Paternity tests support a diallelic self-incompatibility system in a wild olive (Olea europaea subsp. laperrinei, Oleaceae)

Abstract

Self-incompatibility (SI) is the main mechanism that favors outcrossing in plants. By limiting compatible matings, SI interferes in fruit production and breeding of new cultivars. In the Oleeae tribe (Oleaceae), an unusual diallelic SI system (DSI) has been proposed for three distantly related species including the olive (Olea europaea), but empirical evidence has remained controversial for this latter. The olive domestication is a complex process with multiple origins. As a consequence, the mixing of S-alleles from two distinct taxa, the possible artificial selection of self-compatible mutants and the large phenological variation of blooming may constitute obstacles for deciphering SI in olive. Here, we investigate cross-genotype compatibilities in the Saharan wild olive (O. e. subsp. laperrinei). As this taxon was geographically isolated for thousands of years, SI should not be affected by human selection. A population of 37 mature individuals maintained in a collection was investigated. Several embryos per mother were genotyped with microsatellites in order to identify compatible fathers that contributed to fertilization. While the pollination was limited by distance inside the collection, our results strongly support the DSI hypothesis, and all individuals were assigned to two incompatibility groups (G1 and G2). No self-fertilization was observed in our conditions. In contrast, crosses between full or half siblings were frequent (ca. 45%), which is likely due to a nonrandom assortment of related trees in the collection. Finally, implications of our results for orchard management and the conservation of olive genetic resources are discussed.

Keywords: Olea europaea L.; Oleaceae; diallelic self‐incompatibility system; microsatellites; paternity.

Figure 1

Level of relatedness between the mother and the father of the 454 analyzed progenies of Laperrine's olive (excluding the nonfertilized embryo). The relatedness was deduced from available knowledge on the parents of the Laperrine's olive trees of the CEFE collection (Table S1; Data S1B). 1 = crosses between full siblings; 2 = crosses between half siblings; 3 = crosses between individuals from the same population but not sharing a parent; 4 = crosses between individuals from distinct populations. Our observations were compared to expected levels of relatedness between compatible parents considering no limitation of pollination by distance and equal contribution of each parent. An excess of crosses between related individuals was observed, probably due to the nonrandom disposition of trees in the collection (i.e., individuals originating from the same population placed on the same lane; Table S1) and variable parental contribution of trees (Table S7)

Figure 2

Position of individuals in the experimental plot (see Table S1 and Figure S4) according to their mating group: group A in blue and group B in green. These two groups were defined on the first axis of the correspondence analysis (Table S3). Diameters of blue circles are proportional to coordinates along the second correspondence analysis axis, while for green circles their size is related to third axis coordinate (see Figure S3). For a given group, circle size similarity between individuals thus represents some similarity in mating pattern. For both groups, distribution of size similarity is not randomly distributed in the plot suggesting strong pollination limitation by distance (see also Figure 3)

Figure 3

Limitation by distance of the efficient pollination in the Laperrine's olive. Comparison between observed distances of pollination and expected distances considering random crosses between compatible individuals. The expected mean distribution of distances was estimated from the random sampling of 444 embryos, with 1,000 independent iterations