Population genetics of Mediterranean and Saharan olives: geographic patterns of differentiation and evidence for early generations of admixture

Abstract

Background and aims: The olive (Olea europaea subsp. europaea) was domesticated in the Mediterranean area but its wild relatives are distributed over three continents, from the Mediterranean basin to South Africa and south-western Asia. Recent studies suggested that this crop originated in the Levant while a secondary diversification occurred in most westward areas. A possible contribution of the Saharan subspecies (subsp. laperrinei) has been highlighted, but the data available were too limited to draw definite conclusions. Here, patterns of genetic differentiation in the Mediterranean and Saharan olives are analysed to test for recent admixture between these taxa.

Methods: Nuclear microsatellite and plastid DNA (ptDNA) data were compiled from previous studies and completed for a sample of 470 cultivars, 390 wild Mediterranean trees and 270 Saharan olives. A network was reconstructed for the ptDNA haplotypes, while a Bayesian clustering method was applied to identify the main gene pools in the data set and then simulate and test for early generations of admixture between Mediterranean and Saharan olives.

Key results: Four lineages of ptDNA haplotypes are recognized: three from the Mediterranean basin and one from the Sahara. Only one haplotype, primarily distributed in the Sahara, is shared between laperrinei and europaea. This haplotype is detected once in 'Dhokar', a cultivar from the Maghreb. Nuclear microsatellites show geographic patterns of genetic differentiation in the Mediterranean olive that reflect the primary origins of cultivars in the Levant, and indicate a high genetic differentiation between europaea and laperrinei. No first-generation hybrid between europaea and laperrinei is detected, but recent, reciprocal admixture between Mediterranean and Saharan subspecies is found in a few accessions, including 'Dhokar'.

Conclusions: This study reports for the first time admixture between Mediterranean and Saharan olives. Although its contribution remains limited, Laperrine's olive has been involved in the diversification of cultivated olives.

Keywords: Admixture; Laperrine's olive; Mediterranean basin; Olea europaea; Sahara; domestication; microsatellite; population genetic simulations; secondary diversification; wild genetic resources.

Fig. 1.

Plastid DNA haplotype networks reconstructed with the reduced-median method implemented in NETWORK (Bandelt et al., 1999). Haplotypes are represented by yellow or green circles, while the missing, intermediate nodes are indicated by small red dots. The length of branches is proportional to the number of mutation steps. (A) Network based on the whole data set. The Mediterranean lineages E1, E2 and E3 and the Saharan lineage L1 are indicated. (B) Haplotype network for the sister lineages E1 and L1. On this network, the name of each haplotype is indicated, and the circle size is relative to the number of observed occurrences for each haplotype. Haplotypes E1·1, E1·2 and E1·3 are the most frequent haplotypes in cultivars (Besnard et al., 2013a). Haplotype L1·1 (in green) is shared between Saharan and Mediterranean olives, but lineage L1 is primarily distributed in the Saharan Mountains. L1·1 was observed once in the Mediterranean basin (‘Dhokar’; Morocco–Tunisia).

Fig. 2.

Inference of population structure based on ten nuclear SSRs using model-based Bayesian clustering implemented in STRUCTURE (Pritchard et al., 2000) on the whole data set (1130 individuals). Each vertical bar represents an individual. The membership coefficient of assignment (p) of each individual to different gene pools is shown for K = 2, K = 3 and K = 4 clusters. H′ represents the similarity coefficient between ten runs for each K, and ΔK is the ad-hoc measure of Evanno et al. (2005). The graph at the bottom right gives ΔK plotted against K. The three taxa (i.e. Laperrine's olive, oleasters and cultivars) are indicated, and three pre-defined regions are recognized for both oleasters and cultivars (Supplementary Data Tables S1 and S2). ‘West Mediterranean’ corresponds to accessions from Morocco and the Iberian Peninsula, ‘Central Mediterranean’ corresponds to accessions from Algeria to Libya and France to Continental Italy, and ‘East Mediterranean’ corresponds to accessions from Croatia to the Levant. The most likely genetic structure model is K = 2 clusters, according to ΔK and H' (ΔK = 19824·9 and H' = 0·999). At K = 2, each cluster corresponds to subspecies laperrinei and europaea (L and E, respectively), whereas at K= 3, numerous western and central oleasters (that mostly belong to cluster E-I) were shown to be distinguished from cultivars and eastern oleasters (that mostly belong to cluster E-II). At K = 4, most eastern oleasters and cultivars were distinguished from western/central cultivars (clusters E-IIa vs. E-IIb, respectively).

Fig. 3.

Inference of population structure based on ten nuclear SSRs using model-based Bayesian clustering implemented in STRUCTURE (Pritchard et al., 2000) for two pairwise comparisons: (A) Laperrine's olive–oleasters (660 individuals); and (B) Laperrine's olive–cultivars (740 individuals). Each vertical bar represents an individual. The membership coefficients of assignment (p) of each individual to the different clusters averaged over ten iterations is shown for K = 2 clusters (but see Supplementary Data Fig. S3 for K = 3 or 4). H′ represents the similarity coefficient between ten runs for each K, and ΔK is the ad-hoc measure of Evanno et al. (2005). The graph on the bottom right gives ΔK plotted against K. Most accessions of subspecies laperrinei and europaea are assigned to clusters L and E, respectively. The putative admixed individuals (p >0·1) are indicated by arrows.

Fig. 4.

Comparison of membership assignments (p) to the Laperrine's olive and oleaster genetic clusters on natural populations (observations) and simulated panmictic data sets (simulations; ten iterations of 1000 genotypes). A model-based Bayesian clustering implemented in STRUCTURE (Pritchard et al., 2000) was used considering K = 2 clusters. The frequency of genotypes assigned to their respective subspecies is reported for each class of values of p in the Laperrine's olives (A) and oleasters (B). Each simulated data set is individually treated. Frequencies of assignment of genotypes to their genetic cluster for p<0·9 are given on the right for simulated and observed data sets.