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.

Spatial differentiation of background matching strategies along a Late Pleistocene range expansion route

“…We found significant differences in the ability to change dorsal colour and in background colour preferences between populations in Sardinia and Corsica. Although inter-individual and among-population differentiation in background matching abilities has been studied in other taxa (Marshall et al, 2015, 2016; Bailing et al, 2020; Yamamoto and Sota, 2020), including amphibians (Wente & Phillips, 2003; Kang et al, 2016; Barnett et al, 2021), this is the first study analysing patterns of variation in background matching abilities along a historical range expansion route. To the best of our knowledge, this is also the first study addressing spatial patterns of variation in anti-predatory traits in the context of the recent biogeographic history of populations.…”

Camouflage in lichen moths: Field predation experiments and avian vision modelling demonstrate the importance of wing pattern elements and background for survival

“…Similar differential survival on matching and non‐matching backgrounds has been demonstrated in the tiger beetle Chaetodera laetescripta . Yamamoto and Sota ( 2020 ) found that there was a strong selective advantage for artificial beetle models that were placed on colour matching substrates, whereas the models on the non‐matching backgrounds suffered significantly higher predation.…”

Sandy beach dwelling crickets (Orthoptera: Trigonidiidae) have no preference for substrates that match their body color

“…In addition, Yamamoto and Sota (2020) showed that natural selection by visual predators has driven the evolution of finely tuned background‐matching camouflage in the tiger beetle Chaetodera laetescripta . The elytral color of the beetle matches the background of local habitats (Yamamoto & Sota 2020). If selection leads to a correlation between body color and substrate in D. csikii , each type of sand in the different habitats would lead to a different body color of the crickets.…”

“…However, preference for cryptic substrate may have evolved in populations that inhabit narrower beaches or the edges of habitats because of greater opportunities for selection. In addition, Yamamoto and Sota (2020) showed that natural selection by visual predators has driven the evolution of finely tuned background‐matching camouflage in the tiger beetle Chaetodera laetescripta . The elytral color of the beetle matches the background of local habitats (Yamamoto & Sota 2020).…”