Genomic evidence for recurrent genetic admixture during the domestication of Mediterranean olive trees (Olea europaea L.)

Abstract

Background: Olive tree (Olea europaea L. subsp. europaea, Oleaceae) has been the most emblematic perennial crop for Mediterranean countries since its domestication around 6000 years ago in the Levant. Two taxonomic varieties are currently recognized: cultivated (var. europaea) and wild (var. sylvestris) trees. However, it remains unclear whether olive cultivars derive from a single initial domestication event followed by secondary diversification, or whether cultivated lineages are the result of more than a single, independent primary domestication event. To shed light into the recent evolution and domestication of the olive tree, here we analyze a group of newly sequenced and available genomes using a phylogenomics and population genomics framework.

Results: We improved the assembly and annotation of the reference genome, newly sequenced the genomes of twelve individuals: ten var. europaea, one var. sylvestris, and one outgroup taxon (subsp. cuspidata)-and assembled a dataset comprising whole genome data from 46 var. europaea and 10 var. sylvestris. Phylogenomic and population structure analyses support a continuous process of olive tree domestication, involving a major domestication event, followed by recurrent independent genetic admixture events with wild populations across the Mediterranean Basin. Cultivated olives exhibit only slightly lower levels of genetic diversity than wild forms, which can be partially explained by the occurrence of a mild population bottleneck 3000-14,000 years ago during the primary domestication period, followed by recurrent introgression from wild populations. Genes associated with stress response and developmental processes were positively selected in cultivars, but we did not find evidence that genes involved in fruit size or oil content were under positive selection. This suggests that complex selective processes other than directional selection of a few genes are in place.

Conclusions: Altogether, our results suggest that a primary domestication area in the eastern Mediterranean basin was followed by numerous secondary events across most countries of southern Europe and northern Africa, often involving genetic admixture with genetically rich wild populations, particularly from the western Mediterranean Basin.

Keywords: Admixture; Domestication; Genome; Introgression; Olive.

Fig. 1

SNP density (SNPs/kb) in sequenced individuals. a Homozygous versus heterozygous SNPs for each accession, relative to the cv. Farga reference. Dot size correlates with the total amount of SNPs. All the cultivars are marked in green and var. sylvestris in blue. b SNP densities for the plastid and mitochondrial genomes. c Plot showing the relative position and identity of plastid SNPs compared to the cv. Farga (reference genome). Bars on the bottom show the main plastid haplotypes of the individuals as described by Besnard et al. [17, 44]

Fig. 2

Maximum likelihood species tree derived from the nuclear SNPs data. a Nuclear phylogeny. Cultivated olives are shown in green and wild olives in blue. The geographical location of the accession and the plastid haplotype are indicated. Only bootstrap values below 100% are shown. b Bayesian clustering for the nuclear SNP data estimated in Structure v2.3. Structure bar plot shows the genetic clusters differentiated by color. c Heatmap showing the D-statistic and its p value. Red color indicates higher D-statistics, and more saturated colors indicate greater significance

Fig. 3

Maximum likelihood species tree derived from the organellar SNPs data. a Plastid phylogeny. Cultivated olives are shown in green and wild olives in blue. The geographical location of the accession and the plastid haplotype are indicated. Only bootstrap values below 100% are shown. b Mitochondrial phylogeny. The colors and characteristics are the same as in a

Fig. 4

SplitsTree derived from nuclear SNPs. All the cultivars are marked in green and var. sylvestris in blue. The neighbor net method is used here to explore data conflict and not to estimate phylogeny

Fig. 5

SMC++ results for inferring population size histories in cultivated olives. A generation time of 20 years was used to convert coalescent scaling to calendar time