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

Abstract

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.

The industrialization of farming may be driving virulence evolution

“…This is the standard transmission–virulence trade‐off assumption (Alizon, Hurford, Mideo, & Van Baalen, 2009). In other words, increases in transmission can only come at a “cost” of an increase in virulence.…”

“…The shape of the transmission–virulence trade‐off is not known. Although there has been an upsurge in support that transmission increases with virulence (Alizon et al., 2009), whether the curve is concave up, or concave down, is of debate. Our results rely on the curve being concave down, and given the biological constraints on the parameters, we feel that this assumption is reasonable.…”

Testing for local host–parasite adaptation: an experiment with Gyrodactylus ectoparasites and guppy hosts

“…Second, Gyrodactylus can cause high guppy mortality in the field and, especially, in the laboratory (Scott and Anderson, 1984;van Oosterhout et al, 2003;Cable and van Oosterhout, 2007a,b). It may be conceivable that very high virulence in Gyrodactylus might be maladaptive if it increases host mortality in such way that the basic Gyrodactylus reproductive rate is reduced (Dybdahl and Storfer, 2003;Alizon et al, 2008). In this way, lower virulence in Gyrodactylus could evolve in response of the lower resistance of their guppy host (Altizer, 2001;Sternberg et al, 2013) -although the opposite effect has also been reported (Hoeksema and Forde, 2008).…”

“…Theoretical models often predict that increased parasite transmission (and therefore perhaps increased virulence) should evolve under increased host mortality (Anderson and May, 1982;Gandon and Michalakis, 2002). Given that higher parasite reproductive and transmission rates can increase local parasite adaptation (Alizon et al, 2008), Gyrodactylus from HP environments would be expected to perform better (e.g., parasite growth rate, infectivity, prevalence, mean abundance) on their sympatric compared with allopatric hosts (higher performance leads to higher fitness) -although this of course would also select for higher resistance in HP guppies. This expectation has not been demonstrated in our study as we found no relationship between predation regime and local maladaptation by parasites.…”

Broad thermal tolerance is negatively correlated with virulence in an opportunistic bacterial pathogen

“…For example, it has been shown that increased expression of virulence factors is correlated with increased temperature in Vibrio species (Mahoney, Gerding, Jones, & Whistler, 2010; Oh, Lee, Lee, & Choi, 2009). In theory, virulence will evolve to a level at which virulence and transmission are balanced to optimize the spread of the pathogen (Alizon, Hurford, Mideo, & Van Baalen, 2009). Nevertheless, virulence is context–dependent, as both biotic factors such as host condition (Pulkkinen & Ebert, 2004) and host density (Bieger & Ebert, 2009) and abiotic factors such as temperature (Guijarro, Cascales, García‐Torrico, García‐Domínguez, & Méndez, 2015) can influence virulence.…”