Abstract
Multipartite viruses replicate through a puzzling evolutionary strategy. Their genome is segmented into two or more parts, and encapsidated in separate particles that appear to propagate independently. Completing the replication cycle, however, requires the full genome, so that a systemic infection of a host requires the concurrent presence of several particles. This represents an apparent evolutionary drawback of multipartitism, while its advantages remain unclear. A transition from monopartite to multipartite viral forms has been described in vitro under conditions of high multiplicity of infection, suggesting that cooperation between defective mutants is a plausible evolutionary pathway towards multipartitism. However, it is unknown how the putative advantages that multipartitism might enjoy at the microscopic level affect its epidemiology, or if an explicit advantange is needed to explain its ecological persistence. In order to disentangle which mechanisms might contribute to the rise and fixation of multipartitism, we here investigate the interaction between viral spreading dynamics and host population structure. We set up a compartmental model of the spread of a virus in its different forms and explore its epidemiology using both analytical and numerical techniques. We uncover that the impact of host contact structure on spreading dynamics entails a rich phenomenology of ecological relationships that includes cooperation, competition, and commensality. Furthermore, we find out that multipartitism might rise to fixation even in the absence of explicit microscopic advantages. Multipartitism allows the virus to colonize environments that could not be invaded by the monopartite form, while homogeneous contacts between hosts facilitate its spread. We conjecture that these features might have led to an increase in the diversity and prevalence of multipartite viral forms concomitantly with the expansion of agricultural practices.
Highlights
Viruses transport their genetic material inside a protein shell, the capsid, surrounded in some species by a lipid membrane
Using the analytical characterization of the endemic phases and the numerical study of the equilibria, we can investigate under which conditions the interplay between spreading dynamics and topology of contacts leads to the rise and persistence of multipartitism
We have developed a framework that, starting from few key biological features, models the interaction between monopartite and multipartite forms, driven by the spreading dynamics on a host population
Summary
Viruses transport their genetic material inside a protein shell, the capsid, surrounded in some species by a lipid membrane. Each viral particle contains all the genetic material needed to carry out replication inside a host cell, and generate a progeny of viral particles. A prominent exception to this behavior is found in multipartite viruses. These viruses, first described in the 1960s [1], have a genome segmented in two or more parts. The main puzzle regarding multipartite viruses is how the simultaneous presence of multiple segments, which imposes severe constraints on the number of viral particles that have to reach a susceptible host, is balanced by other adaptive advantages of multipartitism, whether microscopic or ecological [5, 6]
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