Genomic insights into stepwise selection reshaping fruit traits and male-biased selection driving hermaphroditism in papayas.

Papaya (Carica papaya) is a promising model system for genetic and genomic studies of fruit traits and sex determination in tropical trees and fruits. However, the genomic basis of the artificial selection for key fruit traits and commercially crucial hermaphroditism remains poorly understood. In this study, we assembled the genomes for two phenotypically divergent hermaphroditic cultivars, including their haplotype-phased sex-determining regions (SDRs). Population genomic analyses of wild, common-type (for vegetable use), and fruit-type (for fresh consumption) papayas revealed a clear domestication history and geographic spread model. By combining genome-wide association study (GWAS), selection scan, and functional validation, we revealed a stepwise selection targeting CpPUP11 and CpICMT during domestication and improvement to reshape fruit size, and artificial selection on CpMAPK1, CpCOX, CpCIN, and CpUBE3 during the improvement process to increase fruit sweetness and vitamin C content. Furthermore, we demonstrated the independent origins of two hermaphroditic lineages through polyphyletic selection from wild male populations, resulting in two distinct hermaphrodite-specific Yh regions (HSY1 and HSY3). This transition was driven by selection targeting male-biased genes, which exhibited stable dominance in their methylation and transcription. Notably, we identified a hermaphrodite-specific, selectively fixed 13-bp insertion in the male-biased gene CpPGLP1A (HSY3-TR-13bp), which is strongly associated with the male-to-hermaphrodite transition. Collectively, our study provides novel insights into the genomic architecture of papaya domestication, revealing a trajectory of stepwise selection reshaping fruit traits and male-biased selection driving the emergence of a novel hermaphroditic sexual system.