Does predation maintain eyespot plasticity in Bicyclus anynana?

The butterfly Bicyclus anynana exhibits phenotypic plasticity involving the wet-season phenotype, which possesses marginal eyespots on the ventral surface of the wings, and the dry-season form, which lacks these eyespots. We examined the adaptive value of phenotypic plasticity of B. anynana in relation to the defence mechanisms of crypsis and deflection. We assessed the visibility differences between spotless and spotted butterflies against backgrounds of brown (dry season) or green (wet season) leaves. Spotless butterflies were highly cryptic and less predated by adult bird predators than were spotted ones when presented against brown leaf litter. However, the advantage of crypsis disappeared in the wet-season habitat as both forms were equally visible. In later experiments, naive birds presented with resting butterflies in the wet-season habitat tended to learn more rapidly to capture spotless butterflies, suggesting a slight selective advantage of possessing eyespots. Moreover, marginal eyespots increased significantly the escape probability of butterflies that were attacked by naive birds compared to those attacked by adult birds, although there were no differences in prey capture success within naive predators. Our results show that natural selection acts against eyespots in the dry season, favouring crypsis, whereas in the wet season it may favour eyespots as deflective patterns.

Lyytinen A ，Brakefield PM ，Lindström L ，Mappes J ... -  《-》

Eyespots deflect predator attack increasing fitness and promoting the evolution of phenotypic plasticity.

Some eyespots are thought to deflect attack away from the vulnerable body, yet there is limited empirical evidence for this function and its adaptive advantage. Here, we demonstrate the conspicuous ventral hindwing eyespots found on Bicyclus anynana butterflies protect against invertebrate predators, specifically praying mantids. Wet season (WS) butterflies with larger, brighter eyespots were easier for mantids to detect, but more difficult to capture compared to dry season (DS) butterflies with small, dull eyespots. Mantids attacked the wing eyespots of WS butterflies more frequently resulting in greater butterfly survival and reproductive success. With a reciprocal eyespot transplant, we demonstrated the fitness benefits of eyespots were independent of butterfly behaviour. Regardless of whether the butterfly was WS or DS, large marginal eyespots pasted on the hindwings increased butterfly survival and successful oviposition during predation encounters. In previous studies, DS B. anynana experienced delayed detection by vertebrate predators, but both forms suffered low survival once detected. Our results suggest predator abundance, identity and phenology may all be important selective forces for B. anynana. Thus, reciprocal selection between invertebrate and vertebrate predators across seasons may contribute to the evolution of the B. anynana polyphenism.

Prudic KL ，Stoehr AM ，Wasik BR ，Monteiro A ... -  《-》

Origin of the mechanism of phenotypic plasticity in satyrid butterfly eyespots.

Plasticity is often regarded as a derived adaptation to help organisms survive in variable but predictable environments, however, we currently lack a rigorous, mechanistic examination of how plasticity evolves in a large comparative framework. Here, we show that phenotypic plasticity in eyespot size in response to environmental temperature observed in atyrid butterflies is a complex derived adaptation of this lineage. By reconstructing the evolution of known physiological and molecular components of eyespot size plasticity in a comparative framework, we showed that 20E titer plasticity in response to temperature is a pre-adaptation shared by all butterfly species examined, whereas expression of EcR in eyespot centers, and eyespot sensitivity to 20E, are both derived traits found only in a subset of species with eyespots.

Bhardwaj S ，Jolander LS ，Wenk MR ，Oliver JC ，Nijhout HF ，Monteiro A ... -  《eLife》

Predation favours Bicyclus anynana butterflies with fewer forewing eyespots.

There are fewer eyespots on the forewings versus hindwings of nymphalids but the reasons for this uneven distribution remain unclear. One possibility is that, in many butterflies, the hindwing covers part of the ventral forewing at rest and there are fewer forewing sectors to display eyespots (covered eyespots are not continuously visible and are less likely to be under positive selection). A second explanation is that having fewer forewing eyespots confers a selective advantage against predators. We analysed wing overlap at rest in 275 nymphalid species with eyespots and found that many have exposed forewing sectors without eyespots: i.e. wing overlap does not constrain the forewing from having the same number or more eyespots than the hindwing. We performed two predation experiments with mantids to compare the relative fitness of and attack damage patterns on two forms of butterflies, both with seven hindwing eyespots, but with two (in wild-type) or four (in Spotty) ventral forewing eyespots. Spotty experienced more intense predation on the forewings, were shorter-lived and laid fewer eggs. These results suggest that predation pressure limits forewing eyespot number in . This may occur if attacks on forewing eyespots have more detrimental consequences for flight than attacks on hindwing eyespots.

Chan IZW ，Ngan ZC ，Naing L ，Lee Y ，Gowri V ，Monteiro A ... -  《-》

Female choice depends on size but not symmetry of dorsal eyespots in the butterfly Bicyclus anynana.

The eyespots on the ventral wings of Bicyclus anynana butterflies are exposed when at rest and interact with predators. Those on the dorsal surface are not exposed in this way, and may be involved in courtship and mate choice. In this study, we examined whether the size and fluctuating asymmetry (FA) of dorsal eyespots are reliable signals of male quality. High developmental stability is considered to result in low FA, and to be associated with high quality. Individuals of high quality are predicted to produce sexually selected traits that are large and symmetrical, at a relatively low cost. In this study, we manipulated eyespot development to uncouple eyespot size and FA in order to examine their independent roles in signalling to the female. Individual females in cages were given the choice between two or three males differing in eyespot traits. The results indicate that although size per se of the eyespots is used as a signal, FA and wing size are not. We discuss the use of FA in studies of sexual selection and aspects of sexual selection on dorsal eyespot size.

Breuker CJ ，Brakefield PM 《-》