Predator learning favours mimicry of a less-toxic model in poison frogs

Abstract

1 . Mimetic advantage is considered to be dependent on frequency because an increase in mimic abundance leads to breakdown of the warning signal 2,3 . Where multiple toxic species are available, batesian polymorphism 4 is predicted-that is, mimics diversify to match sympatric models. Despite the prevalence of batesian mimicry in nature 5 , batesian polymorphism is relatively rare 6 . Here we explore a poison-frog mimicry complex comprising two parapatric models and a geographically dimorphic mimic that shows monomorphism where models co-occur. Contrary to classical predictions, our toxicity assays, field observations and spectral reflectances show that mimics resemble the less-toxic and less-abundant model. We examine "stimulus generalization" 7 as a mechanism for this nonintuitive result with learning experiments using naive avian predators and live poison frogs. We find that predators differ in avoidance generalization depending on toxicity of the model, conferring greater protection to mimics resembling the lesstoxic model owing to overlap of generalized avoidance curves. Our work supports a mechanism of toxicity-dependent stimulus generalization 8 , revealing an additional solution for batesian mimicry where multiple models coexist.In batesian mimicry, an edible species co-opts a warning signal from an unpalatable species to gain advantage through predator deception 1 . If batesian mimics are too common, however, this advantage breaks down as predators learn to ignore the warning signal. Where more than one model species is available 4 , diversifying frequency-dependent selection predicts the evolution of polymorphism in which mimics diverge in appearance to resemble sympatric models 6,9,10 . Batesian polymorphism is suggested to distribute warning signal degradation over several defended model species, enabling the mimic to increase in abundance. Reported accounts of such mimetic polymorphism, however, are relatively rare 6 and unknown in vertebrate mimicry systems 11,12 .Here we investigate a mimicry system that is inconsistent with the predictions of frequency dependence. We examine a poison-frog mimicry complex composed of two parapatric models and a geographically varying mimic (Fig. 1). The model Ecuadorian poison frogs Epipedobates bilinguis and Epipedobates parvulus share a similar warning signal of a bright red-spotted dorsum but differ in axilla and groin colouration (Fig. 1b). Their phylogenetically distant relative 13 , Allobates zaparo, is geographically dimorphic, matching each warning signal where models are parapatric (Fig. 1b). Where the two models co-occur, however, the mimic resembles only a single model (E. bilinguis; Figs 1 and 2). Here we use spectral reflectances, toxicity assays, field abundance measurements and predator learning experiments to investigate mechanisms that may be contributing to this pattern in nature.Theoretical and empirical studies predict that coexistence of aposematic models may lead to (1) batesian polymorphism 6,9,10 , (2) evolution of a mimic phenotype intermed...

A Müllerian mimicry ring in Appalachian millipedes

“…Under these circumstances, a strongly positive, density-driven signal effect (density-dependent generalized avoidance, ref. 24; or another type of Allee effect refs. 25 and 26) may grant novel color morphs a higher likelihood of survival, enabling exploration of an adaptive landscape otherwise made inaccessible by purifying selection.…”

Does spatial variation in predation pressure modulate selection for aposematism?

“…Birds use bitterness to estimate the level of toxicity (Skelhorn & Rowe, 2010), and cardenolides are bitter in taste (Malcolm, 1994). The level of toxicity correlates with the taste and birds learn to reject highly distasteful prey faster than less distasteful prey (Holen, 2013), and moderately toxic species are favored over highly toxic species in learning (Darst & Cummings, 2006). However, once learned, birds avoid prey types that are likely above certain level of toxicity or bitterness (Lindström, Lyytinen, Mappes, & Ojala, 2006).…”

A Predator's Perspective of the Accuracy of Ant Mimicry in Spiders

“…The negative effect on models is due to frequency-dependent selection: if mimics exist in large numbers, the predators may take longer to learn an aversion or the potential for evolving innate fear of dangerous prey is lessened. Although studies of the Batesian mimicry have usually emphasised learning as a mechanism for the evolution of mimicry (e.g., [3]), both innate and learned fear of dangerous or distasteful prey can favour the evolution of the Batesian mimicry, as is clear from studies using naïve jumping spiders (Salticidae) as potential predators (e.g., [4]). …”

“…Yet polymorphism can also be maintained in populations of the Batesian mimics [17], particularly when more than one model species is available [3]. It is especially noticeable that several species of ant mimics are polymorphic [18,19].…”

“…While we traditionally think of dangerous prey as one using bright, contrasting colours as aposematic signals, as in the case of poison dart frogs [3], not all dangerous species that are mimicked use aposematic signals. Correspondingly, deceitful use of aposematic signals appears to be an evolutionary strategy used by some Batesian mimics, but not others.…”