Physiology mediates transcontinental radiations of freshwater fishes

Abstract

Adaptive radiations are clades that have rapidly accumulated exceptional species richness and ecological diversity. The ability to access sources of ecological opportunity, such as new habitats, is thought to be essential for their success. Transcontinental lineages of exclusively freshwater fishes, such as the 1,700 species of cichlids distributed across Central and South America, Africa, India, and Madagascar, are some of the most celebrated adaptive radiations. Yet, what features facilitated their dispersal across marine barriers and diversification in geologically young freshwater ecosystems remain debated. Here, we show that a common mechanism, saltwater tolerance, provides an explanation for how species-rich transcontinental freshwater fish radiations, including cichlids, killifishes, pupfishes, and livebearers, accessed ecological opportunity and subsequently diversified. Marine salinity tolerance was retained after cichlids, killifishes and their relatives emerged from a rapid radiation during the Cretaceous-Paleogene boundary. The retention of this ancestral physiological trait throughout the last 45 million years of Earth history repeatedly enabled cichlids and other fishes to disperse across marine barriers and radiate in freshwater ecosystems on multiple continents, including geologically young features in Africa and North America that have repeatedly experienced saline conditions over tens of thousands of years of global climate change. These results show how the larger evolutionary context of adaptive radiations can sculpt their responses to ecological opportunity.