Directional water transport system resolves fertilization-dispersal conflicts in Marchantia

Complex traits allow organisms to occupy new ecological niches by integrating multiple functions, but the evolutionary forces and mechanisms underlying their assembly remain poorly understood. Here, in the liverwort Marchantia polymorpha, we identify a directional water transport system on the female reproductive structure, the archegoniophore, that enables efficient sperm delivery to elevated archegonia and thereby ensures water-mediated fertilization on water-depriving land. This system relies on the precise spatial coordination of multiple surface structures, whose development is controlled by a single GRAS transcription factor, the MpLAS, through regulation of cell-growth-coupled cell division. We further show that formation of the archegoniophore stalk, which elevates archegonia and the resulting sporophytes to facilitate spore dispersal under desiccating conditions, involves MpGRAS10 by regulating the biosynthetic pathway of gibberellin-related compounds. Ancestral state reconstructions indicate a stepwise evolutionary assembly, with the fertilization-enhancing trait emerging after dispersal-facilitating stalk emergence, suggesting that later innovations may have arisen to enhance earlier ones by resolving their functional limitations. Together, these findings indicate that functional demand conflicts can actively shape evolutionary trajectories and contribute to the emergence of complex, integrated traits.