Project

Polymorphic wood tiger-moths

Goal: This project investigates multiple selection forces that aposematic and colour polymorphic wood tiger moth face in the wild. This system helps us to understand how predation by birds, diseases, sexual selection and thermoregulation shape phenotypes of individuals.

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Johanna Mappes
added 2 research items
Background Diploid genome assembly is typically impeded by heterozygosity because it introduces errors when haplotypes are collapsed into a consensus sequence. Trio binning offers an innovative solution that exploits heterozygosity for assembly. Short, parental reads are used to assign parental origin to long reads from their F1 offspring before assembly, enabling complete haplotype resolution. Trio binning could therefore provide an effective strategy for assembling highly heterozygous genomes, which are traditionally problematic, such as insect genomes. This includes the wood tiger moth (Arctia plantaginis), which is an evolutionary study system for warning colour polymorphism. Findings We produced a high-quality, haplotype-resolved assembly for Arctia plantaginis through trio binning. We sequenced a same-species family (F1 heterozygosity ∼1.9%) and used parental Illumina reads to bin 99.98% of offspring Pacific Biosciences reads by parental origin, before assembling each haplotype separately and scaffolding with 10X linked reads. Both assemblies are contiguous (mean scaffold N50: 8.2 Mb) and complete (mean BUSCO completeness: 97.3%), with annotations and 31 chromosomes identified through karyotyping. We used the assembly to analyse genome-wide population structure and relationships between 40 wild resequenced individuals from 5 populations across Europe, revealing the Georgian population as the most genetically differentiated with the lowest genetic diversity. Conclusions We present the first invertebrate genome to be assembled via trio binning. This assembly is one of the highest quality genomes available for Lepidoptera, supporting trio binning as a potent strategy for assembling heterozygous genomes. Using our assembly, we provide genomic insights into the geographic population structure of A. plantaginis.
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, Arctia plantaginis, differ. Here we show that selection by avian predators on warning colour is predicted by local morph frequency and predator community composition. We found +FDS to be the strongest in monomorphic Scotland and lowest in polymorphic Finland, where the attack risk of moth morphs depended on the local avian community. +FDS was also found where the predator community was the least diverse (Georgia), whereas in the most diverse avian community (Estonia), hardly any models were attacked. Our results support the idea that spatial variation in predator communities alters the strength or direction of selection on warning signals, thus facilitating a geographic mosaic of selection. A geographic mosaic of selection by predators could explain the paradoxical maintenance of warning signal variation, but direct ecological evidence is scarce and focused on tropical systems. We monitored local avian predators and attacks on 4000 + moth models representing red, yellow or white warning colour morphs in a temperate moth system with natural variation in local morph frequencies. We found positive frequency‐dependent selection to be strongest in monomorphic populations and the direction and strength of selection to be significantly associated with local predator community composition and diversification, which can explain not only geographic variation (polytypism) but also local polymorphism when coupled with gene flow.
Bibiana Rojas
added a research item
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 locations, among which the frequencies of hindwing warning coloration of aposematic Arctia plantaginis differ. Here we show that selection by avian predators on warning colour is predicted by local morph frequency and predator community composition. We found +FDS to be strongest in monomorphic Scotland, and in contrast, lowest in polymorphic Finland, where different predators favour different male morphs. +FDS was also found in Georgia, where the predator community was the least diverse, whereas in the most diverse avian community in Estonia, hardly any models were attacked. Our results support the idea that spatial variation in predator and prey communities alters the strength or direction of selection on warning signals, thus facilitating a geographic mosaic of selection.
Bibiana Rojas
added a research item
Multiple-model mimicry, whereby different morphs of an aposematic species each resemble another defended species sharing the costs of predator education, has been proposed as a mechanism allowing colour polymorphisms in aposematic species. Male wood tiger moths, Arctia plantaginis (Linnaeus, 1758), are chemically defended and polymorphic (yellow, white) for hindwing coloration. We selected four potentially aposematic moth species and studied whether Müllerian mimicry exists between them and A. plantaginis morphs. We tested the moths' relative palatability to natural predators with and without visual cues, their phenotypic similarity under a bird visual system, and whether trials with a potential moth model influence a predator's willingness to attack A. plantaginis. Our results show that (1) three of the four tested species were not sufficiently unpalatable and thus not potential models for A. plantaginis, and (2) birds confused the unpalatable yellow model Arichanna melanaria with yellow A. plantaginis, although their overall appearance is distinguishable. This indicates imperfect mimicry based on shared colour cues. Multiple-model mimicry is thus a potential contributor to the maintenance of multiple morphs, although no unpalatable model was found for the white morph. Our findings highlight the importance of accounting for both prey coloration and palatability, which in concert affect predator behaviour, the ultimate driver of mimicry evolution.
