Mimicry can drive convergence in structural and light transmission features of transparent wings in Lepidoptera

Müllerian mimicry is a positive interspecific interaction, whereby co-occurring defended prey species share a common aposematic signal. In Lepidoptera, aposematic species typically harbour conspicuous opaque wing colour patterns with convergent optical properties among co-mimetic species. Surprisingly, some aposematic mimetic species have partially transparent wings, raising the questions of whether optical properties of transparent patches are also convergent, and of how transparency is achieved. Here, we conducted a comparative study of wing optics, micro and nanostructures in neotropical mimetic clearwing Lepidoptera, using spectrophotometry and microscopy imaging. We show that transparency, as perceived by predators, is convergent among co-mimics in some mimicry rings. Underlying micro- and nanostructures are also sometimes convergent despite a large structural diversity. We reveal that while transparency is primarily produced by microstructure modifications, nanostructures largely influence light transmission, potentially enabling additional fine-tuning in transmission properties. This study shows that transparency might not only enable camouflage but can also be part of aposematic signals.

Lack of neophobic responses to color in a jumping spider that uses color cues when foraging (Habronattus pyrrithrix)

Chemically defended prey often advertise their toxins with bright and conspicuous colors. To understand why such colors are effective at reducing predation, we need to understand the psychology of key predators. In bird predators, there is evidence that individuals avoid novelty—including prey of novel colors (with which they have had no prior experience). Moreover, the effect of novelty is sometimes strongest for colors that are typically associated with aposematic prey (e.g., red, orange, yellow). Given these findings in the bird literature, color neophobia has been argued to be a driving force in the evolution of aposematism. However, no studies have yet asked whether invertebrate predators respond similarly to novel colors. Here, we tested whether naive lab-raised jumping spiders (Habronattus pyrrithrix) exhibit similar patterns of color neophobia to birds. Using color-manipulated living prey, we first color-exposed spiders to prey of two out of three colors (blue, green, or red), with the third color remaining novel. After this color exposure phase, we gave the spiders tests where they could choose between all three colors (two familiar, one novel). We found that H. pyrrithrix attacked novel and familiar-colored prey at equal rates with no evidence that the degree of neophobia varied by color. Moreover, we found no evidence that either prey novelty nor color (nor their interaction) had an effect on how quickly prey was attacked. We discuss these findings in the context of what is known about color neophobia in other animals and how this contributes to our understanding of aposematic signals.

Variable utility in the enigmatic presence of ultraviolet reflectance in conspicuous aposematic signals

Warning signals are often characterized by highly contrasting, distinctive and memorable colors. Both chromatic (hue) and achromatic (brightness) contrast contribute to signal efficacy, making longwave colored signals (red and yellow) that generate both chromatic and achromatic contrast common. Shortwave colors (blue and ultraviolet) do not contribute to luminance perception, yet are also common in warning signals. The presence of UV aposematic signals is paradoxical as UV perception is not universal, and evidence for its utility is at best mixed. We used visual modeling to quantify how UV affects signal contrast in aposematic butterflies and frogs. We found that UV only appreciably affected visual contrast in the butterflies. As the butterflies, but not the frogs, have UV-sensitive vision these results support the notion that UV reflectance is associated with intraspecific communication, but appears to be non-functional in frogs. Consequently, we should be careful when assigning a selection-based benefit from UV reflectance.

Meta-analytic evidence for quantitative honesty in aposematic signals

The combined use of noxious chemical defences and conspicuous warning colours is a ubiquitous anti-predator strategy. That such signals advertise the presence of defences is inherent to their function, but their predicted potential for quantitative honesty—the positive scaling of signal salience with the strength of protection—is the subject of enduring debate. Here, we systematically synthesized the available evidence to test this prediction using meta-analysis. We found evidence for a positive correlation between warning colour expression and the extent of chemical defences across taxa. Notably, this relationship held at all scales; among individuals, populations and species, though substantial between-study heterogeneity remains unexplained. Consideration of the design of signals revealed that all visual features, from colour to contrast, were equally informative of the extent of prey defence. Our results affirm a central prediction of honesty-based models of signal function and narrow the scope of possible mechanisms shaping the evolution of aposematism. They suggest diverse pathways to the encoding and exchange of information, while highlighting the need for deeper knowledge of the ecology of chemical defences to enrich our understanding of this widespread anti-predator adaptation.

