Landscape dynamics and diversification of the megadiverse South American freshwater fish fauna

Significance

South America harbors the most diverse freshwater fish fauna worldwide; however, scientists have few clear answers about the origins of this megadiversity. Here, we used the most complete datasets of geographic distributions and evolutionary relationships of South American fishes to date, to track the influence of the geological history on the origins, extinctions, and interchanges of these fishes over the past 100 My. We found that abrupt increases of species origination coincided in time and place with major mountain uplift and river re-arrangement events. Species in Western Amazonia originated faster and persisted longer than those in other regions. Thus, this region acted as a source of dispersal to other regions, enhancing the exceptional diversity of fishes across the entire continent.

Abstract

Landscape dynamics are widely thought to govern the tempo and mode of continental radiations, yet the effects of river network rearrangements on dispersal and lineage diversification remain poorly understood. We integrated an unprecedented occurrence dataset of 4,967 species with a newly compiled, time-calibrated phylogeny of South American freshwater fishes—the most species-rich continental vertebrate fauna on Earth—to track the evolutionary processes associated with hydrogeographic events over 100 Ma. Net lineage diversification was heterogeneous through time, across space, and among clades. Five abrupt shifts in net diversification rates occurred during the Paleogene and Miocene (between 30 and 7 Ma) in association with major landscape evolution events. Net diversification accelerated from the Miocene to the Recent (c. 20 to 0 Ma), with Western Amazonia having the highest rates of in situ diversification, which led to it being an 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 the Early Miocene (c. 23 to 16 Ma) uplift of the Serra do Mar and Serra da Mantiqueira and the Late Miocene (c. 10 Ma) uplift of the Northern Andes and associated formation of the modern transcontinental Amazon River. The combination of high diversification rates and extensive biotic interchange associated with Western Amazonia yielded its extraordinary contemporary richness and phylogenetic endemism. Our results support the hypothesis that landscape dynamics, which shaped the history of drainage basin connections, strongly affected the assembly and diversification of basin-wide fish faunas.