Cheating leads to the evolution of multipartite viruses

Abstract

In multipartite viruses, the genome is split into multiple segments, each of which is transmitted via a separate capsid. The existence of multipartite viruses poses a problem, because replication is only possible when all segments are present within the same host. Given this clear cost, why is multipartitism so common in viruses? Most previous hypotheses try to explain how multipartitism could provide an advantage. In so doing, they require scenarios that are unrealistic and that cannot explain viruses with more than 2 multipartite segments. We show theoretically that selection for cheats, which avoid producing a shared gene product, but still benefit from gene products produced by other genomes, can drive the evolution of both multipartite and segmented viruses. We find that multipartitism can evolve via cheating under realistic conditions and does not require unreasonably high coinfection rates or any group-level benefit. Furthermore, the cheating hypothesis is consistent with empirical patterns of cheating and multipartitism across viruses. More broadly, our results show how evolutionary conflict can drive new patterns of genome organisation in viruses and elsewhere.

Robust Approaches to the Quantitative Analysis of Genome Formula Variation in Multipartite and Segmented Viruses

“…In the past decade, there has been considerable interest in the genome formula of both multipartite and segmented viruses [ 1 , 2 , 8 , 13 , 14 , 25 , 36 , 38 ]. However, different studies have applied different analysis methods, many of which have serious shortcomings.…”

Open questions in the social lives of viruses

“…Cheating can even drive the evolution of new forms of genome organization, that in turn allow new mechanisms of evolvability or genetic plasticity. For example, the sequential invasion of cheats can drive the evolution of segmented and multipartite viral genomes, resulting in a viral population where the genome is split across multiple physically distinct segments (Leeks et al, 2023; Nee, 1987). This new type of genome organization then allows new mechanisms of genetic exchange, such as reassortment between distinct genome segments (Simon‐Loriere & Holmes, 2011), as well as phenotypically plastic ways of responding to environmental change, via expressing genome segments at different levels across different hosts (Gallet et al, 2022; Zwart & Elena, 2020).…”

“…At the other end of the scale, does the presence of selfish genetic elements, such as homing endonucleases in T4 phages, generate sufficient conflict to undermine individual viral genomes themselves as cohesive evolutionary units (Edgell et al, 2010;Gardner & Úbeda, 2017;Patten et al, 2023)? Finally, how do concepts of evolutionary individuality apply when viral genomes are themselves split into different segments (segmented viruses), and especially when those segments can transmit independently (multipartite viruses) (Holmes, 2009;Leeks et al, 2023;Lucía-Sanz & Manrubia, 2017;Michalakis & Blanc, 2020)?…”

“…The existence of these viral social traits, both new and existing, provides many opportunities for both virology and evolutionary biology. From the perspective of virology, evolutionary theory can unify otherwise disparate viral entities, provide new answers to old questions, and offer new directions for empirical research (Díaz‐Muñoz et al, 2017; Domingo‐Calap et al, 2019; Leeks et al, 2021, 2023; Turner & Chao, 1999; Wild et al, 2009; Wilke, 2005). From an evolutionary perspective, viruses represent a new arena for testing existing theory, offer a range of new puzzles to explore, and can both challenge and extend established bodies of theory (Borges et al, 2018; Landsberger et al, 2018; Michalakis & Blanc, 2020; Shirogane et al, 2021, 2023; Sicard et al, 2019; Skums et al, 2015).…”

Conserved untranslated regions of multipartite viruses: Natural markers of novel viral genomic components and tags of viral evolution

“…These benefits provide a foundation for formulating a hypothesis regarding the evolutionary transition of viral genomes from monopartite to multipartite. This hypothesis remains plausible even if multipartite genomes arise through a potential mechanism of cheating in monopartite populations, making them comparatively less competitive ( Leeks et al. 2023 ).…”