Elise N. Paietta, Rachel A. Johnston, Santatra Randrianarisoa, Camille DeSisto, Simona Kraberger, Darren Martin, Tahina T. Razanamahenina, Antsa Ramboninarimalala, Jean-Baptiste Velontsara, Toussaint G. Raherinirina, Victor Rasendrinirina, Laurent Raveloson, Yanting Luo, Nina Finley, Eric Baitchman, Anne D. Yoder, Arvind Varsani
Anelloviruses are circular, negative-sense single-stranded DNA viruses that have remarkable diversity and ubiquity across mammals. However, few studies have attempted to determine anellovirus diversity and dynamics across a biodiverse landscape. Madagascar offers a unique opportunity to study anellovirus diversity, with speciose, endemic mammalian lineages that have evolved in geographic isolation for millions of years. These endemic animals frequently interact with more recently introduced populations of non-native small mammals. From oral swab samples taken from natural populations of lemurs, rodents and shrews in the Manombo Special Reserve and surrounding area in southeastern Madagascar, we determined the complete genomes of anelloviruses from black rats ( n =647 genomes), Webb’s tufted-tailed rats ( n =2), mouse lemurs ( n =4), a woolly lemur ( n =1) and a house shrew ( n =3). We observed distinct anellovirus lineages in the endemic lemurs and tufted-tailed rats, which we infer to be the result of their long-term geographic isolation in Madagascar. Lemur-infecting anelloviruses, in particular, do not cluster with other primate-infecting anelloviruses. In contrast, anellovirus diversity in widespread, non-native rodents (i.e. black rats) was similar to that of closely related, globally dispersed rodent species, concordant with their later introduction to Madagascar. With our large anellovirus dataset from black rats, we examined anellovirus alpha- and beta-diversity and viral co-occurrence networks. Black rat anellovirus populations showed high intra-individual variation, but the overall pool of circulating anelloviruses was consistent across age classes and sexes. Adult relative to juvenile/subadult black rats harboured richer anellovirus populations and were more connected within the co-occurrence network. Proximity between individuals and greater intra-individual viral diversity were also linked to more virus-sharing between black rats.