Spatial heterogeneity, predator cognition, and the evolution of color polymorphism in virtual prey

Abstract

Cryptically colored prey species are often polymorphic, occurring in multiple distinctive pattern variants. Visual predators promote such phenotypic variation through apostatic selection, in which they attack more abundant prey types disproportionately often. In heterogeneous environments, disruptive selection to match the coloration of disparate habitat patches could also produce polymorphism, but how apostatic and disruptive selection interact in these circumstances is unknown. Here we report the first controlled selection experiment on the evolution of prey coloration on heterogeneous backgrounds, in which blue jays (Cyanocitta cristata) searched for digital moths on mixtures of dark and light patches at three different scales of heterogeneity. As predicted by ecological theory, coarse-grained backgrounds produced a functional dimorphism of specialists on the two patch types; fine-grained backgrounds produced generalists. The searching strategies of the jays also varied with the habitat configuration, however. Complex backgrounds with many moth-like features elicited a slow, serial search that depended heavily on selective attention. The result was increased apostatic selection, producing a broad range of moth phenotypes. Backgrounds with larger, more uniform patches allowed the birds to focus on the currently most rewarding patch type and to search entire patches rapidly in parallel. The result was less apostatic selection and lower phenotypic variability. The evolution of polymorphism in camouflaged prey depends on a complex interaction between habitat structure and predator cognition.

Fig. 1.

Four digital moths shown on a sample of each of the three treatment backgrounds, in which the same dark and light pixel distributions are intermixed at progressively finer spatial scales. The moths in this figure evolved on the disjunct background and were among the most cryptic of the individuals in their population. Note that in the disjunct treatment (a), the moths are somewhat harder to detect on the patch that they most closely resemble but that all four can readily be located in a superficial scan. In the mottled (b) and speckled (c) treatments, the backgrounds incorporate high levels of noise at spatial frequencies comparable to the size of moths, and the moths are far more difficult to detect.

Fig. 2.

Fitness sets in a niche space defined by dark and light matching indices, displayed as contour plots of the phenotypes of all moths in all lineages from the 50th through the 100th generations. Data resulting from selection on each of the three experimental backgrounds are contrasted with the results of a nonselective, control process. Note that both the disjunct and mottled treatments produced bimodal, concave fitness sets with peak densities of moths along the axes, dividing the population into dark and light specialists. The speckled treatment produced a mostly convex fitness set that was more cryptic than the controls but not significantly dimorphic.

Fig. 3.

Distribution of moths in phenotypic space, from typical populations resulting from each of the three background treatments. The mean pixel color of each moth is plotted along the abscissa, and the standard deviation of pixel color is plotted on the ordinate. Thus, darker moths are to the left, lighter ones are to the right, more uniform moths are toward the bottom, and more diversely colored ones are at the top. The speckled population consists mainly of generalist moths that are intermediate in mean pixel color but that are relatively variable along the ordinate, reflecting high levels of apostatic selection. The disjunct population shows strong dimorphism along the mean color axis (due to disruptive selection for crypticity on disparate backgrounds) but less apostatic variation. Mottled moths exhibit the combined effects of both apostatic and disruptive selection.

Fig. 4.

Detection accuracy in blocks of 100 trials as a function of the matching index of the target moth and the dissimilarity between the target and the last previous correctly detected moth. Matching index increases from the bottom to the top, dividing the range of indices within each treatment into percentile groupings: low (0–33rd), medium (34–66th), and high (67–100th). Regression lines indicate the relationship between accuracy and dissimilarity within matching index groupings. Solid lines show results from trials in which both the target moth and the previous one occurred on the same patch type; dashed lines indicate results from moths occurring on different patch types.