Johanna Mappes
added a research item
Chemically defended animals often display conspicuous color patterns that predators learn to associate with their unprofitability and subsequently avoid. Such animals (i.e., aposematic), deter predators by stimulating their visual and chemical sensory channels. Hence, aposematism is considered to be "multimodal." The evolution of warning signals (and to a lesser degree their accompanying chemical defenses) is fundamentally linked to natural selection by predators. Lately, however, increasing evidence also points to a role of sexual selection shaping warning signal evolution. One of the species in which this has been shown is the wood tiger moth, Arctia plantaginis, which we here put forward as a promising model to investigate multimodality in aposematic and sexual signaling. A. plantaginis is an aposematic diurnal moth which exhibits sexually dimorphic coloration as well as sex-limited polymorphism in part of its range. The anti-predator function of its coloration and, more recently, its chemical defenses (even when experimentally decoupled from the visual signals), has been well-demonstrated. Interestingly, recent studies have revealed differences between the two male morphs in mating success, suggesting a role of coloration in mate choice or attraction, and providing a possible explanation for its sexual dimorphism in coloration. Here, we: (1) review the lines of evidence showing the role of predation pressure and sexual selection in the evolution of multimodal aposematic signals in general, and in the wood tiger moth in particular; (2) establish gaps in current research linking sexual selection and predation as selective pressures on aposematic signals by reviewing a sample of the literature published in the last 30 years; (3) highlight the need of identifying suitable systems to address simultaneously the effect of natural and sexual selection on multimodal aposematic signals; and (4) propose directions for future research to test how aposematic signals can evolve under natural and sexual selection.
Bibiana Rojas
added a research item
Multiple-model mimicry, whereby different morphs of an aposematic species each resemble another defended species sharing the costs of predator education, has been proposed as a mechanism allowing colour polymorphisms in aposematic species. Male wood tiger moths, Arctia plantaginis (Linnaeus, 1758), are chemically defended and polymorphic (yellow, white) for hindwing coloration. We selected four potentially aposematic moth species and studied whether Müllerian mimicry exists between them and A. plantaginis morphs. We tested the moths' relative palatability to natural predators with and without visual cues, their phenotypic similarity under a bird visual system, and whether trials with a potential moth model influence a predator's willingness to attack A. plantaginis. Our results show that (1) three of the four tested species were not sufficiently unpalatable and thus not potential models for A. plantaginis, and (2) birds confused the unpalatable yellow model Arichanna melanaria with yellow A. plantaginis, although their overall appearance is distinguishable. This indicates imperfect mimicry based on shared colour cues. Multiple-model mimicry is thus a potential contributor to the maintenance of multiple morphs, although no unpalatable model was found for the white morph. Our findings highlight the importance of accounting for both prey coloration and palatability, which in concert affect predator behaviour, the ultimate driver of mimicry evolution.
Bibiana Rojas
added a research item
Although predation is commonly thought to exert the strongest selective pressure on colouration in aposematic species, sexual selection may also influence colouration. Specifically, polymorphism in aposematic species cannot be explained by natural selection alone. 2.Males of the aposematic wood tiger moth (Arctia plantaginis) are polymorphic for hindwing colouration throughout most of their range. In Scandinavia, they display either white or yellow hindwings. Female hindwing colouration varies continuously from bright orange to red. Redder females and yellow males suffer least from bird predation. 3.White males often have higher mating success than yellow males. Therefore, we ask whether females can discriminate the two male morphs by colour. Males approach females by following pheromone plumes from a distance, but search visually at short range. This raises the questions whether males discriminate female colouration and, in turn, whether female colouration is also sexually selected. 4.Using electroretinograms, we found significantly larger retinal responses in male than female A. plantaginis, but similar spectral sensitivities in both sexes, with peaks in the UV (349 nm), blue (457 nm), and green (521 nm) wavelength range. 5.According to colour vision models, conspecifics can discriminate white and yellow males as separate morphs, but not orange and red females. For moths and birds (Cyanistes caeruleus), white males are more conspicuous against green and brown backgrounds, mostly due to UV reflectivity, and red females are slightly more conspicuous than orange females. 6.The costly red colouration among females is likely selected by predator pressure, not by conspecifics, whereas male colour polymorphism is probably maintained, at least partly, by a the opposing forces of predation pressure favouring yellow males, and female preference for white males. Whether or not the preference for white males is based on visual cues requires further testing. 7.The evolution of polymorphic aposematic animals can be better understood when the visual system of the species and their predators is taken into consideration. This article is protected by copyright. All rights reserved.
