Phylogenetic evidence reveals the classification and evolutionary history of endemic cavefish in China

The phylogeny, classification, diversity, and distribution of cave species have always been difficult problems for taxonomists. In this study, we aim to clarify the phylogeny and evolutionary history of the cave-dwelling fish genus Sinocyclocheilus, a group that is not only difficult to collect but is also frequently under-recognized due to its cryptic nature, in order to elucidate its evolutionary patterns and dynamics. Our phylogeny supports the monophyly of the five current species groups (S. angularis, S. cyphotergous, S. jii, S. microphthalmus, and S. tingi groups), but a variety of evidence suggests that corresponding subgenera should be elevated. Our species delimitation analysis identified 84 species, including 18 cryptic. Molecular dating and biogeographic analyses revealed that Sinocyclocheilus originated in the late Eocene, ~ 40.32 millions of years ago (Ma), that the most recent common ancestor inhabited the Guijiang-Hejiang River and the Nanpanjiang River, ~ 34.61 Ma, and dispersed outward from the Nanpanjiang River Basin, and that an acceleration of speciation rates occurred during the late Eocene. A biogeographic dynamic meta-analysis showed that lineage divergence and in situ diversification began at ~ 38 Ma and increased sharply at ~ 24 Ma, with two peaks at ~ 15 and ~ 2.5 Ma and a valley at 2.5 Ma. Dispersal events began at ~ 28 Ma and increased sharply at ~ 12 Ma, with a distinct peak at ~ 5 Ma. The speciation rate increased rapidly between approximately 40 and 32 Ma, followed by a sustained, gradual decline. The diversity of Sinocyclocheilus has been severely underestimated and requires a comprehensive reassessment integrating both morphological and genetic evidence. The revised classification comprises seven species groups or subgenera. The origin and diversification history of the genus were likely coupled with orogenic activities and the intensification of the Asian monsoon rainfall, which facilitated the formation of extensive subterranean voids, thereby creating ecological opportunities for speciation. Early high-temperature events may have initially triggered a rapid increase in speciation rates, whereas the relatively stable and cooler conditions of cave environments likely became less conducive to subsequent speciation. Our results also suggest a four-phase model of karst cave formation in southwestern China, with accelerating and decelerating periods in each phase. These evolutionary dynamics can be viewed as a response to shifts in paleogeoclimatic events since the Eocene.