The Effects of Predator Learning, Forgetting, and Recognition Errors on the Evolution of Warning Coloration

Abstract

This paper demonstrates that the specifics of predator avoidance learning, information loss, and recognition errors may heavily influence the evolution of aposematism. I establish a mathematical model of the change in frequency over time of bright individuals of a distasteful prey species. Warning color spreads through green beard selection as reformulated by Guilford (1990); bright colored forms gain an advantage due to their phenotypic resemblance to other bright forms, which have been sampled by the predator. I use a general classical conditioning model to examine gradual predator learning and forgetting, and then consider the extreme of one-trial learning and no forgetting over time that may occur with very toxic prey. The advantage of conspicuous coloration under these latter conditions depends upon its role in lowering a constant probability of the prey being misidentified and thus mistakenly attacked by a predator, a rarely emphasized factor in the evolution of warning coloration. This constant probability of mistaken attacks can also be interpreted as a constant probability that forgetting has occurred (forgetting does not increase with time) or a periodic decision by the predator to resample avoided prey. I show that when predators learn and forget gradually, as under the general classical conditioning model, it is very difficult for aposematic coloration to become established unless bright individuals cross an often high threshold frequency through chance factors. In contrast, the conditions expected with highly toxic prey promote the evolution of warning coloration more easily, by means from the fixation of very bright mutations to the fixation of successive mutations each of which causes a small increase in a prey's conspicuousness. The results therefore predict that aposematic coloration may have evolved in a different manner in different predator and prey systems. They also suggest that it may be extremely difficult for warning coloration to evolve in more mildly toxic or distasteful prey outside of a mimicry system.

Avoidance of an aposematically coloured butterfly by wild birds in a tropical forest

“…Prey palatability is known to influence predator learning and memory of warning colours (Lindström et al , 2006; Skelhorn & Rowe, 2006; Svádová et al , 2009). Having both warning colouration and distastefulness can change predator decision‐making and increase avoidance (Servedio, 2000). However, the short period between trials means that we cannot distinguish between true ‘memory’ and a short‐term aversion reaction to explain these results.…”

“…Similar results were found for another Heliconius predation experiment in which the ‘nonlocal’ phenotype had higher attack rates (Finkbeiner et al , 2014). Different predators are likely to have different aversion responses to colour, and so the heterogeneity of predators in the wild might explain this result (Endler, 1988; Servedio, 2000; Speed et al , 2000; Endler & Mappes, 2004). …”

“…Predator psychology models assume that the rate of predation is dependent on learning and forgetting rates, and the absence of reinforcing experiences might lead to forgetfulness (Turner & Speed, 1996; Speed & Turner, 1999; Servedio, 2000; Speed, 2000). For instance, Jacamars have been shown to forget novel colour morphs after an interval of 2 years (Langham, 2004), which might have been as a result of a lack of reinforcing encounters with the artificial prey.…”

“…Memory is linked to recognition, and if predators forget about experiences with prey, then recognition of an aposematic signal is not possible (Speed, 2000). Warning signals should, therefore, be selected to be memorable, to provoke low rates of forgetting and enhance predator aversion (Servedio, 2000; Speed, 2000). Among mimetic butterflies, long‐term memorability of learned avoidance of the model is vital for the protection of the co‐mimic.…”

The evolution of coloration and toxicity in the poison frog family (Dendrobatidae)

“…These results are consistent with the hypothesis that coloration in this group is aposematic. aposematism ͉ phylogeny ͉ amphibian A posematism (warning coloration) occurs when conspicuous appearance (particularly coloration) functions to advertise unprofitability (unpalatability, toxicity, or ability to resist or escape predation) to predators (1). The evolution of aposematism has been the subject of considerable debate (2,3).…”