Which way to go? How a virus is transmitted determines its virulence

Many pathogens have the ability to be transmitted through more than one route: horizontally (between host individuals that are not parent and offspring) and vertically (from parent to offspring). Using a plant-virus system, CBGP researchers find evidence that pathogen virulence depends on which of these two transmission ways predominates in the virus life cycle.

Plant pathogens are responsible for about 15% of crop yield reduction worldwide every year, and cause economic loses estimated in more than €25 billions. In a world where the human population is constantly expanding, plant pathogens are not only a major economic problem as limiting factor for crop production, but also a social concern as they may compromise food supply. This is specially so in developing countries where small-plot agriculture represents the only food input for many families, and yield loses may reach 100%.

The great socio-economic impact of plant pathogens is due to their deleterious effect in the host, that is, to their virulence. Hence, a fundamental step to reduce the burden of plant infectious diseases, and improve food security, is to understand the factors that determine virulence evolution. It has been proposed that one of such factors is the mode of pathogen transmission. This hypothesis is based on the assumption that higher pathogen multiplication results in higher virulence. Pathogens that are horizontally transmitted (the pathogen is not transmitted through descent) would increase their chances of transmission at higher multiplication levels. Therefore, virulence and transmission rate would be positively correlated. On the other hand, hosts need to reproduce for pathogens that are vertically transmitted (from parent to offspring) to infect new individuals. Since virulence, by definition, reduces host fitness, vertically transmitted pathogens should evolve towards lower virulence to maximize their transmission success. To date, experimental support for this theory is scarce, and whether (and how) pathogen transmission mode affects virulence evolution remains only partially understood.

A group of CBGP researchers directed by Prof. Fernando García-Arenal has analyzed the evolution of virulence evolution of the plant virus Cucumber mosaic virus (CMV) under different modes of transmission in its natural host Arabidopsis thaliana. Three CMV strains were serially passaged in one Arabidopsis genotype for five generations under three transmission modes: strict vertical transmission, strict horizontal transmission, and alternating vertical and horizontal transmission. After the last passage, virus accumulation, virulence, and vertical transmission rate of the evolved and the non-evolved viruses, both in the original plant stock and in the progeny of plants derived from the fifth passage of vertical transmission, were compared. Results indicated that vertical passaging led to adaptation of the virus to greater vertical transmission, which was associated with reductions of virus accumulation and virulence. Comparison of virus performance in the two types of plants infected revealed that increases in vertical transmission and reductions in virus accumulation and virulence were determined also by reciprocal host adaptation during vertical passages. On the other hand, virulence and virus accumulation did not significantly change across passages of horizontal transmission.

Thus, this work provides evidence that strongly supports theoretical predictions, and illustrate on the key role that the complex interplay between mode of transmission and host-pathogen co-evolution has in determining virulence evolution. Considering this type of interplay is relevant to design more efficient strategies for controlling plant pathogens, and infectious diseases at large.