Hierarchical overshadowing of stimuli and its role in mimicry evolution

Abstract

An elegant study by Kazemi et al. (2014, Current Biology, 24, 965e969) found that blue tits, Cyanistes caeruleus, that had been trained to distinguish between rewarding and nonrewarding prey subsequently avoided novel prey that had the same colour (but not the same shape or pattern) as the nonrewarding prey. Their work suggested that certain high-salience discriminatory traits can overshadow other informative traits, allowing imperfect mimics to establish. Here we began by replicating their ambitious experiment by evaluating the behaviour of 320 human subjects foraging on computer-generated prey. However, to fully understand how overshadowing might facilitate the establishment of incipient mimics, we significantly extended their protocol to a full factorial design involving mimics with colour, pattern and/or shape in common with their former models. As Kazemi et al. reported, participants placed more weight on colour similarity than on shape similarity when rejecting prey. Two-trait mimics with the same colour and pattern or the same colour and shape as their former models were avoided as frequently as perfect mimics, while colour-only mimics were avoided more frequently than shape-only mimics. Nevertheless, novel prey with no traits in common with nonrewarding models were avoided at high rates, possibly in part due to their dissimilarity to familiar rewarding prey. The implications of these findings for mimicry evolution are discussed.

Which traits do observers use to distinguish Batesian mimics from their models?

“…The "carry-over" we observed emphasizes that differences in early learning experiences (which in the wild can be varied and unpredictable) can have persistent effects on later behavior. Several previous studies have adopted a similar approach of using humans as surrogate predators to judge the accuracy of mimics, and show the utility of using human test subjects in enabling a large sample size (Golding et al 2005b;Penney et al 2012;Sherratt et al 2015). Of course, results from human trials can only be applied to real mimetic systems with a degree of caution, although their results tally well with other studies that have used avian predators (Dittrich et al 1993;Kazemi et al 2014).…”

“…Past studies that have used humans as predators (Golding et al 2005b;Sherratt et al 2015) have (to varying degrees) used the somewhat unrealistic scenario of the subjects being given time to inspect the images at their leisure, and in addition, Penney et al (2012) presented large, high-resolution images. The present work used a short presentation of a low resolution image in order to best resemble the situation in which a predator must make a quick decision based on an insect viewed from a distance, with any hesitation allowing the prey a chance to escape (Chittka and Osorio 2007;Abbott and Sherratt 2013).…”

“…Thus, a trait could be clearly perceivable by the predator but nonetheless overlooked. Such a trait will be under little or no selection for mimetic accuracy, which may account for inaccurate mimicry of some aspects of the model phenotype (Kazemi et al 2014;Sherratt et al 2015).…”

“…However, with birds as predators, experiments using artificial prey generally support the idea that color is an especially salient signal in the context of mimicry, although other traits such as pattern may come into play if color is not informative (Terhune 1977;Kazemi et al 2014). Humans also give a strong weighting to color in discriminating among rewarding and non-rewarding artificial prey Sherratt et al 2015), to an extent that may be suboptimal . The use of artificial prey in such experiments allows careful control over the stimuli, allowing different traits to be varied entirely independently.…”

“…Humans provide a useful model "predator", with fewer ethical and practical constraints, and experimental games in which humans "forage" for prey have previously generated large datasets to explore hypotheses about mimicry (Golding et al 2005b;McGuire et al 2006;Sherratt et al 2015;Morris and Reader, in review). Humans have been shown to make judgments about mimetic accuracy similar to those of birds, which are thought to provide the main selective pressure for mimicry in hoverflies (Dittrich et al 1993;Penney et al 2012;Sherratt et al 2015). While bird vision is sensitive to some ultraviolet wavelengths that are invisible to humans, these colors do not feature in the aposematic patterns of wasps or their mimics (Green et al 1999;Taylor et al 2016a).…”