The limits of evolutionary convergence in sympatry: reproductive interference and developmental constraints leading to local diversity in aposematic signals

ABSTRACTMutualistic interaction between defended species is a striking case of evolutionary convergence in sympatry, driven by the increased protection against predators brought by mimicry. However, such convergence is often limited: sympatric defended species frequently display different or imperfectly similar warning traits. The phylogenetic distance between sympatric species may indeed prevent evolution towards the exact same signal. Moreover, warning traits are also implied in mate recognition, so that trait convergence might result in heterospecific courtship and mating. Here, we investigate the strength and direction of convergence in warning trait in defended species with different ancestral traits, using a mathematical model. We specifically determine the effect of phenotypic distances among ancestral traits of converging species, and costs of heterospecific sexual interactions on imperfect mimicry and trait divergence. Our analytical results confirm that reproductive interference limits the convergence of warning trait, leading to either imperfect mimicry or complete divergence. More surprisingly, our model pinpoints that reproductive interference can change the direction of convergence depending on the relative species densities. We also show that reproductive interference can generate imperfect mimicry only between species with different ancestral traits. Our model therefore highlights that convergence triggered by Müllerian mimicry not only depends on relative defence levels, but that relative species densities, heterospecific sexual interactions and ancestral traits interfere in the direction and strength of convergence between species.

Prey with hidden colour defences benefit from their similarity to aposematic signals

Some camouflaged animals hide colour signals and display them only transiently. These hidden colour signals are often conspicuous and are used as a secondary defence to warn or startle predators (deimatic displays) and/or to confuse them (flash displays). The hidden signals used in these displays frequently resemble typical aposematic signals, so it is possible that prey with hidden signals have evolved to employ colour patterns of a form that predators have previously learned to associate with unprofitability. Here, we tested this hypothesis by conducting two experiments that examined the effect of predator avoidance learning on the efficacy of deimatic and flash displays. We found that the survival benefits of both deimatic and flash displays were substantially higher against predators that had previously learned to associate the hidden colours with unprofitability than against naive predators. These findings help explain the phenological patterns we found in 1568 macro-lepidopteran species on three continents: species with hidden signals tend to occur later in the season than species without hidden signals.

Convergence in light transmission properties of transparent wing areas in clearwing mimetic butterflies

Müllerian mimicry is a positive interspecific interaction, whereby co-occurring defended prey species share a common aposematic signal that advertises their defences to predators. In Lepidoptera, aposematic species typically harbour conspicuous opaque wing colour pattern, which have convergent optical properties, as perceived by predators. Surprisingly, some aposematic mimetic species have partially or totally transparent wings, which raises the question of whether optical properties of such transparent areas are also under selection for convergence. To answer this question and to investigate how transparency is achieved in the first place, we conducted a comparative study of optics and structures of transparent wings in neotropical mimetic clearwing Lepidoptera. We quantified transparency by spectrophotometry and characterised clearwing microstructures and nanostructures by microscopy imaging. We show that transparency is convergent among co-mimics in the eyes of predators, despite a large diversity of underlying micro- and nanostructures. Notably, we reveal that nanostructure density largely influences light transmission. While transparency is primarily produced by modification of microstructure features, nanostructures may provide a way to fine-tune the degree of transparency. This study calls for a change of paradigm in transparent mimetic lepidoptera: transparency not only enables camouflage but can also be part of aposematic signals.SignificanceTransparency in animals has long been associated to camouflage, but the existence of aposematic mimetic Lepidoptera with partly transparent wings raises the question of the role of transparency in aposematism. Here, we undertake the first comparative analysis of transparency features in mimetic Lepidoptera. We show that transparency is likely part of the aposematic signal, as light transmission properties are convergent among co-mimics. We also reveal a high diversity of wing structures (scales and wing membrane nanostructures) underlying transparency, which enables fine-tuning the degree of transparency. This study, at the interface between physical optics and evolutionary biology, sheds light on the evolution of transparency in aposematic mimetic lineages and may promote bioinspired applications for transparent materials such as antireflective devices.

Evolution of switchable aposematism: insights from individual-based simulations

Some defended prey animals can switch on their normally hidden aposematic signals. This switching may occur in reaction to predators’ approach (pre-attack signals) or attack (post-attack signals). Switchable aposematism has been relatively poorly studied, but we can expect that it might bring a variety of benefits to an aposmetic organism. First, the switching could startle the predators (deimatism). Second, it could facilitate aversive learning. Third, it could minimize exposure or energetic expense, as the signal can be switched off. These potential benefits might offset costs of developing, maintaining and utilizing the switchable traits. Here we focused on the third benefit of switchability, the cost-saving aspect, and developed an individual-based computer simulation of predators and prey. In 88,128 model runs, we observed evolution of permanent, pre-attack, or post-attack aposematic signals of varying strength. We found that, in general, the pre-attack switchable aposematism may require moderate predator learning speed, high basal detectability, and moderate to high signal cost. On the other hand, the post-attack signals may arise under slow predator learning, low basal detectability and high signal cost. When predator population turnover is fast, it may lead to evolution of post-attack aposematic signals that are not conforming to the above tendency. We also suggest that a high switching cost may exert different selection pressure on the pre-attack than the post-attack switchable strategies. To our knowledge, these are the first theoretical attempts to systematically explore the evolution of switchable aposematism relative to permanent aposematism in defended prey. Our simulation model is capable of addressing additional questions beyond the scope of this article, and we open the simulation software, program manual and source code for free public use.