Whole-genome resequencing unveils the phylogeographic coevolution of Oncomelania hupensis with Yangtze River dynamics in China

The freshwater snail Oncomelania hupensis is the only intermediate host of Schistosoma japonicum and is currently mainly distributed in the middle and lower reaches of the Yangtze River in China. To explore the evolutionary history and adaptations of O. hupensis, we re-sequenced 283O. hupensis accessions from 30 geographic locations across the middle and lower Yangtze River. Our study raises and proves an intriguing hypothesis: O. hupensis has its distribution and adaptation closely tied to the geological evolution of the Yangtze River. Despite varying degrees of isolation and differentiation, lake-type snail populations in the middle and lower reaches may migrate westward to eastward (from middle to lower reaches) via water flow, while hill ecotype snails in the middle reaches potentially disperse from hilly region to lake areas. Population genetics and evolutionary analyses revealed that O. hupensis exhibits a gradual dispersal history from hilly region to downstream areas, closely mirroring the Yangtze River's flow and geological evolution. Compared to hill ecotype populations, lake populations displayed higher genetic diversity, consistent with dynamic habitats and increased gene flow. This west-to-east migration pattern may be driven by the Yangtze River's geological dynamics and associated climatic-ecological shifts. Notably, we found genes under strong positive selection differed between lake and hill ecotype populations. Our study provides comprehensive insights into the population dynamics and genetic architecture of O. hupensis, underscoring its coevolution with the Yangtze River's geological history. These findings advance the genetic understanding of O. hupensis adaptation to different ecological environments and inform schistosomiasis control strategies.