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.