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.

Incipient sympatric speciation in wild barley caused by geological-edaphic divergence

“…We conclude that SS, far from being a rare model of species origin, is a common model, since "ECs" in sharply ecologically divergent microsites, abound on our planet caused by geologic, edaphic, climatic, biotic, and abiotic contrasts. Such microsites represent evolution in action across life, where both adaptive evolution and incipient or full SS abound, actively generating continuously new species evolving from primary SS as shown in the present study at EP, and dramatically in the evolution of three species of wild emmer wheat at EC I (Wang et al, 2020). The vision of Darwin in 1859 has been substantiated in microsites where sharp ecological divergence in free breeding populations with gene flow (Brown et al, 1978) and two contrasting ecologies occur.…”

“…These results suggest that the two populations unfold primary SS with gene flow, and reject the secondary contact hypothesis from allopatry ( Fig 4A , model 1). This is also the case in EC I in the dramatic SS of three species of wild emmer wheat the progenitor of bread wheat ( Wang et al, 2020 ), and other species that speciated sympatrically from bacteria to mammals ( Nevo, 2014 ). The best fitting model, suggesting primary in situ SS , gene flow, and divergence time, were estimated and shown in Fig 4B .…”

“…In 2003, we embarked upon a microsite divergent edaphically, dubbed “EP,” deeply studied for SS in the blind mole rat, S. galili ( Hadid et al, 2013 ; Li et al, 2015 , 2016b , Lövy et al, 2015 , 2017 ), and the current study on wild barley, H. spontaneum , the progenitor of cultivated barley, which originated a new species of WB on the basalt, adapted to a siliceous world of volcanic basalt, derived from the calcareous chalk progenitor. In a parallel article, we described how wild barley initiated formation of a new species of wild barley at EC I, together with other six species from bacteria to mammals ( Nevo, 2014 ; Qian et al, 2018 ; Wang et al, 2020 ).…”

Toward the Genetic Basis and Multiple QTLs of Kernel Hardness in Wheat

“…More importantly, these SNP arrays increase the number of SNPs available for QTL mapping from several thousand to tens or hundreds of thousand at affordable costs, allowing the accurate mapping of minor QTLs [146][147][148]. Third, as the complements to array-based genotyping, datasets of wheat whole-genome resequencing [149][150][151], representative sequencing (such as GBS) [131,132] and exome sequencing [152,153] have been recently published, enriching the repertoire of wheat genomic resources. These new resources are powerful not only for association mapping but also for identifying potential functional changes in genes and regions subjected to domestication and/or selection.…”

Limited divergent adaptation despite a substantial environmental cline in wild pea

“…In the case of wild wheat (Triticum dicoccoides), which inhabits diverse environments in Israel, physiological adaptation and genetic variation is eco-geographically structured (e.g., Peleg et al, 2005Peleg et al, , 2008). Indeed, a recent claim was made for cryptic speciation processes across very short distances supposedly driven by contrasting habitat ecologies (Wang et al, 2020). Likewise, the phenology and population structure of Levantine wild barley were strongly correlated with environmental predictors despite high rates of gene flow among populations from different habitats (Hübner et al, 2009(Hübner et al, , 2012(Hübner et al, , 2013.…”