Evolutionary transitions from camouflage to aposematism: Hidden signals play a pivotal role

Abstract

The initial evolution of warning signals in unprofitable prey, termed aposematism, is often seen as a paradox because any new conspicuous mutant would be easier to detect than its cryptic conspecifics and not readily recognized by naïve predators as defended. One possibility is that permanent aposematism first evolved through species using hidden warning signals, which are only exposed to would-be predators on encounter. Here, we present a large-scale analysis of evolutionary transitions in amphibian antipredation coloration and demonstrate that the evolutionary transition from camouflage to aposematism is rarely direct but tends to involve an intermediary stage, namely cryptic species that facultatively reveal conspicuous coloration. Accounting for this intermediate step can resolve the paradox and thereby advance our understanding of the evolution of aposematism.

Outstanding issues in the study of antipredator defenses

“…Both deimatic behavior and aposematism can utilize bright coloration; indeed, deimatism may be an evolutionary precursor of aposematism (Loeffler‐Henry et al., 2023). For example, the long exposure of the conspicuous ventrum of several amphibian species upon disturbance has been historically thought of as aposematism (Wells, 2007) but is now being considered as deimatic behavior (Chiocchio et al., 2023).…”

Evolution of multiple prey defences: From predator cognition to community ecology

“…Other prey animals deploy their multiple defensive traits either sequentially or simultaneously during the predation sequence, as a system of barriers that predators must breach before prey subjugation and consumption (Riley et al, 2022, Ruxton et al, 2018). For example, many amphibian species rely primarily on camouflage to avoid detection and expose their warning coloration to predators only after encounter (Loeffler‐Henry et al, 2023). The same colour patterns can also be effective for camouflage when viewed from a distance, and at the same time act as conspicuous warning coloration close up (Barnett et al, 2017; Tullberg et al, 2005).…”

“…The evolution of antipredator defences cannot be understood without applying a broader comparative approach and considering the defences of a particular prey species in the context of prey and predator communities. Application of phylogenetic comparative methods allows for reconstructing the evolution of defensive traits in given animal taxa (Loeffler‐Henry et al, 2023; Motyka et al, 2021) and testing hypotheses about correlated evolution among multiple defensive traits and between defences and other aspects of species biology. For instance, the results of comparative phylogenetic analysis support the relationship between prey body size and the evolution of various antipredator defences including eyespots (Hossie et al, 2015) and hidden colour signals (Loeffler‐Henry et al, 2019).…”

“…Other prey animals deploy their multiple defensive traits either sequentially or simultaneously during the predation sequence, as a system of barriers that predators must breach before prey subjugation and consumption (Riley et al, 2022, Ruxton et al, 2018. For example, many amphibianspeciesrelyprimarily on camouflagetoavoiddetectionandexposetheirwarningcolorationtopredatorsonlyafter encounter (Loeffler-Henry et al, 2023). The same colour patterns canalsobeeffectiveforcamouflagewhenviewedfromadistance, andatthesametimeactasconspicuouswarningcolorationcloseup (Barnettetal.,2017;Tullbergetal.,2005).Thediversityofmultiple defencesmaybefurtherincreasedbyintraspecificvariationandontogeneticchangesindefencestrategies (Barnettetal.,2022,Rönkä etal.,2020.Multipledefencesmightalsotargetalternativetypesof predators (Raškaetal.,2023;Rojasetal.,2017)…”

Why are vertebrates so big?

“…Numerous adaptations have arisen that act to reduce mortality in early life stages, thereby permitting a slower pace of life. Parental care, toxicity, armour and camouflage have all evolved in response to predation pressure to increase juvenile survival rates (Caro, 2005; Gross, 2005; Kats et al, 1988; Loeffler‐Henry et al, 2023). With predation curtailed in this way, life‐history optima shift, natural selection favours delaying maturity, affording more time to grow compared with conspecifics and reaping the rewards of larger adult body sizes.…”