Evolutionary fine-tuning of background-matching camouflage among geographical populations in the sandy beach tiger beetle

Abstract

Background-matching camouflage is a widespread adaptation in animals; however, few studies have thoroughly examined its evolutionary process and consequences. The tiger beetle Chaetodera laetescripta exhibits pronounced variation in elytral colour pattern among sandy habitats of different colour in the Japanese Archipelago. In this study, we performed digital image analysis with avian vision modelling to demonstrate that elytral luminance, which is attributed to proportions of elytral colour components, is fine-tuned to match local backgrounds. Field predation experiments with model beetles showed that better luminance matching resulted in a lower attack rate and corresponding lower mortality. Using restriction site-associated DNA (RAD) sequence data, we analysed the dispersal and evolution of colour pattern across geographical locations. We found that sand colour matching occurred irrespective of genetic and geographical distances between populations, suggesting that locally adapted colour patterns evolved after the colonization of these habitats. Given that beetle elytral colour patterns presumably have a quantitative genetic basis, our findings demonstrate that fine-tuning of background-matching camouflage to local habitat conditions can be attained through selection by visual predators, as predicted by the earliest proponent of natural selection.

Keywords: camouflage; character evolution; coloration; local adaptation.

Figure 1.

(a) Sampling sites, sand coloration and elytral colour pattern of the tiger beetle Chaetodera laetescripta. (b) Resemblance of C. laetescripta body colour to sand background at Site F (i) and Site K (ii). Photographs by N. Yamamoto. (Online version in colour.)

Figure 2.

(a) Correlation of luminance between elytra of Chaetodera laetescripta and the sand of its habitats, from the perspective of avian predator vision. Error bars indicate standard deviation. Grey lines are contour lines for given JND values. (b) Correlation between the mean percentage of white area and luminance among C. laetescripta elytra. (Online version in colour.)

Figure 3.

Percentages of paper tiger beetle models attacked by birds on light sand (left; Site J) and dark sand (right; Site F) during the experiments (n = 2981). (Online version in colour.)

Figure 4.

(a) ML tree of restriction site-associated DNA (RAD) sequences. See electronic supplementary material, table S1 for details of samples. (b) Relationships of genetic distance (F_ST) with geographical distance and (c) difference in mean percentage of white area in the elytra of Chaetodera laetescripta. (d) Mean percentage of elytral white area in the elytra of C. laetescripta from each locality (right), with phylogenetic relationships among populations (left). (Online version in colour.)