The occurrence of parallel speciation strongly implies the action of natural selection. However, it is unclear how general a phenomena parallel speciation is since it was only shown in a small number of animal species. In particular, the adaptive process and mechanisms underlying the process of parallel speciation remain elusive. Here, we used an integrative approach incorporating population genomics, common garden, and crossing experiments to investigate parallel speciation of the wild rice species Oryza nivara from O. rufipogon . We demonstrated that O. nivara originated multiple times from different O. rufipogon populations and revealed that different O. nivara populations have evolved similar phenotypes under divergent selection, a reflection of recurrent local adaptation of ancient O. rufipogon populations to dry habitats. Almost completed premating isolation was detected between O. nivara and O. rufipogon in the absence of any postmating barriers between and within these species. These results suggest that flowering time is a “magic” trait that contributes to both local adaptation and reproductive isolation in the origin of wild rice species. Our study thus demonstrates a convincing case of parallel ecological speciation as a consequence of adaptation to new environments.
Ecological speciation is a common mechanism by which new species arise. Despite great efforts, the role of gene expression in ecological divergence and speciation is poorly understood. Here, we conducted a genome-wide gene expression investigation of two Oryza species that are evolutionarily young and distinct in ecology and morphology. Using digital gene expression technology and the paired-end RNA sequencing method, we obtained 21,415 expressed genes across three reproduction-related tissues. Of them, approximately 8% (1,717) differed significantly in expression levels between the two species and these differentially expressed genes are randomly distributed across the genome. Moreover, 62% (1,064) of the differentially expressed genes exhibited a signature of directional selection in at least one species. Importantly, the genes with differential expression between species evolved more rapidly at the 5' flanking sequences than the genes without differential expression relative to coding sequences, suggesting that cis-regulatory changes are likely adaptive and play an important role in the ecological divergence of the two species. Finally, we showed evidence of significant differentiation between species in phenotype traits and observed that genes with differential expression were overrepresented with functional terms involving phenotypic and ecological differentiation between the two species, including reproduction- and stress-related characteristics. Our findings demonstrate that ecological speciation is associated with widespread and adaptive alterations in genome-wide gene expression and provide new insights into the importance of regulatory evolution in ecological speciation in plants.
It is of critical importance for our understanding of speciation process to determine the forms of reproductive isolation and their relative importance in species divergence. Oryza nivara and O. rufipogon are direct ancestors of Asian cultivated rice and a progenitor-daughter species pair. Investigating the reproductive isolation between them provides insights into plant speciation and helps understanding of the rice domestication. Here, we quantitatively measured the major components of reproductive isolation between the two species based on common garden and crossing experiments for three pairs of sympatric populations in Nepal, Cambodia and Laos.We revealed significant differences in the flowering times between species pairs, with O. nivara flowering much earlier than O. rufipogon. A very weak reduction in seed set but no reduction in F1 viability and fertility were detected for the crosses between species relative to those within species. Moreover, we detected asymmetrical compatibility between species and found that emasculation significantly decreased pollination success in O. nivara but not in O. rufipogon. Our study demonstrates that the divergence between O. nivara and O. rufipogon is maintained almost entirely by the difference in flowering times and suggests that differential flowering times contribute to both habitat preferences and reproductive isolation between species.
