Sympatric speciation of wild emmer wheat driven by ecology and chromosomal rearrangements

Abstract

In plants, the mechanism for ecological sympatric speciation (SS) is little known. Here, after ruling out the possibility of secondary contact, we show that wild emmer wheat, at the microclimatically divergent microsite of "Evolution Canyon" (EC), Mt. Carmel, Israel, underwent triple SS. Initially, it split following a bottleneck of an ancestral population, and further diversified to three isolated populations driven by disruptive ecological selection. Remarkably, two postzygotically isolated populations (SFS1 and SFS2) sympatrically branched within an area less than 30 m at the tropical hot and dry savannoid south-facing slope (SFS). A series of homozygous chromosomal rearrangements in the SFS1 population caused hybrid sterility with the SFS2 population. We demonstrate that these two populations developed divergent adaptive mechanisms against severe abiotic stresses on the tropical SFS. The SFS2 population evolved very early flowering, while the SFS1 population alternatively evolved a direct tolerance to irradiance by improved ROS scavenging activity that potentially accounts for its evolutionary fate with unstable chromosome status. Moreover, a third prezygotically isolated sympatric population adapted on the abutting temperate, humid, cool, and forested north-facing slope (NFS), separated by 250 m from the SFS wild emmer wheat populations. The NFS population evolved multiple resistant loci to fungal diseases, including powdery mildew and stripe rust. Our study illustrates how plants sympatrically adapt and speciate under disruptive ecological selection of abiotic and biotic stresses.

Keywords: Robertsonian translocation; abiotic stress; biotic stress; sympatric speciation; wild emmer wheat.

Fig. 1.

Population history of wild emmer accessions in EC-I. (A) The geographic distribution of the emmer wheat accessions used in this study. The green circles represent the collection location outside EC-I. The red circle represents the location of EC-I. The arrows represent the collection stations on each slope. (B) Phylogenetic tree of 168 wild emmer wheat accessions by neighbor-joining method with 1,000 bootstraps. The arabic notation following the collection location in Israel is shown in the map. (C) Inferred historical population sizes by pairwise sequential Markovian coalescent (PSMC) analysis. Three typical samples from each population were shown. The lower x axis gives time measured by pairwise sequence divergence, and the y axis gives the effective population size measured by the scaled mutation rate. (D) Distribution of Ks values for 12,352 one-to-one orthologous gene sets between each population. The full-length transcripts from one representative sample from each population (SFS1-7, SFS2-14, and NFS-8) was employed for Ks evaluation.

Fig. 2.

Genetic differentiation of wild emmer populations in EC-I. (A) Genetic differentiation revealed by Fst across genome window between each population. (B) Progeny ratio of F₁ hybrids between accessions of SFS1 population and the other two populations. A 100% ratio of progeny was supposed as the seed setting rate of three progeny seeds per spikelet, and more than 10 spikes per sample were employed for seed setting rate calculation.

Fig. 3.

Chromosome rearrangements in SFS1 population. (A) The representative for three typical Robertsonian translocations by FISH. (B) The pattern genome rearrangements for different individuals in SFS1 population. The paring and division events during meiosis of F₁ are shown in the table as percentages. (C) The representative of paring and division events during meiosis of F₁. The abnormal paring or division is shown by arrows.

Fig. 4.

Distinct adaptation mechanisms of wild emmer populations in EC-I. (A) Representative photograph of phenotypic variance of accessions from each population. (B) The distribution of the XP-CLR score along 14 chromosomes with 20-Kb sliding window. The genome-wide threshold was defined both by the top 5% and 1%, as marked in black dotted lines. (C) GO terms enriched by candidate regions selected in the SFS1 population. The top 20 terms with the most significant enrichment are shown. The GO items involved with antioxidant pathway are noted with asterisk. (D) Phenotype of transgenic wheat overexpressing TaPRX1 under irradiance condition. The seedlings were subjected to high radiation with 30,000 Lux light for 1 wk and then photographed.

Fig. 5.

Sympatric ecological speciation model of wild emmer wheat at EC-I. The blue dotted line indicates the extent of genetic drift. The red full lines indicate postzygotic reproductive isolation, and the red dotted line indicates prezygotic reproductive isolation. The yellow five-pointed stars indicate powdery mildew-resistant genes evolved, and the orange one indicates strip rust-resistant gene.