Xiaotong Wang, Chunhui Li, Peidong Xin, Meiwei Zhang, Baoyu Huang, T. Chen, Siyi Li, Yijing Han, Lei Wei, Xuekai Zhang, Yaqiong Liu, Chenglong Zhu, Wenjie Xu, Zhiyong Yue, Wenshi Xue, Wenchao Yu, Peng Zhang, Lin Li, Mengqiang Yuan, Deyang Tian, Jiyan Qi, Qiang Qiu, Kun Wang, Ximing Guo, Chenguang Feng
Abstract Gastropod diversification represents one of the most spectacular evolutionary radiations, underpinned by a fundamentally asymmetric body plan and diverse pigmentation patterns. To understand the genetic underpinnings of these cardinal traits, we constructed a chromosome-level genome assembly for the rainbow abalone, Haliotis iris . Integrating systematic genomics, histoembryology, and molecular assays, we uncover an ancient regulatory axis, conserved for over 544 million years, in which the long non-coding RNA lncRNA1 functions as a competing endogenous RNA to shield pitx transcripts from miRNA-mediated degradation, thereby driving the establishment of asymmetric body patterning, including the mantle. Furthermore, we identify a wnt-mitf-tyr cascade as the driver of melanogenesis and demonstrate that the mantle is the primary site of melanin synthesis. Concurrently, we reveal the mantle as a multifunctional organ possessing mechanosensory capabilities. These findings elucidate the ancient genetic toolkit governing trait evolution in gastropods. Teaser A deeply conserved RNA switch directs gastropod body plans and reveals the mantle’s hidden talents.