Characterising the genomic landscape of differentiation between annual and perennial rye

Abstract

Annuality and perenniality represent two different life-history strategies in plants, and an analysis of genomic differentiation between closely related species of different life histories bears the potential to identify the underlying targets of selection. Additionally, understanding the interactions between patterns of recombination and signatures of natural selection is a central aim in evolutionary biology, because patterns of recombination shape the evolution of genomes by affecting the efficacy of selection. Here, our aim was to characterise the landscape of genomic differentiation between weedy annual rye (Secale cereale L.) and wild perennial rye (Secale strictum C. Presl), and explore the extent to which signatures of selection are influenced by recombination rate variation. We used population-level sequence data of annual and perennial rye to analyse population structure and their demographic history. Based on our analyses, annual and perennial rye diverged approximately 26,500 years ago (ya) from an ancestral population size of ~85,000 individuals. We analysed patterns of genetic diversity and genetic differentiation, and found highly differentiated regions located in low-recombination regions, indicative of linked selection. Although all highly differentiated regions, as revealed by FST-outlier scans, were located in low-recombining regions, not all chromosomes showed this tendency. We therefore performed a gene ontology enrichment analysis, which showed that highly differentiated regions comprise genes involved in photosynthesis. This enrichment was confirmed when FST outlier scans were performed separately in low- and intermediate-recombining regions, but not in high-recombining regions, suggesting that local recombination rate variation in rye affects outlier scans. Cultivated rye is an annual crop, but the introduction of perenniality may be advantageous in regions with poor soil quality or under low-input farming. Although the resolution of our analysis is limited to a broad-scale, knowledge about the evolutionary divergence between annual and perennial rye might support breeding efforts towards perennial rye cultivation.