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Wood tiger moth morph frequencies compared to expected and observed predation risk and selection differential by country. (a) Local morph frequencies calculated from annual monitoring data, (b) expected attack risk according to the + FDS hypothesis, where each morph is attacked according to its local frequency, (c) observed predation illustrated as GLMM estimates of daily attack risk for each morph by country and (d) observed difference in attacks per morph compared to a situation where all morphs would be attacked equally. Morph colours (white, yellow, red) as in Figure 1.

Wood tiger moth morph frequencies compared to expected and observed predation risk and selection differential by country. (a) Local morph frequencies calculated from annual monitoring data, (b) expected attack risk according to the + FDS hypothesis, where each morph is attacked according to its local frequency, (c) observed predation illustrated as GLMM estimates of daily attack risk for each morph by country and (d) observed difference in attacks per morph compared to a situation where all morphs would be attacked equally. Morph colours (white, yellow, red) as in Figure 1.

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Article
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Warning signals are predicted to develop signal monomorphism via positive frequency‐dependent selection (+FDS) albeit many aposematic systems exhibit signal polymorphism. To understand this mismatch, we conducted a large‐scale predation experiment in four countries, among which the frequencies of hindwing warning coloration of the aposematic moth,...

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... Yellow morphs have stronger chemical defences (Rojas et al., 2017), 71 but show reduced flight activity compared to white males, although yellows may fly at more 72 selective times, i.e. at peak female calling periods (Rojas, Gordon and Mappes, 2015). In 73 summary, there is a trade-off between natural selection through predation and reproductive 74 success, which contributes to the maintenance of this polymorphism (Rönkä et al., 2020). 75 ...
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Colour is often used as an aposematic warning signal, with predator learning expected to lead to a single colour pattern within a population. However, there are many puzzling cases where aposematic signals are also polymorphic. The wood tiger moth, Arctia plantaginis , uses bright hindwing colours as a signal of unpalatability, and males have discrete colour morphs which vary in frequency geographically. In Finland, both white and yellow morphs can be found, and these colour morphs also differ in behavioural and life-history traits. Complex polymorphisms such as these are often explained by supergenes. Here, we show that male colour is linked to an extra copy of a yellow family gene that is only present in the white morphs. This white-specific duplication, which we name valkea , is highly upregulated during wing development, and could act to reduce recombination, thus potentially representing a supergene. We also characterise the pigments responsible for yellow, white and black colouration, showing that yellow is partly produced by pheomelanins, while black is dopamine-derived eumelanin. The yellow family genes have been linked to melanin synthesis and behavioural traits in other insect species. Our results add to only a few examples of seemingly paradoxical and complex polymorphisms which are associated with single genes.
... From an evolutionary standpoint, it is plausible that interplay between natural and sexual selection facilitates polymorphism in this species (Gordon et al., 2015Nokelainen et al., 2012;Rönkä et al., 2020). Since male wood tiger moths, which are actively searching for females in the vegetation, have limited ability to see differences in yellow-orange-red hues (Henze et al., 2018), it is unlikely that sexual selection alone would be responsible for the colouration of females, but we cannot exclude the possibility that male colouration could be used in intraspecific commu- For tetrachromatic avian vision uv, sw and lw sensitivities were used for blue, green and red channels respectively. ...
... Also, avian predators may distinguish between the nuances in colouration among the genotypes as they, and wood tiger moths, perceive UV wavelengths that are beyond human perception (Henze et al., 2018). Thus, ecologically relevant receivers, predators and conspecifics, may exert different selection pressures on visual signals beyond our perception (Endler, 1978) and maintain colour polymorphism in natural conditions (Galarza et al., 2014;Mochida, 2011;Nokelainen et al., 2014;Rönkä et al., 2020). ...
