Phylogeomics reveals ancestral introgression and paleogeoclimate co-facilitated speciation and radiation of Chinese endemic cavefishes

Recent genomic analyses have suggested that ancient introgression may facilitate rapid diversification and adaptive radiation. The cave-dwelling group (TCG) of Triplophysa sensu lato, cave fishes endemic to the karst regions of southwestern China, exhibits high diversity and rapid evolution, representing a potential example of adaptive radiation during the evolution of karst landscapes. Herein, we investigated the complex evolutionary history of the TCG by sampling 24 species and analyzing whole-genome resequencing data. We reconstructed the phylogeny of the TCG using different methods and quantified introgression to infer speciation and dispersal processes, confirming that there have been extensive gene flow events among TCG species. Our study demonstrated that, against the backdrop of phylogenetic discordance in the TCG, interspecific introgression has played a more significant role than incomplete lineage sorting. These highly introgressed regions (top 1% of fdm values) are enriched for Gene Ontology terms closely related to circadian behavior, phenotypic remodeling, lipid metabolism, oxygen transport, and reproduction. Simulation analyses suggested that geoclimatic together with the unique genetic characteristics of the group may have led to founder effects, inbreeding, and subsequent declines in effective population size, resulting in two distinct demographic trajectories. The results also indicated that the origin and radiation of the TCG were closely synchronized with the rapid uplift of the Qinghai-Tibet Plateau and the associated climate transitions. We also delineated three distinct stages of lineage diversification, characterized by alternating acceleration and decline driven by tectonic–climate interactions that were synchronized with the Asian orogeny and monsoon cycles.