Genetic architecture of ecological divergence between Oryza rufipogon and Oryza nivara

Abstract

Ecological divergence due to habitat difference plays a prominent role in the formation of new species, but the genetic architecture during ecological speciation and the mechanism underlying phenotypic divergence remain less understood. Two wild ancestors of rice (Oryza rufipogon and Oryza nivara) are a progenitor‐derivative species pair with ecological divergence and provide a unique system for studying ecological adaptation/speciation. Here, we constructed a high‐resolution linkage map and conducted a quantitative trait locus (QTL) analysis of 19 phenotypic traits using an F2 population generated from a cross between the two Oryza species. We identified 113 QTLs associated with interspecific divergence of 16 quantitative traits, with effect sizes ranging from 1.61% to 34.1% in terms of the percentage of variation explained (PVE). The distribution of effect sizes of QTLs followed a negative exponential, suggesting that a few genes of large effect and many genes of small effect were responsible for the phenotypic divergence. We observed 18 clusters of QTLs (QTL hotspots) on 11 chromosomes, significantly more than that expected by chance, demonstrating the importance of coinheritance of loci/genes in ecological adaptation/speciation. Analysis of effect direction and v‐test statistics revealed that interspecific differentiation of most traits was driven by divergent natural selection, supporting the argument that ecological adaptation/speciation would proceed rapidly under coordinated selection on multiple traits. Our findings provide new insights into the understanding of genetic architecture of ecological adaptation and speciation in plants and help effective manipulation of specific genes or gene cluster in rice breeding.

Phenological and morphological variations of Oryza rufipogon and O. nivara in Sri Lanka and their evolutionary implications

“…For instance, predominantly vegetative propagation, longer and more spreading culms make O. rufipogon better adapt to permanently inundated habitats; whereas being annual, shorter and less decumbent culms of O. nivara are more suitable for seasonally dry habitats (Banaticla-Hilario et al 2013a;Cai et al 2019;Sandamal et al 2021). Congruent with ecological speciation (Cai et al 2019;Meng et al 2024;Sandamal et al 2018;Zheng and Ge 2010), the differences in morphological traits between O. rufipogon and O. nivara are mainly explained by distinct habitats they grow and have important implications for their ecological adaptation and evolutionary dynamics.…”

“…We assessed ten individuals for in situ observation and fifteen individuals in common garden experiment. Three randomly selected tillers per plant were measured following the descriptors for wild and cultivated rice (Biodiversity International 2007;Cai et al 2019;Meng et al 2024).…”

“…To investigate the morphological variation, we measured nine traits for five O. rufipogon and seven O. nivara populations (Fig. 1) using three randomly selected tillers per plant following the descriptors for wild and cultivated rice (Biodiversity International 2007;Meng et al 2024).…”

“…Moreover, as an accurate indicator of the completion of speciation and a mechanism for maintaining species identity (Abbott 2017;Nosil 2012;Schluter and Rieseberg 2022), flowering time difference was considered to be a major driver of reproductive isolation and thus species divergence between O. rufipogon and O. nivara (Barbier 1989;Cai et al 2019;Xu et al 2020). Although the flowering time of the wild rice species has been amply documented in literatures (e.g., Barbier 1989;Banaticla-Hilario et al 2013a;Cai et al 2004;Cai et al 2019;Eizenga et al 2022;Grillo et al 2009;Meng et al 2024;Oka 1988;Vicentini et al 2023), it is still less clear about their variation pattern and plasticity across populations because, to our knowledge, no research on flowering phenology of any Oryza species has been undertaken based on in situ observation for its entire life cycle. Also, few comparative studies of morphological variation have been made on the two wild rice species in terms of ecological adaptation and divergence.…”