Ossi Nokelainen

Trade-off between warning signal efficacy and mating success in the wood tiger moth

The coloration of species can have multiple functions, such as predator avoidance and sexual signalling, that directly affect fitness. As selection should favour traits that positively affect fitness, the genes underlying the trait should reach fixation, thereby preventing the evolution of polymorphisms. This is particularly true for aposematic species that rely on coloration as a warning signal to advertise their unprofitability to predators. Nonetheless, there are numerous examples of aposematic species showing remarkable colour polymorphisms. We examined whether colour polymorphism in the wood tiger moth is maintained by trade-offs between different functions of coloration. In Finland, males of this species have two distinct colour morphs: white and yellow. The efficacy of the warning signal of these morphs was tested by offering them to blue tits in the laboratory. Birds hesitated significantly longer to attack yellow than white males. In a field experiment, the survival of the yellow males was also higher than white males. However, mating experiments in the laboratory revealed that yellow males had lower mating success than white males. Our results offer an explanation for the maintenance of polymorphism via trade-off between survival selection and mating success.

Changes in predator community structure shifts the efficacy of two warning signals in Arctiid moths

Polymorphism in warning coloration is puzzling because positive frequency-dependent selection by predators is expected to promote monomorphic warning signals in defended prey. We studied predation on the warning-coloured wood tiger moth (Parasemia plantaginis) by using artificial prey resembling white and yellow male colour morphs in five separate populations with different naturally occurring morph frequencies. We tested whether predation favours one of the colour morphs over the other and whether that is influenced either by local, natural colour morph frequencies or predator community composition. We found that yellow specimens were attacked less than white ones regardless of the local frequency of the morphs indicating frequency-independent selection, but predation did depend on predator community composition: yellows suffered less attacks when Paridae were abundant, whereas whites suffered less attacks when Prunellidae were abundant. Our results suggest that spatial heterogeneity in predator community composition can generate a geographical mosaic of selection facilitating the evolution of polymorphic warning signals. This is the first time this mechanism gains experimental support. Altogether, this study sheds light on the evolution of adaptive coloration in heterogeneous environments.

To quiver or to shiver: increased melanization benefits thermoregulation, but reduces warning signal efficacy in the wood tiger moth

Melanin production is often considered costly, yet beneficial for thermoregulation. Studies of variation in melanization and the opposing selective forces that underlie its variability contribute greatly to understanding natural selection. We investigated whether melanization benefits are traded off with predation risk to promote observed local and geographical variation in the warning signal of adult male wood tiger moths (Parasemia plantaginis). Warning signal variation is predicted to reduce survival in aposematic species. However, in P. plantaginis, male hindwings are either yellow or white in Europe, and show continuous variation in melanized markings that cover 20 to 90 per cent of the hindwing. We found that the amount of melanization increased from 40 to 59 per cent between Estonia (58° N) and north Finland (67° N), suggesting melanization carries thermoregulatory benefits. Our thermal measurements showed that more melanic individuals warmed up more quickly on average than less melanic individuals, which probably benefits flight in cold temperatures. With extensive field experiments in central Finland and the Alpine region, we found that more melanic individuals suffered increased predation. Together, our data suggest that warning signal efficiency is constrained by thermoregulatory benefits. Differences in relative costs and benefits of melanin probably help to maintain the geographical warning signal differences.

Environment-mediated morph-linked immune and life-history responses in the aposematic wood tiger moth

1. Warning signals are expected to evolve towards conspicuousness and monomorphism, and thereby hamper the evolution of multiple colour morphs. Here, we test fitness responses to different rearing densities to explain colour polymorphism in aposematic wood tiger moth (Parasemia plantaginis) males. 2. We used larval lines sired by white or yellow adult males selected for small or large melanization patterns of coloration. We reared these selected lines either solitarily (favourable conditions) or in aggregations (challenged conditions), and followed their performance to adult stage. We tested whether differences in larval density affected life-history traits, adult melanin expression, adult morph (white or yellow) survival and immunological responses. 3. We found that the aggregated environment increased mortality of larvae, but decreased larval developmental time and pupa weight. Adult wing melanin pigmentation was dependent on larval melanin expression but not rearing density. We also confirmed that adult wing coloration had a genetic basis (h(2) = 0.42) and was not influenced by larval growth density. Adult yellow males survived better from aggregations in comparison with white males, which may be related to differences in immune defence. White males had better encapsulation ability, whereas yellow males had increased lytic activity of haemolymph in the aggregations. 4. Our main results highlight, that morph-linked immune responses mediated by differential growth density may facilitate the maintenance of colour polymorphism in aposematic species. In nature, risk of diseases and parasites vary spatially and temporally. Therefore, both yellow and white adult morphs can be maintained due to their differential investment in immune defence in heterogeneous environments.

