Host adaptive radiation is associated with rapid virus diversification and cross-species transmission in African cichlid fishes.

ABSTRACT

Adaptive radiations are generated through a complex interplay of biotic and abiotic factors. Although adaptive radiations have been widely studied in the context of animal and plant evolution, little is known about how they impact the evolution of the viruses that infect these hosts, which in turn may provide insights into the drivers of cross-species transmission and hence disease emergence. We examined how the rapid adaptive radiation of the cichlid fishes of African Lake Tanganyika over the last 10 million years has shaped the diversity and evolution of the viruses they carry. Through metatranscriptomic analysis of 2,242 RNA sequencing libraries, we identified 121 vertebrate-associated viruses among various tissue types that fell into 13 RNA and 4 DNA virus groups. Host-switching was commonplace, particularly within the Astroviridae, Metahepadnavirus, Nackednavirus, Picornaviridae, and Hepacivirus groups, occurring more frequently than in other fish communities. A time-calibrated phylogeny revealed that hepacivirus diversification was not constant throughout the cichlid radiation but accelerated 2-3 million years ago, coinciding with a period of rapid cichlid diversification and niche packing in Lake Tanganyika, thereby providing more closely related hosts for viral infection. These data depict a dynamic virus ecosystem within the cichlids of Lake Tanganyika, characterized by rapid virus diversification and frequent host jumping, and likely reflecting their close phylogenetic relationships that lower the barriers to cross-species virus transmission.