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 disease emergence. We examined how the rapid adaptive radiation of the African cichlid fishes of Lake Tanganyika over the last 10 million years has shaped the diversity and evolution of the viruses they carry. Through metatranscriptomic analysis 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 evolution 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 show that African cichlids contain a complex interacting pool of virus diversity, likely reflecting their close genetic relationships that reduces the barriers to cross-species virus transmission.

Limited transmission of microbial species among coral reef fishes from the Great Barrier Reef, Australia

“…These findings offer further support for recent studies of virus ecology in fish that show that host phylogeny has a strong influence on virome composition (16, 33). For example, closely related African cichlid species, that have evolved in situ within Lake Tanganyika over the last 10 million years, exhibit highly similar viromes with high levels of cross-species transmission and viral generalism (33).…”

“…These findings offer further support for recent studies of virus ecology in fish that show that host phylogeny has a strong influence on virome composition (16, 33). For example, closely related African cichlid species, that have evolved in situ within Lake Tanganyika over the last 10 million years, exhibit highly similar viromes with high levels of cross-species transmission and viral generalism (33). African cichlids are members of a single family, the Cichlidae, and exhibit some of the lowest pairwise genetic distances observed between vertebrates (e.g., differences of 0.03% between some species).…”

“…Both letoviruses ( Coronaviridae , subfamily Letovirinae ) —Chromis atripectoralis letovirus and Scarus psittacus letovirus—from Lizard Island formed a basal clade with Microhyla letovirus and three other viruses identified in African cichlids (32, 33). Together, this group likely formed a novel genus within the Letovirinae that includes diverse ectothermic hosts such as amphibians, jawless and ray-finned fishes (32).…”

“…Notably, we identified a novel chapparvovirus in Cryptocentrus strigilliceps that was related to tilapia parvovirus—a pathogen in farmed Tilapia in China—making it the second fish virus identified in this group (34). Among the genus Ichthamaparovirus , both pleurosicya icthamaparvovirus (Lizard Island) and Luposicya lupus ichthamaparvovirus (Orpheus Island) shared a common ancestor (57.9% NSI similarity) and formed a distinct clade with other fish-infecting parvoviruses (16, 33, 35).…”

“…In marked contrast, the adaptive radiation of the African cichlids would have provided a more favourable environment for cross-species transmission as their diversification occurred rapidly within the confinements of Lake Tanganyika, generating a large pool of closely related host species for infection. Indeed, a time-calibrated phylogeny of cichlid hepaciviruses showed that elevated rates of virus diversification coincided with a period of rapid cichlid speciation (33).…”