Caves as species pumps: key innovations, isolation, and periodic introgression drive the world's largest cavefish radiation in a dynamic karstic landscape

Abstract

Species diversification is shaped by intricate interactions among biotic drivers, including gene flow, hybridization, and key innovations, and abiotic drivers, such as historical climate change, geological events, and ecological opportunity. However, the relative contributions of these drivers in large radiations remain poorly understood. We investigate the interplay among these factors in the diversification of Sinocyclocheilus, a cavefish radiation comprising 79 species. Sinocyclocheilus include typical surface-dwelling forms, with well-developed eyes and pigmentation, to cave-dwelling forms with regressed eyes, reduced pigmentation, and the presence of a horn and a hump. Using reduced representation genomic data (RADseq), we show extensive gene flow events across different species, with introgression playing a key role compared to incomplete lineage sorting in creating phylogenetic discordance and contributing genetic variation for cave adaptation and diversification in this group. Key traits such as eye degeneration, reduced pigmentation, and horn evolved independently multiple times, as adaptations for effectively exploiting cave environments. Furthermore, the uplift of the Tibetan plateau and the late Miocene cooling also significantly impacted speciation rates. Demographic analyses suggest population expansions during the Gonghe Movement and stability during the Last Glacial Maximum, possibly due to cave refugia. Periodic events of introgression promoted by isolation and reconnections due to the changing climate and geological activity, combined with the repeated evolution of key cave-adapted traits, are the primary drivers of this radiation. Our findings underscore the complex interplay of biotic and abiotic factors in the evolution of Sinocyclocheilus fish, offering new insights into the mechanisms of cave adaptation and diversification.