Kin Selection and Parasite Evolution: Higher and Lower Virulence with Hard and Soft Selection

Abstract

Conventional models predict that low genetic relatedness among parasites that coinfect the same host leads to the evolution of high parasite virulence. Such models assume adaptive responses to hard selection only. We show that if soft selection is allowed to operate, low relatedness leads instead to the evolution of low virulence. With both hard and soft selection, low relatedness increases the conflict among coinfecting parasites. Although parasites can only respond to hard selection by evolving higher virulence and overexploiting their host, they can respond to soft selection by evolving other adaptations, such as interference, that prevent overexploitation. Because interference can entail a cost, the host may actually be underexploited, and virulence will decrease as a result of soft selection. Our analysis also shows that responses to soft selection can have a much stronger effect than responses to hard selection. After hard selection has raised virulence to a level that is an evolutionarily stable strategy, the population, as expected, cannot be invaded by more virulent phenotypes that respond only to hard selection. The population remains susceptible to invasion by a less virulent phenotype that responds to soft selection, however. Thus, hard and soft selection are not just alternatives. Rather, soft selection is expected to prevail and often thwart the evolution of virulence in parasites. We review evidence from several parasite systems and find support for soft selection. Most of the examples involve interference mechanisms that indirectly prevent the evolution of higher virulence. We recognize that hard selection for virulence is more difficult to document, but we take our results to suggest that a kin selection model with soft selection may have general applicability.

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

“…Indeed, most models on the evolution of virulence in multiple infections consider systems where the parasite's fitness is affected only by adverse effects on the host's survival (Bonhoeffer & Nowak 1994;Nowak & May 1994;May & Nowak 1995;Van Baalen & Sabelis 1995;Frank 1996;Chao et al 2000). Although in such host2parasite associations multiple infections may select for higher virulence, we have shown here that in other kinds of host2parasite associations multiple infections need not do so.…”

“…These studies indicate that some mechanisms of host exploitation may select cooperative interactions among the parasites and, therefore, lead to the evolution of lower virulence in multiple infections (Turner & Chao 1999). The mechanisms could be based on a trade-off between competitive ability of the parasite and their growth rate (Chao et al 2000) or on the collective action of parasites-manufacturing products that are shared by the phage during their reproduction-when they are exploiting their host (Turner & Chao 1999;Brown 2001;Brown et al 2002). The latter idea has been used to indicate a dichotomy in the prediction for the evolution of virulence in multiple infections.…”

Competitive fates of bacterial social parasites: persistence and self–induced extinction ofMyxococcus xanthuscheaters

“…RNA replicase in viral infections or developmental signals in M. xanthus) that are generated by group members themselves. In recent studies, investigators have modelled the effects of relatedness within coinfecting groups on virulence when the reproductive rate of individuals is limited by the collective action of all group members (Chao et al 2000;Brown et al 2002;West & Buckling 2003). Because genetic heterogeneity increases the likelihood of interference competition and social cheating, low within-group relatedness can decrease the collective effect (virulence in this case) of an infecting group.…”

Taking Stock: Relating Theory to Experiment

“…No doubt, the consequences for the evolution of virulence are decisive. For example, if parasite clones invest more energy in interference than in replication, multiple infections may lead to reduced instead of increased virulence (Chao et al 2000).…”