The true cost of host manipulation by parasites

Abstract

If there is one thing that the past three decades of research in behavioural and evolutionary ecology have taught us, it is that there are no free lunches. Adaptive traits provide net fitness benefits to the animals bearing them, but the gains would be even greater if there were no concurrent costs associated with the expression of those traits. The ability of many parasites to enhance their transmission success by manipulating the behaviour of their hosts is one such trait (see Moore, 2002). In their excellent synthesis of past and current research on this phenomenon, Thomas et al. (2005) cast a doubt on the importance of the cost incurred by manipulating parasites. They argue that the existence and magnitude of such costs are dependent upon the type of mechanism used by a parasite to alter host behaviour. Thomas et al. (2005) focus exclusively on physiological, or proximate, costs such as the energetic costs necessary for the production of neuroactive substances in parasite species that use them to modify host behaviour. In a broader evolutionary context, however, one must consider costs at the ultimate level, in terms of fitness. Fitness is usually defined as the average number of surviving offspring produced by individuals with a certain genotype relative to that produced by other genotypes, or as an individual's relative contribution of genes to future generations (Ridley, 1996; Freeman and Herron, 2001), Energy is not the best currency to measure loss of fitness, because other fitness components, such as mortality risk, cannot readily be quantified in units of energy. Elsewhere in their review, in their discussion of mafia-like strategies, Thomas et al. (2005) consider fitness costs, but a similar perspective is needed to assess the cost of manipulation itself. Here, we wish to re-visit the issue of costs associated with manipulation.