AN EXPERIMENTAL TEST OF THE TRANSMISSION‐VIRULENCE TRADE‐OFF HYPOTHESIS IN A PLANT VIRUS

The transmission–virulence trade‐off hypothesis is one of the few adaptive explanations of virulence evolution, and assumes that there is an overall positive correlation between parasite transmission and virulence. The shape of the transmission–virulence relationship predicts whether virulence should evolve toward either a maximum or to an intermediate optimum. A positive correlation between each of these traits and within‐host growth is often suggested to underlie the relationship between virulence and transmission. There are few experimental tests of this hypothesis; this study reports on the first empirical test on a plant pathogen. We infected Brassica rapa plants with nine natural isolates of Cauliflower mosaic virus and then estimated three traits: transmission, virulence, and within‐host viral accumulation. As predicted by the trade‐off hypothesis, we observed a positive correlation between transmission and virulence, suggestive of the existence of an intermediate optimum. We discovered the unexpected existence of two groups of within‐host accumulation, differing by at least an order of magnitude. When accumulation groups were not accounted for, within‐host accumulation was correlated neither to virulence nor transmission, although our results suggest that within each group these correlations exist.     

HOST POPULATION STRUCTURE AND THE EVOLUTION OF VIRULENCE: A “LAW OF DIMINISHING RETURNS”

Structure in a population of host individuals, whether spatial or temporal, can have important effects on the transmission and evolutionary dynamics of its pathogens. One of these is to limit dispersal of pathogens and thus increase the amount of contact between a given pair or within a small group of host individuals. We introduce a “law of diminishing returns” that predicts an evolutionary decline of pathogen virulence whenever there are on average more possibilities of pathogen transmission between the same pair of hosts. Thus, the effect of repeated contact between hosts will be to shift the balance of any trade-off between virulence and transmissibility toward lower virulence.     

Virulence evolution and the trade‐off hypothesis: history,current state of affairs and the future

It has been more than two decades since the formulation of the so‐called ‘trade‐off’ hypothesis as an alternative to the then commonly accepted idea that parasites should always evolve towards avirulence (the ‘avirulence hypothesis’). The trade‐off hypothesis states that virulence is an unavoidable consequence of parasite transmission; however, since the 1990s, this hypothesis has been increasingly challenged. We discuss the history of the study of virulence evolution and the development of theories towards the trade‐off hypothesis in order to illustrate the context of the debate. We investigate the arguments raised against the trade‐off hypothesis and argue that trade‐offs exist, but may not be of the simple form that is usually assumed, involving other mechanisms (and life‐history traits) than those originally considered. Many processes such as pathogen adaptation to within‐host competition, interactions with the immune system and shifting transmission routes, will all be interrelated making sweeping evolutionary predictions harder to obtain. We argue that this is the heart of the current debate in the field and while species‐specific models may be better predictive tools, the trade‐off hypothesis and its basic extensions are necessary to assess the qualitative impacts of virulence management strategies.     

Virulence‐driven trade‐offs in disease transmission: A meta‐analysis*

The virulence–transmission trade‐off hypothesis proposed more than 30 years ago is the cornerstone in the study of host–parasite co‐evolution. This hypothesis rests on the premise that virulence is an unavoidable and increasing cost because the parasite uses host resources to replicate. This cost associated with replication ultimately results in a deceleration in transmission rate because increasing within‐host replication increases host mortality. Empirical tests of predictions of the hypothesis have found mixed support, which cast doubt about its overall generalizability. To quantitatively address this issue, we conducted a meta‐analysis of 29 empirical studies, after reviewing over 6000 published papers, addressing the four core relationships between (1) virulence and recovery rate, (2) within‐host replication rate and virulence, (3) within‐host replication and transmission rate, and (4) virulence and transmission rate. We found strong support for an increasing relationship between replication and virulence, and replication and transmission. Yet, it is still uncertain if these relationships generally decelerate due to high within‐study variability. There was insufficient data to quantitatively test the other two core relationships predicted by the theory. Overall, the results suggest that the current empirical evidence provides partial support for the trade‐off hypothesis, but more work remains to be done.