Phytoliths, as one of the important sources of microfossils, have been widely used in paleobotanyrelated studies, especially in the grass family (Poaceae) where abundant phytoliths are found. Despite great efforts, several challenges remain when phytoliths are used in various studies, including the accurate description of phytolith morphology and the effective utilization of phytolith traits in taxon identification or discrimination. In this study, we analyzed over 1000 phytolith samples from 18 taxa representing seven main genera in the tribe Oryzeae (subfamily Ehrhartoideae) and five taxa in the subfamilies Bambusoideae and Pooideae. By focusing on Oryzeae, which has been extensively investigated in terms of taxonomy and phylogeny, we were able to evaluate the discrimination power of phytoliths at lower taxonomic levels in grasses. With the help of morphometric analysis and by introducing several machine learning algorithms, we found that 87.7% of the phytolith samples could be classified correctly at the genus level. In spite of slightly different performances, all four machine learning algorithms significantly increased the resolving power of phytolith evidence in taxon identification and discrimination compared with the traditional phytolith analysis. Therefore, we propose a pipeline of phytolith analyses based on machine learning algorithms, including data collection, morphometric analysis, model building, and taxon discrimination. The methodology and pipeline presented here should be applied to various studies across different groups of plants. This study provides new insights into the utilization of phytoliths in evolutionary and ecology studies involving grasses and plants in general.
No abstract
Miscanthus species have received considerable attention as a potential biomass source for renewable energy production because of their ability to produce high yields of biomass and adapt to a wide range of climates and soils. To explore the genetic diversity and phylogenetic relationship of Miscanthus species in China, we used 24 simple sequence repeat markers to genotype 100 natural populations representing all four Chinese Miscanthus species (M. sinensis Andersson, M. floridulus (Lab.) Warb. ex K. Schum. & Lauterb., M. sacchariflorus (Maxim.) Hack., and M. lutarioriparius L. Liu ex Renvoize & S. L. Chen). Based on phylogenetic, principal coordinate, and STRUCTURE analyses, we found that the 100 populations formed two major groups corresponding to sect. Triarrhena and sect. Miscanthus. Group 1 (i.e., sect. Triarrhena) was further subdivided into two subgroups corresponding to M. sacchariflorus and M. lutarioriparius; Group 2 (i.e., sect. Miscanthus) was subdivided into three subgroups, group 2a (M. sinensis populations in southern China), group 2b (M. sinensis populations in northern China), and group 2c (all the M. floridulus populations). Population genetics analyses indicated high levels of the genetic diversity at both population (H E = 0.468-0.599) and species (H E = 0.559-0.708) levels, indicative of the potential of these wild resources in future breeding programs. The species distribution modeling showed that M. sacchariflorus and M. lutarioriparius have experienced population reductions during the last glacial maximum and population expansion afterward; in contrast, M. sinensis and M. floridulus both underwent gradual population expansions from the last interglaciation to the present. We also suggest that M. floridulus originated from M. sinensis in southeast China through ecological speciation. The understanding of the evolutionary history and population dynamics of these species not only provides valuable information for further genetic improvement and breeding of this energy crop but also gives important insights into the origin and speciation processes of the Miscanthus species.
Parallel domestication has been widely acknowledged but its genetic basis remains largely unclear. As an important rice ecotype, upland rice was assumedly domesticated multiple times in two rice subspecies (Indica and Japonica) and provides a feasible system to explore the genetic basis of parallel domestication. To uncover the genome‐wide pattern of genetic differentiation between upland and lowland rice and explore the parallelism of genetic changes during upland rice domestication, we obtained whole‐genome sequences of 95 rice landraces and yielded genome‐wide expression data for five tissues of representative accessions of upland and lowland rice. Our phylogenetic analyses confirmed multiple domestications of the upland ecotype in two rice subspecies. Genomic scans based on resequencing data identified substantial differentiation between the upland and lowland ecotypes with 11.4% and 14.8% of the genome diverged between the two ecotypes in Indica and Japonica, respectively. Further genome‐wide gene expression analyses found that 30% of effectively expressed genes were significantly differentiated between two ecotypes, indicating the importance of regulation changes in the domestication of upland rice. Importantly, we found that only 1.8% of differentiated genomes and 1.6% of differentially expressed genes were shared by upland Indica and upland Japonica, suggestive of largely unparallel genetic alterations during upland rice domestication. These findings not only provide new insights into the genetic basis of parallel domestication at the genome scale but could also facilitate genetic improvement and breeding of rice and crops in general.
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