Interspecific Infection Mimicry: False Infection as an Anti-Predator Strategy
For prey, exhibiting dishonest signals of infection could deter predators under a range of circumstances. Dishonest signals to predators are not uncommon in prey: for example, Batesian mimicry is the well-studied phenomenon of non-harmful prey mimicking the honest signals and cues of dangerous species (Bates, 1862). We propose that cases in which parasites are generalists (i.e., could infect both predator or prey) or merely negatively impact the predator (i.e., make it sick or render the prey distasteful) could foster the evolution of dishonest signals of infection or sickness in prey.
Lafferty (1992) produced a model and classic review paper demonstrating that predators do not tend to be deterred by parasitized prey and may prefer them. He explains this as a result of parasites causing their prey to become easier to catch and handle, often via parasite-induced behavioural changes or increased conspicuousness. While this article is often cited as an argument against predators avoiding parasitized prey, it should be noted that this model specifically considers trophically-transmitted parasites. As such, these parasites have evolved to be consumed by a secondary (predator) host and use behavioural manipulations of their intermediate hosts to complete this lifecycle. By contrast, parasites that are not adapted to this multi-host lifecycle may not induce host behaviours that increase ease of capture. In extreme cases, some parasites cause aposematism (Fenton et al.2011) or other defensive mechanisms in their hosts (Chailleux et al. 2013) to reduce the risk of predation. Thus, we argue that there could be a range of conditions where the evolution of infection-mimicry is favored by causing prey to become less appealing to predators.
There is evidence to suggest predators do avoid sick or parasitized prey. For example, Macrolophus pygmaeus , an egg predator, shows a preference for Tuta absoluta eggs unparasitized byTrichogamma parasitoids (Chailleux et al. 2013). Late-stage parasitized eggs turn black due to melanisation by the parasitoid larvae, and these black eggs are highly discriminated against. Similarly, rejection of parasitized prey has been noted in a variety of other vertebrate and invertebrate taxa (Holling 1955; MacLellan 1958; Hulscher 1973; Quezada & DeBach 1973; Sloan & Simmons 1973; Cowan 1981; Hoelmer et al. 1994; Roger et al. 2001; Al-Zyoud & Sengonca 2004). In such cases, it is plausible for mimics to exploit these predator preferences and to be maintained at some frequency.
The same general argument can apply to mimicry as a means of avoiding attack by parasitoids. Multiple parasitism often increases the odds of premature host mortality or can otherwise reduce parasitoid fitness, so parasitoids regularly evolve preferences against pre-parasitized hosts (Salt 1961; Prince 1976; Iwasa et al. 1984). In such cases, selection could favor the evolution of mimics that can falsely convey pre-infection.
The maintenance of dishonest signaling in these circumstances depends on the particulars of the system. For example, characteristics of the parasite are important as the parasite must either cause infection in the predator, render it ill, or otherwise decrease the value of the prey relative to alternatives. The plausibility of mimic strategies will also depend on the availability of alternative prey (Kokko et al.2003), meaning that the success of mimicry will depend on how specialized the predator is, and the composition of the prey community as a whole. Highly specialized predators will be under strong selection to counter mimicry as a deterrent strategy.