising the infraspecific taxonomy of this pine species based on the integration of molecular data with its demographic history resulting from geological events. Regarding the wide and patchy distribution of P. nigra, it was expected a strong genetic differentiation among populations and a low within-population genetic diversity (Giovannelli et al 2019;Scotti-Saintagne et al 2019). However, these authors reported a weak genetic spatial structure probably resulting from the fragmentation of an ancestral population at the late Pleistocene or early Holocene into six to seven genetic lineages with high gene flow among them, actively contributing for admixture (Giovannelli et al 2019;Scotti-Saintagne et al 2019).…”

“…Due to their geographically fragmented distribution areas, a reduced intrapopulation genetic diversity for these P. nigra populations is expected (Scotti-Saintagne et al 2019). Nonetheless, recent molecular studies revealed a weak genetic spatial structure originated from events that occurred in the late Pleistocene or early Holocene (Giovannelli et al 2019;Scotti-Saintagne et al 2019). These events fragmented one ancestral P. nigra population into six to seven distinct genetic lineages with high gene flow among them (Giovannelli et al 2019;Scotti-Saintagne et al 2019).…”

“…Nonetheless, recent molecular studies revealed a weak genetic spatial structure originated from events that occurred in the late Pleistocene or early Holocene (Giovannelli et al 2019;Scotti-Saintagne et al 2019). These events fragmented one ancestral P. nigra population into six to seven distinct genetic lineages with high gene flow among them (Giovannelli et al 2019;Scotti-Saintagne et al 2019). The same authors proposed the revision of the infraspecific taxonomy of P. nigra species on five subspecies with Mediterranean distribution based on the length and stiffness of needles: (i) salzmannii (Dunal) Franco; (ii) nigra Arnold; (iii) dalmatica (Visiani) Franco; (iv) pallasiana (Lambert) Holmboe and (v) laricio (Poiret) Maire (Gaussen et al 1993), and a sixth subspecies, P. nigra subsp.…”

“…The wide and fragmented distribution of P. nigra, gene flow, weak spatial genetic structure and admixed origin of the populations contributed to taxonomic classification issues (Giovannelli et al 2019). Recent studies based on simple sequence repeat (SSR) markers were developed to resolve the complex taxonomy and evolutionary history of P. nigra in Europe (Giovannelli et al 2017(Giovannelli et al , 2019. These authors developed for the first time specific nSSRs to P. nigra but also revealed that nSSRs and EST-SSRs from other pine species are transferable to P. nigra.…”