Macroevolution of protective coloration across caterpillars reflects relationships with host plants

Abstract

A critical function of animal coloration is avoiding attack, either by warning predators or reducing detectability. Evolution of these divergent strategies may depend on prey palatability and apparency to predators: conspicuous coloration may be favoured if species are distasteful, or habitats make hiding difficult; by contrast, camouflage may be effective if prey lack defences or environments are visually complex. For insect herbivores, host plants provide both chemical defence and the background against which they are detected or obscured; thus, plant traits may be key to coloration in these foundational terrestrial organisms. We use 1808 species of larval Lepidoptera to explore macroevolution of protective coloration strategy. We find that colour and pattern evolve jointly in caterpillars, similar to an array of species across the animal kingdom, while individual elements of coloration evolve closely with diet ecology. Consistent with key tenets of plant defence and plant–herbivore coevolutionary theory, conspicuous colours are associated with herbaceous host plants—thought to be defended by toxins—while camouflage colours and patterns are associated with woody plants and grasses. Contrary to theory, dietary specialization is not associated with conspicuous coloration. Our results add valuable insights into the evolutionary forces shaping colour and pattern in nature.

Pattern variation is linked to anti-predator coloration in butterfly larvae

“…Previous work has found that bands may be linked to sociality across various taxa [43] yet, despite the potential enhancement of the warning signal by grouping overall [13,37,41,42], we found no evidence that specific aposematic patterns are used more by solitary or gregarious larvae. This is aligned with previous findings that the patterns of warning signals are of secondary importance to avian predators, which instead focus primarily on colour [10][11][12].…”

“…For aposematic species, our findings support those of a recent study using a similar approach [13], in that larvae are most likely to use a pattern of colour-contrasting, horizontal bands or spots. This suggests there is some inherent quality (or qualities) of these patterns which support effective aposematic signalling.…”

“…To our knowledge, our study provides the first investigation into the covariance of colour pattern and grouping behaviour in lepidopteran larvae. Indeed, to date, only one other study has explored the pattern variation between lepidopteran larvae using different anti-predator colour strategies [13].…”

“…The pattern elements recorded were bands, coloured defences, longitudinal stripes, 'other' (includes patches and countershading), spots and no pattern element (detailed descriptions provided in figure 1). A recent study by Robinson et al [13] independently devised a highly similar categorization of larval colour strategy and patterning, in which specific colour combinations, and whether colours typically contrast with the background or not, were used to infer crypsis and aposematism. Nevertheless, we recognize that pattern categorization, and whether a signal is perceived as aversive or not, may be dependent on the natural setting and distance of the viewer.…”

“…By contrast, for aposematic species, the precise benefits of pattern use, instead of a single, conspicuous colour, are less obvious, given that colour is thought to be the more salient element of warning signals for birds [10][11][12]. Nevertheless, aposematic signals often contain multiple contrasting colours with repeating pattern elements [5,13]. Evidence suggests that these patterns help to enhance warning signal conspicuousness [14], aversiveness or recognizability/memorability [15][16][17][18][19], distinctiveness from more profitable prey [18,20], and may also reduce long-distance detectability of prey [21,22].…”