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Phenotypic variation is suggested to facilitate the persistence of environmentally growing pathogens under environmental change. Here we hypothesized that the intensive farming environment induces higher phenotypic variation in microbial pathogens than natural environment, because of high stochasticity for growth and stronger survival selection compared to the natural environment. We tested the hypothesis with an opportunistic fish pathogen Flavobacterium columnare isolated either from fish farms or from natural waters. We measured growth parameters of two morphotypes from all isolates in different resource concentrations and two temperatures relevant for the occurrence of disease epidemics at farms and tested their virulence using a zebrafish (Danio rerio) infection model. According to our hypothesis, isolates originating from the fish farms had higher phenotypic variation in growth between the morphotypes than the isolates from natural waters. The difference was more pronounced in higher resource concentrations and the higher temperature, suggesting that phenotypic variation is driven by the exploitation of increased outside‐host resources at farms. Phenotypic variation of virulence was not observed based on isolate origin but only based on morphotype. However, when in contact with the larger fish, the less virulent morphotype of some of the isolates also had high virulence. As the less virulent morphotype also had higher growth rate in outside‐host resources, the results suggest that both morphotypes can contribute to F. columnare epidemics at fish farms, especially with current prospects of warming temperatures. Our results suggest that higher phenotypic variation per se does not lead to higher virulence, but that environmental conditions at fish farms could select isolates with high phenotypic variation in bacterial population and hence affect evolution in F. columnare at fish farms. Our results highlight the multifaceted effects of human‐induced environmental alterations in shaping epidemiology and evolution in microbial pathogens.
... From an evolutionary standpoint, it is plausible that interplay between natural and sexual selection facilitates polymorphism in this species (Gordon et al., 2015Nokelainen et al., 2012;Rönkä et al., 2020). Since male wood tiger moths, which are actively searching for females in the vegetation, have limited ability to see differences in yellow-orange-red hues (Henze et al., 2018), it is unlikely that sexual selection alone would be responsible for the colouration of females, but we cannot exclude the possibility that male colouration could be used in intraspecific commu- For tetrachromatic avian vision uv, sw and lw sensitivities were used for blue, green and red channels respectively. ...
... Also, avian predators may distinguish between the nuances in colouration among the genotypes as they, and wood tiger moths, perceive UV wavelengths that are beyond human perception (Henze et al., 2018). Thus, ecologically relevant receivers, predators and conspecifics, may exert different selection pressures on visual signals beyond our perception (Endler, 1978) and maintain colour polymorphism in natural conditions (Galarza et al., 2014;Mochida, 2011;Nokelainen et al., 2014;Rönkä et al., 2020). ...
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The definition of colour polymorphism is intuitive: genetic variants express discretely coloured phenotypes. This classification is, however, elusive as humans form subjective categories or ignore differences that cannot be seen by human eyes. We demonstrate an example of a 'cryptic morph' in a polymorphic wood tiger moth (Arctia plantaginis), a phenomenon that may be common among well-studied species. We used pedigree data from nearly 20,000 individuals to infer the inheritance of hindwing colouration. The evidence supports a single Mendelian locus with two alleles in males: WW and Wy produce the white and yy the yellow hindwing colour. The inheritance could not be resolved in females as their hindwing colour varies continuously with no clear link with male genotypes. Next, we investigated if the male genotype can be predicted from their phenotype by machine learning algorithms and by human observers. Linear discriminant analysis grouped male genotypes with 97% accuracy, whereas humans could only group the yy genotype. Using vision modelling, we also tested whether the genotypes have differential discriminability to humans, moth conspecifics and their bird predators. The human perception was poor separating the genotypes, but avian and moth vision models with ultraviolet sensitivity could separate white WW and Wy males. We emphasize the importance of objective methodology when studying colour polymorphism. Our findings indicate that by-eye categorization methods may be problematic, because humans fail to see differences that can be visible for relevant receivers. Ultimately, receivers equipped with different perception than ours may impose selection to morphs hidden from human sight.
