Contrasting genomic routes to domestication in Occidental and Oriental pears

Abstract

The domestication of perennial fruit trees remains poorly understood compared with annual crops, which were shaped by strong bottlenecks and elevated genetic load. Pears (Pyrus spp.) provide an ideal model for exploring how long-lived, outcrossing crops evolved under human selection. Here, we combined high-coverage whole-genome resequencing of 396 wild and cultivated accessions from Occidental and Oriental pears with analyses of nucleotide and transposable element (TE) polymorphisms to reconstruct the demographic and adaptive history of pear domestication. Demographic inferences revealed weak or no domestication bottlenecks and extensive gene flow between wild and cultivated populations. In the Occidental lineage, dessert and perry P. communis cultivars underwent independent domestications from the same wild progenitor, P. pyraster, with divergent selection linked to fruit use. In the Oriental lineage, regionally independent domestications gave rise to Chinese and Japanese P. pyrifolia cultivars, shaped by both environmental adaptation and human selection. Selection scans identified lineage- and use-specific targets related to fruit texture, metabolism, and immunity. Contrary to the classical "cost of domestication" hypothesis, cultivated pears carried fewer deleterious variants than their wild relatives, suggesting efficient purging through selection and introgression. TE insertions mirrored population structure and occasionally occurred near selected genes, indicating a limited but detectable adaptive role. Together, our findings go beyond confirming the dual origins of Pyrus domestication to reveal contrasting demographic and adaptive pathways in Occidental and Oriental pears, illustrating independent adaptive trajectories in perennial crops, where long lifespan, self-incompatibility, and recurrent introgression shape distinctive genomic outcomes.