Plastid and nuclear DNA polymorphism reveals historical processes of isolation and reticulation in the olive tree complex (Olea europaea)

Abstract

Aim The olive tree is considered one of the best indicators of the Mediterranean climate. The species' distribution is associated with geographical and bioclimatic factors, as well as being influenced by a long period of cultivation. Despite concerted efforts of different research groups, the origin of the Mediterranean olive tree still remains elusive. In the present study, relationships between taxa and populations covering the entire range of Olea europaea were investigated using both maternal (plastid genome) and biparental (nuclear genome) markers to disclose evolutionary patterns in the olive complex. Phylogenetic and phylogeographical results of the two-genome analyses were interpreted in a biogeographical context.Location Mediterranean, temperate and subtropical floristic regions of the Old World.Methods Phylogeographical reconstructions of plastid DNA polymorphism were performed using microsatellites, restriction sites and indels on a wide sample of 185 representative trees across the Old World, including 28 herbarium specimens from remote areas. Additionally, the potential utility of one ITS-1 pseudogene for phylogenetic analyses was explored using Bayesian and maximum parsimony approaches on a subsample of 38 olive trees.Results Forty plastid haplotypes were recognized and split into two lineages and seven sublineages. The analysis of ITS-1 sequences also allowed the identification of seven well differentiated groups. Distribution of plastid and ribosomal DNA lineages was congruent, but particular cases of phylogenetic incongruence were disclosed (particularly in the Sahara and Madeira). Lastly, two divergent ITS-1 copies were isolated from the same sample of four individuals of different subspecies.Main conclusions Phylogenetic congruence of both ITS-1 and plastid lineages suggested an evolutionary scenario of predominant isolation during the PlioPleistocene in Macaronesia, the Mediterranean, southern Africa, eastern Africa and Asia. The Saharan desert appeared to have played an important role of vicariant barrier between southern and northern African populations in early times. Incongruence of some plastid and nuclear results, as well as intermingled ITS-1 copies of different lineages in single individuals, was interpreted as a result of recurrent reticulation events in the olive complex. We identified an ancient hybrid zone from the Sahara to north-eastern African mountains, where divergent plastid and nuclear lineages still co-exist. Results of this paper, and previous studies, suggest that the cultivated olive originated from a pre-Quaternary Mediterranean ancestor, with no evidence for a recent hybrid origin. In contrast, a continuous process of olive domestication through local hybridization events of cultivated trees with natural populations may have brought about a remarkably high genomic diversity among cultivated trees across the Mediterranean.

The complex history of the olive tree: from Late Quaternary diversification of Mediterranean lineages to primary domestication in the northern Levant

“…The high diversity of lineage E1 in the eastern Mediterranean basin (see the electronic supplementary material, figure S4) suggests that this lineage originated in this area [10]. This result thus disagrees with previous statements about an impoverished ptDNA diversity in the Near East [10,11].…”

“…DNA was extracted as previously described [10]. Owing to the highly fragmented and human-disturbed Mediterranean habitat, oleaster populations were usually collected from present orchards, but we cannot exclude that some trees/populations were feral (i.e.…”

“…Microsatellite data from lineages E1, E2, E3 and A were analysed with DIYABC [21], which implements an approximate Bayesian computation (ABC) method of inference in population genetics. Lineages E1, E2 and E3 were treated as populations to force the coalescence of individuals within the three separate lineages (as defined by SNPs and indels that were not used for this analysis) [10,16]. The demographic model (see the electronic supplementary material, figure S1) thus consisted of four populations (E1, E2, E3 and A).…”

“…Although early exploitation and use of wild olive trees (namely oleasters) has been documented since the Neolithic from the Near East to Spain [2,6], it is usually accepted that the domestication of the olive tree-characterized by vegetative propagation of the best cultivated genotypes that may have preceded orchard establishmentbegan in the Near East approximately 6000 years ago [2,4]. Several genetic studies have, however, supported multiple origins of cultivars across the Mediterranean area [7][8][9][10][11][12], but it remains unclear whether this reflects secondary diversification or multiple independent primary events. Also, a centre of domestication for the olive tree in the Near East was questioned because the eastern Mediterranean oleaster populations have low genetic diversity compared with those of the western area [10][11][12][13].…”

On the origin of the invasive olives (Olea europaea L., Oleaceae)

“…Besnard et al (2007) have recently reconstructed a detailed phylogeography of the O. europaea complex in its native range based on DNA polymorphism from the nuclear (bi-parentally inherited) and plastid (maternally inherited) genomes. This study provided powerful data to test the origins of naturalized olive populations.…”