... Additional experiments are needed to determine the interactive effects of predator's generalization, larval group size, larval defensive displays, and color. To assess whether predation risk for yellow-and white-bodied larvae varies among N. lecontei populations, future research should also test for differences in the survival of white-and yellow-bodied larvae across their geographical range and across different visual backgrounds (Rojas et al. 2014;Rönkä et al. 2020). ...
... Thus, rather than strong top-down selection by predators and pathogens, bottom-up selection via host-plant characteristics may have driven shifts in warning color among N. lecontei populations. This finding contrasts with strong top-down selection pressures that may explain endogenously produced polymorphic and polytypic warning color in Arctia plantaginis (Rönkä et al. 2020) and polytypic warning color in Heliconius melpomene. Historical demographic analyses suggest that H. melpomene radiated into areas already occupied by another, more abundant aposematic species, H. erato (e.g., Turner et al. 1996;Mallet and Joron 1999;Kronforst and Gilbert 2008;Quek et al. 2010). ...
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Our understanding of how novel warning color traits evolve in natural populations is largely based on studies of reproductive stages and organisms with endogenously produced pigmentation. In these systems, genetic drift is often required for novel alleles to overcome strong purifying selection stemming from frequency‐dependent predation and positive assortative mating. Here, we integrate data from field surveys, predation experiments, population genomics, and phenotypic correlations to explain the origin and maintenance of geographic variation in a diet‐based larval pigmentation trait in the redheaded pine sawfly (Neodiprion lecontei), a pine‐feeding hymenopteran. Although our experiments confirm that N. lecontei larvae are indeed aposematic—and therefore likely to experience frequency‐dependent predation—our genomic data do not support a historical demographic scenario that would have facilitated the spread of an initially deleterious allele via drift. Additionally, significantly elevated differentiation at a known color locus suggests that geographic variation in larval color is currently maintained by selection. Together, these data suggest that the novel white morph likely spread via selection. However, white body color does not enhance aposematic displays, nor is it correlated with enhanced chemical defense or immune function. Instead, the derived white‐bodied morph is disproportionately abundant on a pine species with a reduced carotenoid content relative to other pine hosts, suggesting that bottom‐up selection via host plants may have driven divergence among populations. Overall, our results suggest that life stage and pigment source can have a substantial impact the evolution of novel warning signals, highlighting the need to investigate diverse aposematic taxa to develop a comprehensive understanding of color variation in nature. This article is protected by copyright. All rights reserved
... A geographic mosaic theory of coevolution (Thompson 1999) can predict that heterogeneous predator selection may facilitate multiple prey appearances (Rönkä et al. 2020). With this respect, variable light conditions have been identified as a potential source of heterogeneous selection that could result in the emergence of such phenotype variation (Rojas et al. 2014;Tate et al. 2016;Passarotto et al. 2018;Kranz et al. 2018). ...
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A big question in behavioral ecology is what drives diversity of color signals. One possible explanation is that environmental conditions, such as light environment, may alter visual signaling of prey, which could affect predator decision-making. Here, we tested the context-dependent predator selection on prey coloration. In the first experiment, we tested detectability of artificial visual stimuli to blue tits (Cyanistes caeruleus) by manipulating stimulus luminance and chromatic context of the background. We expected the presence of the chromatic context to facilitate faster target detection. As expected, blue tits found targets on chromatic yellow background faster than on achromatic grey background whereas in the latter, targets were found with smaller contrast differences to the background. In the second experiment, we tested the effect of two light environments on the survival of aposematic, color polymorphic wood tiger moth (Arctia plantaginis). As luminance contrast should be more detectable than chromatic contrast in low light intensities, we expected birds, if they find the moths aversive, to avoid the white morph which is more conspicuous than the yellow morph in low light (and vice versa in bright light). Alternatively, birds may attack first moths that are more detectable. We found birds to attack yellow moths first in low light conditions, whereas white moths were attacked first more frequently in bright light conditions. Our results show that light environments affect predator foraging decisions, which may facilitate context-dependent selection on visual signals and diversity of prey phenotypes in the wild.
