Cross-species hybridization and the origin of North African date palms

Abstract

Date palm (Phoenix dactylifera L.) is a major fruit crop of arid regions that were domesticated ∼7,000 y ago in the Near or Middle East. This species is cultivated widely in the Middle East and North Africa, and previous population genetic studies have shown genetic differentiation between these regions. We investigated the evolutionary history of P. dactylifera and its wild relatives by resequencing the genomes of date palm varieties and five of its closest relatives. Our results indicate that the North African population has mixed ancestry with components from Middle Eastern P. dactylifera and Phoenix theophrasti, a wild relative endemic to the Eastern Mediterranean. Introgressive hybridization is supported by tests of admixture, reduced subdivision between North African date palm and P. theophrasti, sharing of haplotypes in introgressed regions, and a population model that incorporates gene flow between these populations. Analysis of ancestry proportions indicates that as much as 18% of the genome of North African varieties can be traced to P. theophrasti and a large percentage of loci in this population are segregating for single-nucleotide polymorphisms (SNPs) that are fixed in P. theophrasti and absent from date palm in the Middle East. We present a survey of Phoenix remains in the archaeobotanical record which supports a late arrival of date palm to North Africa. Our results suggest that hybridization with P. theophrasti was of central importance in the diversification history of the cultivated date palm.

Keywords: archaeobotany; crop wild relative; domestication; introgression; range expansion.

Fig. 1.

The geographic distribution and phylogeny of cultivated date palm (P. dactylifera) and its wild relatives. (A) Approximate geographic distribution of Phoenix species included in this study (27). (B) Maximum-likelihood phylogeny of Phoenix species based on a subset of SNPs from whole-genome sequencing data. Support values are the percentage of RAxML bootstrap replicates that support each node. The tree is midpoint rooted.

Fig. 2.

North African date palm has mixed ancestry from Middle Eastern date palm and a wild relative, P. theophrasti. Shown is a STRUCTURE (29) diagram for K = 2 to K = 4 using the independent allele-frequency model.

Fig. 3.

Admixture between North African date palm and P. theophrasti. (A) D statistics $\pm$ SE. (B) $f_3$ statistics $\pm$ SE. (C and D) Maximum-likelihood tree based on TreeMix with block size of 3,000 SNPs for (C) zero (m = 0) and (D) one migration (m = 1) event. These models explain 98.6% and 99.9% of the variance in relatedness among populations. The migration edge pointing from P. theophrasti to North African date palm has a mixture weight of 15.7%. Abbreviations: Af, North Africa; can, P. canariensis; ME, Middle East; rec, P. reclinata; syl, P. sylvestris; and the, P. theophrasti.

Fig. 4.

Introgressed regions in North African date palm. (A) The introgression fraction (f_d) in 5-kb nonoverlapping windows from the 30 longest scaffolds in the draft assembly. (B) Population genetic summary statistics of North African date palm for scaffold NW_008246512.1 in 5-kb windows. B, Bottom shows the frequency of P. theophrasti-like alleles (main text) segregating in North Africa. Each circle represents a SNP. Curves were fitted to the data using local polynomial regression (LOESS). (C) Neighbor-joining 50% majority rule tree based on phased haplotypes in a 5-kb interval at position 1,100 kb of the scaffold in B. Colored circles represent the population origin of phased sequences. The single haplotype from the Middle East in the P. theophrasti/North Africa clade bearing the shared haplotype is from a Pakistani variety (Aseel) with a mixed Middle Eastern/North African ancestry (7). Single haplotypes from each of two probable hybrids (a P. theophrasti sample from Almyros, Crete and a P. sylvestris sample from Faisalabad, Pakistan) are nested within P. dactylifera clades as are haplotypes from two P. atlantica samples.

Fig. 5.

Patterns of genetic diversity in North African and Middle Eastern date palm populations. (A) Boxplot distributions of F_st based on 5-kb nonoverlapping intervals between pairs of populations (M.E., Middle East; N.A., North Africa; the, P. theophrasti). (B) Distribution of nucleotide diversity in Middle Eastern and North African date palm populations. (C) Decay of LD calculated separately for each population. Symbols on decay curves represent the half-decay distance at 20.5 kb and 30.8 kb for Middle Eastern and North African populations.