Phylogeomics Reveals Ancestral Introgression and Paleogeoclimate Co‐Facilitated Speciation and Diversification of Chinese Endemic Cavefishes

Abstract

ABSTRACT Recent genomic studies have suggested that ancient introgression may facilitate rapid diversification. 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 compelling potential example of rapid speciation during the evolution of karst landscapes. Here, we investigated the complex evolutionary history of the TCG by sampling 24 species and analysing whole‐genome resequencing data. We reconstructed the phylogeny using different methods and quantified introgression to infer speciation and dispersal processes, which collectively confirm extensive historical gene flow both between TCG and Claea , as well as among TCG species. Our study demonstrated that, against the backdrop of widespread phylogenetic discordance within the TCG, interspecific introgression has played a more significant role than incomplete lineage sorting. Genomic regions with the highest levels of introgression (top 1% of f dM values) are enriched for Gene Ontology terms related to circadian behaviour, phenotypic plasticity, lipid metabolism, oxygen transport and reproduction. Demographic simulations further suggest that geoclimatic factors, together with the unique genetic attributes of the group, likely promoted founder effects, inbreeding, and subsequent declines in effective population size, resulting in two distinct demographic trajectories. Additionally, our results indicate that the origin and speciation of the TCG were closely synchronised with the rapid uplift of the Qinghai–Tibet Plateau and associated climatic transitions. We further identify three distinct stages of lineage diversification, characterised by alternating accelerations and declines driven by tectonic–climate interactions that were synchronised with major Asian orogenic events and monsoon cycles.