Convergent life-history evolution in Hordeum: Phylogenomic insights into climatic niche variation and functional genetic differentiation among annual and perennial wild relatives of barley

Abstract

Annual and perennial life-history strategies have evolved repeatedly across angiosperms, yet the genomic and environmental underpinnings of these transitions remain poorly understood, particularly in grasses. We generated de novo transcriptomes from 82 accessions representing 22 Hordeum species, including barley, and identified 257 single-copy orthologs present in all accessions to infer a robust phylogeny of the genus. By combining phylogenetic network inference with ABBA-BABA tests, we detected four cases of interspecific hybridization, three coinciding with major long-distance dispersal events across continents. Comparative climatic niche analysis indicated annual Hordeum species inhabit environments with higher temperatures, greater interannual variability, and increased human disturbance, compared to perennials, although no consistent precipitation differences were observed. Using our phylogeny as a framework, we analyzed selection and gene expression to uncover genomic changes associated with life-history strategy while accounting for phylogenetic non-independence. Additionally, we analysed gene copy number variations associated with life-history strategy. These analyses yielded 174 candidate genes across diverse biological functions, suggesting the genetic architecture underlying life-history evolution is more complex than assumed. Candidate genes grouped into six major functional categories, the most prominent being signal transduction and development, including regulators of flowering, dormancy, and meristem activity, metabolic and biosynthetic processes related to carbon allocation and storage, and stress response and defense, reflecting the resilience of perennials compared to the accelerated growth strategies of annuals. Our study reconstructs the evolutionary history and climatic niche differentiation of Hordeum species and demonstrates that convergent life-history evolution is driven by multifaceted, functionally diverse genetic mechanisms.