Johanna Mappes
added a research item
Predators efficiently learn to avoid one type of warning signal rather than several, making colour polymorphisms unexpected. Aposematic wood tiger moth males Parasemia plantaginis have either white or yellow hindwing coloration across Eu-rope. Previous studies indicate that yellow males are better defended from predators, while white males have a positively frequency dependent mating advantage. However, the potential frequency-dependent behavioural differences in flight between the morphs, as well as the role of male-male interactions in inducing flying activity, have not been previously considered. We ran an outdoor cage experiment where proportions of both male morphs were manipulated to test whether flying activity was frequency-dependent and differed between morphs. The white morph was significantly more active than the yellow one across all treatments, and sustained activity for longer. Overall activity for both morphs was considerably lower in the yellow-biased environment, suggesting that higher proportions of yellow males in a population may lead to overall reduced flying activity. The activity of the yellow morph also followed a steeper, narrower curve than that of the white morph during peak female calling activity. We suggest that white males, with their presumably less costly defences, have more resources to invest in flight for predator escape and finding mates. Yellow males, which are better protected but less sexually selected, may instead compensate their lower flight activity by 'flying smart' during the peak female-calling periods. Thus, both morphs may be able to behaviourally balance the trade-off between warning signal selection and sexual selection. Our results emphasize the greater need to investigate animal behaviour and colour polymorphisms in natural or semi-natural environments [Current Zoology 61 (4): 765–772, 2015].
Johanna Mappes
added 18 research items
To predict evolutionary responses of warning signals under selection, we need to determine the inheritance pattern of the signals, and how they are genetically correlated with other traits contributing to fitness. Furthermore, protective coloration often undergoes remarkable changes within an individual's lifecycle, requiring us to quantify the genetic constraints of adaptive coloration across all the relevant life stages. Based on a 12 generation pedigree with > 11 000 individuals of the wood tiger moth (Arctia plantaginis), we show that high primary defense as a larva (large warning signal) results in weaker defenses as adult (less efficient warning color), due to the negative genetic correlation between the efficacy of larval and adult warning coloration. However, production of effective warning coloration as a larva, did not incur any life-history costs and was positively genetically correlated with reproductive output. These results provide novel insights into the evolutionary constraints on protective coloration in animals, and explain the maintenance of variation in the signal expression despite the strong directional selection by predators. By analyzing the genetic and environmental effects on warning signal and life-history traits in all relevant life stages, we can accurately determine the mechanisms shaping the evolutionary responses of phenotypic traits under different selection environments. This article is protected by copyright. All rights reserved.
Polymorphic warning signals in aposematic species are enigmatic because predator learning and discrimination should select for the most common coloration, resulting in positive frequency-dependent survival selection. Here, we investigated whether differential mating success could create sufficiently strong negative frequency-dependent selection for rare morphs to explain polymorphic (white and yellow) warning coloration in male wood tiger moths (Parasemia plantaginis). We conducted an experiment in semi-natural conditions where we estimated mating success for both white and yellow male moths under three different morph frequencies. Contrary to expectations, mating success was positively frequency-dependent: white morph males had high relative fitness when common, likewise yellow morph males had high relative fitness when instead they were common. We hence built a model parameterized with our data to examine whether polymorphism can be maintained despite two sources of positive frequency dependence. The model includes known spatial variation in the survival advantage enjoyed by the yellow morph, and assumes that relative mating success follows our experimentally derived values. It predicts that polymorphism is possible under migration for up to approximately 20% exchange of individuals between subpopulations in each generation. Our results suggest that differential mating success combined with spatial variation in predator communities may operate as a selection mosaic that prevents complete fixation of either morph.
Sequestration of plant defensive chemicals by herbivorous insects is a way of defending themselves against their natural enemies. Such herbivores have repeatedly evolved bright colours to advertise their unpalatability to predators, i.e. they are aposematic. This often comes with a cost. In this study, we examined the costs and benefits of sequestration of iridoid glycosides (IGs) by the generalist aposematic herbivore, the wood tiger moth, Parasemia plantaginis. We also asked whether the defence against one enemy (a predator) is also effective against another (a parasitoid). We found that the larvae excrete most of the IGs and only small amounts are found in the larvae. Nevertheless, the amounts present in the larvae are sufficient to deter ant predators and also play a role in defence against parasitoids. However, excreting and handling these defensive plant compounds is costly, leading to longer development time and lower pupal mass. Interestingly, the warning signal efficiency and the amount of IGs in the larvae of P. plantaginis are negatively correlated; larvae with less efficient warning signals contain higher levels of chemical defence compounds. Our results may imply that there is a trade-off between production and maintenance of coloration and chemical defence. Although feeding on a diet containing IGs can have life-history costs, it offers multiple benefits in the defence against predators and parasitoids.
Johanna Mappes
added a project goal
This project investigates multiple selection forces that aposematic and colour polymorphic wood tiger moth face in the wild. This system helps us to understand how predation by birds, diseases, sexual selection and thermoregulation shape phenotypes of individuals.