Frequency-dependent assistance as a way out of competitive exclusion between two strains of an emerging virus

Abstract

Biological invasions are the main causes of emerging viral diseases and they favour the co-occurrence of multiple species or strains in the same environment. Depending on the nature of the interaction, co-occurrence can lead to competitive exclusion or coexistence. The successive fortuitous introductions of two strains of Tomato yellow leaf curl virus (TYLCV-Mld and TYLCV-IL) in Réunion Island provided an ideal opportunity to study the invasion of, and competition between, these worldwide emerging pathogens. During a 7-year field survey, we observed a displacement of the resident TYLCV-Mld by the newcomer TYLCV-IL, with TYLCV-Mld remaining mostly in co-infected plants. To understand the factors associated with this partial displacement, biological traits related to fitness were measured. The better ecological aptitude of TYLCV-IL in single infections was demonstrated, which explains its rapid spread. However, we demonstrate that the relative fitness of virus strains can drastically change between single infections and co-infections. An epidemiological model parametrized with our experimental data predicts that the two strains will coexist in the long run through assistance by the fitter strain. This rare case of unilateral facilitation between two pathogens leads to frequency-dependent selection and maintenance of the less fit strain.

The Strange Lifestyle of Multipartite Viruses

“…However, cases in which this bottleneck was actually quantified are rare in plant viruses and not yet available in animal viruses. The transmission of Potato virus Y (PVY) was shown to result from the transfer of as few as one or two genomes per aphid vector [92], and similar figures were obtained for the whitefly-transmission of Tomato yellow leaf curl virus (TYLCV) [93]. Higher numbers are intuitively expected for multipartite viruses, in order to increase the chances of co-transmitting a set of particles containing at least one copy of each segment.…”

Exposing the Diversity of Multiple Infection Patterns

“…Hence, there are only two different inoculation outcomes per genotype. The outcome may nevertheless depend on the presence of other genotypes inoculated previously or simultaneously and we define a 65 multiple infection pattern as the set of outcomes over all possible inoculation challenges.…”

“…Some experimental articles apply the adjective 'coinfected' to hosts that are infected by potentially non self-sufficient parasites, such as satellite viruses (see the discussion part on ambinfection below and [34]). These studies are usually interested in the interactions between parasites and search for synergistic or antagonistic effects that may affect epidemiological traits such as virulence or transmission [65]. However, they do not focus on qualitative properties of the outcome, such as one genotype being 410 rescued by the other.…”

“…In nature, coinfection is a common pattern: Mycobacterium tuberculosis and the Human immunodeficiency virus (HIV) in humans [68], or the two strains of the Tomato yellow leaf curl virus, TYLCV-Mld and TYLCV-IL, in tomato plants [65], are two examples of coinfections, since parasites can infect their host both together and alone. Furthermore, results from metagenomics suggest that coinfection is commonplace [69].…”

The susceptibility of primary cultured rhesus macaque kidney epithelial cells to rhesus cytomegalovirus strains

“…Given the low frequency (~6.7 %) of the full-length variant in the original Telo-RF-propagated stock, coupled with propagation of the 180.92 stock in MKE at exceedingly low m.o.i. (<0.01), it is possible that the loss of the full-length 180.92 variant in MKE virus stock may result from negative selection induced by the predominant truncated variant or frequency-dependent strain selection Perefarres et al, 2014;Renzette et al, 2011).…”