... Therea are also differences between genotypes in the white hue of the forewings, which is perceptible to birds (Nokelainen et al., in prep a). The color polymorphism is under selection by bird predators in the wild (Rönkä et al., 2020). In predation experiments, birds respond differently toward the hindwing morphs, avoiding either yellow (Nokelainen et al., 2012(Nokelainen et al., , 2014 or white , but see Rönkä et al. (2018). ...
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Aposematic organisms warn predators of their unprofitability using a combination of defenses, including visual warning signals, startling sounds, noxious odors, or aversive tastes. Using multiple lines of defense can help prey avoid predators by stimulating multiple senses and/or by acting at different stages of predation. We tested the efficacy of three lines of defense (color, smell, taste) during the predation sequence of aposematic wood tiger moths ( Arctia plantaginis ) using blue tit ( Cyanistes caeruleus ) predators. Moths with two hindwing phenotypes (genotypes: WW/Wy = white, yy = yellow) were manipulated to have defense fluid with aversive smell (methoxypyrazines), body tissues with aversive taste (pyrrolizidine alkaloids) or both. In early predation stages, moth color and smell had additive effects on bird approach latency and dropping the prey, with the strongest effect for moths of the white morph with defense fluids. Pyrrolizidine alkaloid sequestration was detrimental in early attack stages, suggesting a trade-off between pyrrolizidine alkaloid sequestration and investment in other defenses. In addition, pyrrolizidine alkaloid taste alone did not deter bird predators. Birds could only effectively discriminate toxic moths from non-toxic moths when neck fluids containing methoxypyrazines were present, at which point they abandoned attack at the consumption stage. As a result, moths of the white morph with an aversive methoxypyrazine smell and moths in the treatment with both chemical defenses had the greatest chance of survival. We suggest that methoxypyrazines act as context setting signals for warning colors and as attention alerting or “go-slow” signals for distasteful toxins, thereby mediating the relationship between warning signal and toxicity. Furthermore, we found that moths that were heterozygous for hindwing coloration had more effective defense fluids compared to other genotypes in terms of delaying approach and reducing the latency to drop the moth, suggesting a genetic link between coloration and defense that could help to explain the color polymorphism. Conclusively, these results indicate that color, smell, and taste constitute a multimodal warning signal that impedes predator attack and improves prey survival. This work highlights the importance of understanding the separate roles of color, smell and taste through the predation sequence and also within-species variation in chemical defenses.
... Whilst aposematism is taxonomically widespread, we focussed on how the colour patterns of Lepidoptera stimulate the visual systems of birds. This is a well-established model system for the study of defensive strategies, particularly aposematism and crypsis [20][21][22] , and where the visual system of the predator is also relatively well understood 23 . From an initial literature search (see Methods for details), we built a representative database of 125 species of Lepidoptera for our analysis (96 aposematic and 29 non-aposematic species). ...
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Animal warning signals show remarkable diversity, yet subjectively appear to share visual features that make defended prey stand out and look different from more cryptic palatable species. Here we develop and apply a computational model that emulates avian visual processing of pattern and colour to Lepidopteran wing patterns to show that warning signals have specific neural signatures that set them apart not only from the patterns of undefended species but also from natural scenes. For the first time, we offer an objective and quantitative neural-level definition of warning signals based on how the pattern generates neural activity in the brain of the receiver. This opens new perspectives for understanding and testing how warning signals function and evolve, and, more generally, how sensory systems constrain general principles for signal design.
... An anecdote from the field aligns with this conclusion: in a study attempting to quantify predation on artificial grasshoppers, no desert clicker models were disturbed on plant stems but a model inadvertently left on the ground suffered an unambiguous rodent attack (Fig S2.11). Additional sources of unexplained variance may include geographic turnover in predator communities (e.g., Rönkä et al. 2020) or tradeoffs between crypsis and thermoregulation (e.g., Forsman 2018). ...
