Landscape dynamics promoted the evolution of mega-diversity in South American freshwater fishes

Landscape dynamics and river network rearrangements are widely thought to shape the diversity of Neotropical freshwater fishes, the most species-rich continental vertebrate fauna on Earth. Yet the effects of hydrogeographic changes on fish dispersal and diversification remain poorly understood. Here we integrate an unprecedented occurrence dataset of 4,967 South American freshwater fish species with a species-dense phylogeny to track the evolutionary processes associated with hydrogeographic events over 100 Ma. Net lineage diversification was heterogeneous through time, across space, and among clades. Three abrupt shifts in diversification rates occurred during the Paleogene (between 63 and 23 Ma) in association with major landscape evolution events, and net diversification accelerated from the Miocene to the Recent (c. 20 - 0 Ma). The Western Amazon exhibited the highest rates of in situ diversification and was also the most important source of species dispersing to other regions. All regional biotic interchanges were associated with documented hydrogeographic events and the formation of biogeographic corridors, including Early Miocene (c. 20 Ma) uplift of the Serra do Mar, and Late Miocene (c. 10 Ma) uplift of the Northern Andes and formation of the modern transcontinental Amazon River. Reciprocal mass dispersal of fishes between the Western and Eastern Amazon coincided with this phase of Andean uplift. The Western Amazon has the highest contemporary levels of species richness and phylogenetic endemism. Our results support the hypothesis that landscape dynamics were constrained by the history of drainage basin connections, strongly affecting the assembly and diversification of basin-wide fish faunas. Significance StatementDespite progress in mapping geographic distributions and genealogical relationships, scientists have few clear answers about the origins of South American freshwater fishes, the most diverse vertebrate fauna on Earth. Here we used the most complete dataset of geographic distributions and evolutionary relationships of South American fishes to track how the geological history of river dynamics influenced the origin, extinction, and interchange of species over the past 100 Ma. We found abrupt increases of species origination between 66 and 23 Ma, coinciding with repeated uplifts of the Andes. The Western Amazon region served as source of freshwater fishes to other regions, as a place where species tended to persist over longer historical periods, and where species originations occurred with higher frequency.