Sub-lethal effects of pathogens can lead to the evolution of lower virulence in multiple infections

Abstract

According to current evolutionary dogma, multiple infections generally increase a parasite's virulence (i.e. reduce the host's reproductive success). The basic idea is that the competitive interactions among strains of parasites developing within a single host select individual parasites to exploit their host more rapidly than their competitors (thereby causing an increase in virulence) to ensure their transmission. Although experimental evidence is scarce, it often contradicts the theoretical expectation by suggesting that multiple infections lead to decreased virulence. Here, we present a theoretical model to explain this contradiction and show that the evolutionary outcome of multiple infections depends on the characteristics of the interaction between the host and its parasite. If we assume, as current models do, that parasites have only lethal effects on their host, multiple infections indeed increase virulence. By contrast, if parasites have sub-lethal effects on their host (such as reduced growth) and, in particular, if these effects feed back onto the parasites to reduce their rate of development, then multiplicity of infection generally leads to lower virulence.

Introduction. Ecological immunology

“…Lower virulence may result if parasites are closely related (thus being subject to kin selection), if they cooperate in host exploitation, and/or if they get the same share irrespective of their actions (e.g. Frank 1996;Brown 1999;Brown et al 2002;Schjorring & Koella 2003;Rauch et al 2008). In turn, the former scenario should increase, whereas the latter decreases selection on host immunity.…”

Bacteriocins, spite and virulence

“…One possible explanation for this is that variation in the underlying biological details can lead to alternative relationships (Frank 1996;Ganusov & Antia 2003;Schjørring & Koella 2003). In particular, it has been shown that if parasites can cooperate to overcome their host's defences then the opposite prediction is favoureda positive relationship between parasite kinship and virulence (Chao et al 2000;Brown et al 2002;West & Buckling 2003).…”

Competition, virulence, host body mass and the diversification of macro-parasites

“…On the contrary, if the ecological character was to evolve before virulence, then adaptive diversification would lead to a lower level of competition between types of parasites and would reduce the strength of selection for virulence. On the other hand, if one was to consider the evolution of virulence, then an interesting point is that such evolution has been shown to be significantly affected if parasites have sublethal effects on the host and that, correlatively, infection decreases within-host parasite fitness [93]. This could, indeed, be the case as many macro-parasites are well known to have such sublethal effects, typically affecting their host growth [95,96] or rate of reproduction [97,98], and because parasite development and reproduction [99 -101] can, indeed, be restricted in infected hosts.…”

“…This could, indeed, be the case as many macro-parasites are well known to have such sublethal effects, typically affecting their host growth [95,96] or rate of reproduction [97,98], and because parasite development and reproduction [99 -101] can, indeed, be restricted in infected hosts. Multiple infections could then actually select for reduced (rather than increased) virulence [93], leading to other original patterns of coevolution between ecological traits involved in competitive interactions and virulence.…”