The ultimate expansion of our knowledge of viral diversity, fostered by the last advances on virus transcriptomics (Shi et al., 2016), has just begun. Studies using those techniques have led to the discovery of new viral species at an unprecedented rate. Major gaps in virus evolution understanding will in all likelihood start to close in forthcoming years. The catalogue of multipartite species, mostly infecting plants, will benefit from the new sampling and sequencing techniques. It is foreseeable that their, in principle narrow, host- range will broaden. Actually, we already have evidence indicating that multipartitism is not limited to plants: possible multipartite candidates are infecting fungi and animals (Ghabrial et al., 2008; Olveira et al., 2009; Ladner et al., 2016).
Though general molecular advantages of multipartitism are, as of yet, a puzzle, these viruses do depend on the metabolism and the structure of plant tissues (Miyashita and Kishino, 2010; Sicard et al., 2019). However, it would be important to study the lifestyles of non-plant multipartite viruses at a level of detail similar to that of multipartite plant viruses to find out whether the complementation among genomic segments follows a mech- anism analogous to that known to take place in plant tissues. Spatial structure might be es- sential to guarantee the persistence of multipartite viruses by reducing the cost of coinfec- tion through local clustering. Recent theoretical work illustrates the importance of spatial propagation for the maintenance of multipartite viruses, not only in regard to their within- host transmission: actually, most multipartite species described infect monocultures where plants are spatially distributed. In particular, a structured host-to-host transmission, to- gether with genetic drift, as been put forward as a plausible explanation for a contingent success of multipartite viruses over monopartite counterparts (Valdano et al., 2019). An
Multipartite viruses: Organization, emergence and evolution. By Adriana Luc´ıa Sanz
58 DISCUSSION & PERSPECTIVES
independent approach considers a spatial distribution of hosts that can be progressively infected. Intermediate infected hosts with one to few genomic segments that remain for a long enough time in the host might boost a more pervasive infection compared to the monopartite case (Zhang et al., 2019). The previous theoretical results notwithstanding, this intermediate, latent state, is not likely to exist in nature.
Different ways in which the complementation requirement can be alleviated are possi- ble, but not yet investigated. Perhaps the success of multipartitism is partly relying on a dynamical strategy where its advantages are the opportunistic colonization of new hosts by eliciting fast adaptive responses through complementation of formerly independent ge- nomic segments. Cooperation of such segments is a must for this strategy to be plausible. In fact, it is plants that offer a particularly suitable environment for loose cooperative asso- ciations between virus and virus-like agents of different origins. The association of genetic elements might have turned permanent when the ecological conditions drove the partners to an interdependent relationship. For example, if infection becomes conditional on the joint cooperation of a pair of genetic elements, a bipartite species appears as a natural so- lution. We hypothesize that this scenario offers a plausible origin for multipartite species. However, further mathematical models and additional empirical evidence will be essential to reveal which ecological conditions might favour the emergence of multipartite forms in competition with monopartite viral species.
Cooperation of genetic elements could be followed by recombination as a fundamental mechanism for the generation of novel viruses (Sachs and Bull, 2005). However, multipar- tite and segmented viruses apparently break that rule (Varsani et al., 2018). In particular cases, such as -RNA viruses, the coverage of the genetic material by a nucleocapsid protein represents a physical limitation to recombination, since the genetic material is not exposed. Nonetheless, the lack of recombination of the rest of Baltimore classes might be compen- sated by a more plastic mechanism of reassortment or gene shuffling. In fact, multipartite RNA viruses are more prone to share genes with other multipartite species than segmented or monopartite viruses with akin genome configurations. Cooperation might show up as a modular constructive principle of multipartite viral species. In fact, cooperation acquires a broader meaning if ensembles of viral species are portrayed as complex, gene-sharing networks, where it emerges as a distributed property of the ensemble. Contrary to highly stable associations of genes in chromosomes, gene sharing in multipartite viruses offers an exploding number of combinatorial possibilities that might translate into many possible different viral species in short evolutionary time.
Whether associations among genetic segments is a stable strategy or whether they might evolve to monoparticle viral forms (segmented or monopartite) remains as a further open question (Nee and Maynard-Smith, 1990). Actually, there might be restrictions to recombi- nation and single particle encapsidation that either stabilize the multipartite state or at least delay the emergence of a monopartite cognate form —provided it would be a fitter solu- tion. Multipartite viruses have emerged many times in evolution, and at present it seems easier to understand them as a fit, but only transiently stable solution in evolutionary time. Multipartite viruses might be the dynamic product of a huge and plastic pangenome that is constantly proposing, permitting and sustaining new associations in a complex, changing and diverse global ecology.