Parasitism and the evolutionary ecology of animal personality

Abstract

The ecological factors responsible for the evolution of individual differences in animal personality (consistent individual differences in the same behaviour across time and contexts) are currently the subject of intense debate. A limited number of ecological factors have been investigated to date, with most attention focusing on the roles of resource competition and predation. We suggest here that parasitism may play a potentially important, but largely overlooked, role in the evolution of animal personalities. We identify two major routes by which parasites might influence the evolution of animal personality. First, because the risk of acquiring parasites can be influenced by an individual's behavioural type, local parasite regimes may impose selection on personality traits and behavioural syndromes (correlations between personality traits). Second, because parasite infections have consequences for aspects of host 'state', parasites might induce the evolution of individual differences in certain types of host behaviour in populations with endemic infections. Also, because infection often leads to specific changes in axes of personality, parasite infections have the potential to decouple behavioural syndromes. Host-parasite systems therefore provide researchers with valuable tools to study personality variation and behavioural syndromes from a proximate and ultimate perspective.

Figure 1.

Graphical illustration of how parasites could influence the evolution of behavioural syndromes. In this example, one parasite (‘A’, an introduced endoparasite) is acquired through the predation of an introduced (and hence novel) prey item, whereas another parasite (‘B’, an established ectoparasite) is acquired directly, through social contact with conspecifics. Hence, neophilic individuals may have a higher probability of exposure to parasite A, since they are more likely to approach the previously unencountered prey item, whereas more sociable individuals would be more exposed to parasite B. It is assumed that neophilia also has benefits, such as discovering new feeding opportunities, and that sociality has benefits. In this population, acquiring heavy loads of either species of parasite, or intermediate loads of each, is manageable, but acquiring high loads of both is fatal as a result of synergistic effects of infection. The diagonal line shows the syndrome that is likely to evolve in the host population because of parasite-induced correlational survival selection.

Figure 2.

Graphical illustration of how infection status might generate intraspecific variation in behavioural syndromes, if parasites selectively alter behaviour. (a) A ‘behavioural reaction norm’ plot (Dingemanse et al. 2010b) with two environmental conditions (N, no parasites, and P, with parasites) on the x-axis and values of a behavioural trait on the y-axis, where each individual is represented by two points connected by a line. The parallel lines indicate that this behaviour is unaffected by parasite infection. (b) the reaction norm plot for a second behaviour, where behavioural phenotypes of individuals differ under condition ‘N’ but are all the same in condition ‘P’ (i.e. all show high values when parasitized). (c) The expected correlation between the two behaviours (1 versus 2), with the two ellipses depicting the predicted phenotypic correlations for the parasitized (shaded) and non-parasitized (open) states.