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Color polymorphic species can offer exceptional insight into the ecology and genetics of adaptation. Although the genetic architecture of animal coloration is diverse, many color polymorphisms are associated with large structural variants and maintained by biotic interactions. Grasshoppers are notably polymorphic in both color and karyotype, making them excellent models for understanding the ecological drivers and genetic underpinnings of color variation. Banded and uniform morphs of the desert clicker grasshopper (Ligurotettix coquilletti) are found across the western deserts of North America. To address the hypothesis that predation maintains local color polymorphism and shapes regional crypsis variation, we surveyed morph frequencies and tested for covariation with two predation environments. Morphs coexisted at intermediate frequencies at most sites, consistent with local balancing selection. Morph frequencies covaried with the appearance of desert substrate – an environment used only by females – suggesting that ground-foraging predators are major agents of selection on crypsis. We next addressed the hypothesized link between morph variation and genome structure. To do so, we designed an approach for detecting inversions and indels using only RADseq data. The banded morph was perfectly correlated with a large putative indel. Remarkably, indel dominance differed among populations, a rare example of dominance evolution in nature. This article is protected by copyright. All rights reserved
... ; model suffered an unambiguous rodent attack when left on the ground , but no such models were attacked on plant stems (Fig S2.10). Additional sources of unexplained variance may include geographic turnover in predator communities (e.g., Rönkä et al. 2020) or tradeoffs between crypsis and thermoregulation (e.g., Forsman 2018). ...
Preprint
Full-text available
Color polymorphic species can offer exceptional insight into the ecology and genetics of adaptation. Although the genetic architecture of animal coloration is diverse, many color polymorphisms are associated with large structural variants and maintained by biotic interactions. Grasshoppers are exceptionally polymorphic in both color and karyotype, making them excellent models for understanding the ecological drivers and genetic underpinnings of color variation. Banded and uniform morphs of the desert clicker grasshopper ( Ligurotettix coquilletti ) are found across the western deserts of North America. To address the hypothesis that predation maintains local color polymorphism and shapes regional crypsis variation, we surveyed morph frequencies and tested for covariation with two predation environments. Morphs coexisted at intermediate frequencies at most sites, consistent with local balancing selection. Morph frequencies covaried with the appearance of desert substrate – an environment used only by females – indicating that ground-foraging predators are major agents of selection on crypsis. We next addressed the hypothesized link between morph variation and genome structure. To do so, we designed an approach for detecting inversions and indels using only RADseq data. The banded morph was perfectly correlated with a large putative indel. Remarkably, indel dominance differed among populations, a rare example of dominance evolution in nature.
... It is also important to keep in mind that not only the community structure of predators (see e.g. [65]), but also prey communities influence the outcome of avoidance learning and generalization of distasteful prey [49]. ...
Article
Most research on aposematism has focused on chemically defended prey, but the signalling difficulty of capture remains poorly explored. Similar to classical Batesian and Müllerian mimicry related to distastefulness, such ‘evasive aposematism' may also lead to convergence in warning colours, known as evasive mimicry. A prime candidate group for evasive mimicry are Adelpha butterflies, which are agile insects and show remarkable colour pattern convergence. We tested the ability of naive blue tits to learn to avoid and generalize Adelpha wing patterns associated with the difficulty of capture and compared their response to that of birds that learned to associate the same wing patterns with distastefulness. Birds learned to avoid all wing patterns tested and generalized their aversion to other prey to some extent, but learning was faster with evasive prey compared to distasteful prey. Our results on generalization agree with longstanding observations of striking convergence in wing colour patterns among Adelpha species, since, in our experiments, perfect mimics of evasive and distasteful models were always protected during generalization and suffered the lowest attack rate. Moreover, generalization on evasive prey was broader compared to that on distasteful prey. Our results suggest that being hard to catch may deter predators at least as effectively as distastefulness. This study provides empirical evidence for evasive mimicry, a potentially widespread but poorly understood form of morphological convergence driven by predator selection.