How and why parasite virulence (terms in bold font are in the Glossary) evolves are arguably some of the most important questions addressed by evolutionary biologists. The 1990s saw rich and abounding research in this area, mostly based on the 'trade-off hypothesis' (Anderson & May, 1982), which states that virulence is an unavoidable consequence of parasite transmission (see Box 1). In this review, we first briefly outline the seldomdiscussed history of virulence evolution. Then, we expose the current debate in the field, which can be summarized as a challenge to the trade-off hypothesis. Finally, to answer this challenge, we discuss the advances made in the past decade and we argue that, in the light of these advances, we need not abandon the trade-off model. Instead, we argue that these new insights ought to be incorporated into the current theory and we identify promising future directions.
A history of virulenceMany, if not most, of the recent theories that attempt to explain how parasites evolve assume that there is a link between virulence and transmission, the so-called 'virulence-transmission trade-off'. However, this idea has become the focus of intense debate. To better understand the issues of current debates in the field, one should be aware that virulence evolution was studied long before the trade-off hypothesis was formulated. Our purpose here is not to present an exhaustive review of the history of the study of infectious diseases but to give a mere glimpse of the richness and originality of this field that has linked many disciplines, from ecology to molecular biology.The notion that virulence is not fixed but evolves can be traced to Pasteur and Koch in the 19th century.
AbstractIt 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.