Temporal relationship between genetic and warning signal variation in the aposematic wood tiger moth (Parasemia plantaginis).

Many plants and animals advertise unpalatability through warning signals in the form of colour and shape. Variation in warning signals within local populations is not expected because they are subject to directional selection. However, mounting evidence of warning signal variation within local populations suggests that other selective forces may be acting. Moreover, different selective pressures may act on the individual components of a warning signal. At present, we have a limited understanding about how multiple selection processes operate simultaneously on warning signal components, and even less about their temporal and spatial dynamics. Here, we examined temporal variation of several wing warning signal components (colour, UV‐reflectance, signal size and pattern) of two co‐occurring colour morphs of the aposematic wood tiger moth (Parasemia plantaginis). Sampling was carried out in four geographical regions over three consecutive years. We also evaluated each morphs temporal genetic structure by analysing mitochondrial sequence data and nuclear microsatellite markers. Our results revealed temporal differences between the morphs for most signal components measured. Moreover, variation occurred differently in the fore‐ and hindwings. We found no differences in the genetic structure between the morphs within years and regions, suggesting single local populations. However, local genetic structure fluctuated temporally. Negative correlations were found between variation produced by neutrally evolving genetic markers and those of the different signal components, indicating a non‐neutral evolution for most warning signal components. Taken together, our results suggest that differential selection on warning signal components and fluctuating population structure can be one explanation for the maintenance of warning signal variation in this aposematic species.

Colour polymorphism torn apart by opposing positive frequency‐dependent selection, yet maintained in space

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.

Preference for C4 shade grasses increases hatchling performance in the butterfly, Bicyclus safitza.

Abstract The Miocene radiation of C4 grasses under high‐temperature and low ambient CO 2 levels occurred alongside the transformation of a largely forested landscape into savanna. This inevitably changed the host plant regime of herbivores, and the simultaneous diversification of many consumer lineages, including Bicyclus butterflies in Africa, suggests that the radiations of grasses and grazers may be evolutionary linked. We examined mechanisms for this plant–herbivore interaction with the grass‐feeding Bicyclus safitza in South Africa. In a controlled environment, we tested oviposition preference and hatchling performance on local grasses with C3 or C4 photosynthetic pathways that grow either in open or shaded habitats. We predicted preference for C3 plants due to a hypothesized lower processing cost and higher palatability to herbivores. In contrast, we found that females preferred C4 shade grasses rather than either C4 grasses from open habitats or C3 grasses. The oviposition preference broadly followed hatchling performance, although hatchling survival was equally good on C4 or C3 shade grasses. This finding was explained by leaf toughness; shade grasses were softer than grasses from open habitats. Field monitoring revealed a preference of adults for shaded habitats, and stable isotope analysis of field‐sampled individuals confirmed their preference for C4 grasses as host plants. Our findings suggest that plant–herbivore interactions can influence the direction of selection in a grass‐feeding butterfly. Based on this work, we postulate future research to test whether these interactions more generally contribute to radiations in herbivorous insects via expansions into new, unexploited ecological niches.

Transparency reduces predator detection in chemically protected clearwing butterflies

1. Predation is an important selective pressure and some prey have evolved warning colour signals advertising unpalatability (i.e. aposematism) as an antipredator strategy. Unexpectedly, some butterfly species from the unpalatable tribe Ithomiini possess transparent wings, an adaptation rare on land but common in water where it helps avoiding predator detection. 2. We tested if transparency of butterfly wings was associated with decreased detectability by predators, by comparing four butterfly species exhibiting different degrees of transparency, ranging from fully opaque to largely transparent. We tested our prediction using using both wild birds and humans in behavioural experiments. Vision modelling predicted detectability to be similar for these two predator types. 3. In concordance with predictions, more transparent species were almost never the first detected items and were detected less often than the opaque species by both birds and humans, suggesting that transparency enhances crypsis. However, humans could learn to better detect the most transparent species over time. Our study demonstrates for the first time that transparency on land likely decreases detectability by visual predators.

Multimodal Aposematic Signals and Their Emerging Role in Mate Attraction

Chemically defended animals often display conspicuous colour 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 defences) 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 signalling. A. plantaginis is an aposematic diurnal moth which exhibits sexually dimorphic colouration as well as sex-limited polymorphism in part of its range. The anti-predator function of its colouration and, more recently, its chemical defences (even when experimentally decoupled from the visual signals) have been well-demonstrated. Interestingly, recent studies have revealed differences between the two male morphs in mating success, suggesting a role of colouration in mate choice or attraction, and providing a possible explanation for its sexual dimorphism in colouration. 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.