Aposematic Traits Research Articles

Predator selection on multicomponent warning signals in an aposematic moth.

Aposematic prey advertise their unprofitability with conspicuous warning signals that are often composed of multiple color patterns. Many species show intraspecific variation in these patterns even though selection is expected to favor invariable warning signals that enhance predator learning. However, if predators acquire avoidance to specific signal components, this might relax selection on other aposematic traits and explain variability. Here, we investigated this idea in the aposematic moth Amata nigriceps that has conspicuous black and orange coloration. The size of the orange spots in the wings is highly variable between individuals, whereas the number and width of orange abdominal stripes remains consistent. We produced artificial moths that varied in the proportion of orange in the wings or the presence of abdominal stripes. We presented these to a natural avian predator, the noisy miner (Manorina melanocephala), and recorded how different warning signal components influenced their attack decisions. When moth models had orange stripes on the abdomen, birds did not discriminate between different wing signals. However, when the stripes on the abdomen were removed, birds chose the model with smaller wing spots. In addition, we found that birds were more likely to attack moths with a smaller number of abdominal stripes. Together, our results suggest that bird predators primarily pay attention to the abdominal stripes of A. nigriceps, and this could relax selection on wing coloration. Our study highlights the importance of considering individual warning signal components if we are to understand how predation shapes selection on prey warning coloration.

Outcomes of multifarious selection on the evolution of visual signals.

Multifarious sources of selection shape visual signals and can produce phenotypic divergence. Theory predicts that variance in warning signals should be minimal due to purifying selection, yet polymorphism is abundant. While in some instances divergent signals can evolve into discrete morphs, continuously variable phenotypes are also encountered in natural populations. Notwithstanding, we currently have an incomplete understanding of how combinations of selection shape fitness landscapes, particularly those which produce polymorphism. We modelled how combinations of natural and sexual selection act on aposematic traits within a single population to gain insights into what combinations of selection favours the evolution and maintenance of phenotypic variation. With a rich foundation of studies on selection and phenotypic divergence, we reference the poison frog genus Oophaga to model signal evolution. Multifarious selection on aposematic traits created the topology of our model's fitness landscape by approximating different scenarios found in natural populations. Combined, the model produced all types of phenotypic variation found in frog populations, namely monomorphism, continuous variation and discrete polymorphism. Our results afford advances into how multifarious selection shapes phenotypic divergence, which, along with additional modelling enhancements, will allow us to further our understanding of visual signal evolution.

Joint effects of female preference intensity and frequency-dependent predation on the polymorphism maintenance in aposematic sexual traits.

Maintenance of variation in aposematic traits within and among populations is paradoxical because aposematic species are normally under positive frequency‐dependent predation (PFD), which is expected to erode variation. Aposematic traits can evolve in an ecological context where aposematic traits are simultaneously under mate choice. Here, we examine how the mate preference intensity affects the permissiveness of polymorphism in sexually selected aposematic traits under different PFD regimes. We use the haploid version of the classical sexual selection model and show that strong mate preferences can substantially increase the permissiveness of polymorphism in aposematic traits under different PFD regimes. The Fisher process can interact with PFD, and their interaction can promote the maintenance of polymorphism within populations when mate preferences are strong. We show that the same selective conditions that promote the maintenance of polymorphism within populations reduce the likelihood of divergence in aposematic traits among populations.

Aposematic signalling in prey-predator systems: determining evolutionary stability when prey populations consist of a single species

Aposematism is the signalling of a defence for the deterrence of predators. We presently focus on aposematic organisms that exhibit chemical defences, which are usually signalled by some type of brightly coloured skin pigmentation (as is the case with poison frog species of the Dendrobatidae family), although our treatment is likely transferable to other forms of secondary defence. This setup is not only a natural one to consider but also opens up the possibility for rich mathematical modelling: the strength of aposematic traits (signalling and defence) can be unambiguously realised using variables that are continuously quantifiable, independent from one another and which together define a two-dimensional strategy space wherein the aposematic behaviour of any one organism can be represented by a single point. We presently develop an extensive mathematical model in which we explore the joint co-evolution of aposematic traits within the context of evolutionary stability. Even though empirical and model-based studies are conflicting regarding how aposematic traits are related to one another in nature, the majority of works allude to a positive correlation. We presently suggest that both positively and negatively correlated combinations of traits can achieve evolutionarily stable outcomes and further, that for a given level of signal strength there can be more than one optimal level of defence. Our findings are novel and pertinent to a sizeable body of physical evidence, which we discuss.

<p align="center">A new Norwegian Lemming subspecies from Novaya Zemlya, Arctic Russia

Norwegian Lemming Lemmus lemmus is a remarkable population cycling species having a number of aposematic traits in coloration and behavior. This species was thought to be the only mammal endemic to Fennoscandia. Here, we report on the discovery of a distinct lineage of this species from Novaya Zemlya. This lineage is described here as the new subspecies Lemmus lemmus chernovi ssp. nov. that morphologically differs from the nominate subspecies by having a cryptic coloration. Our time-calibrated phylogeny revealed that this insular subspecies was isolated there since the Eemian interglacial (mean age 93 Ka). Hence, bright coloration and antipredator behavior of the nominate subspecies are novel aposematic traits that evolved since its isolation in a European refugium. This new discovery indicates that Novaya Zemlya supported a cryptic polar refugium for cold-adapted terrestrial fauna during the Pleistocene. Finally, our findings highlight that allopatric ranges of the true lemmings (Lemmus) reflect stepwise range expansions in cold climatic episodes with subsequent isolation in refugia during interglacial events.

Amphibiomorphic Modeled and Painted Pottery from Argentine Patagonia and Central-Southern Chile. Functional Interpretation and Identification of Species Based on Mimetic and Aposematic Traits

Abstract This work aims to identify attributes or features related to endemic amphibians in modeled and painted pottery from central-southern Chile and north-western Argentina. From this work, we were able to identify four species of amphibians represented in certain types of modeled and painted pottery, and we also complemented this data with modern references and ethnohistorical chronicles of the potential use given to this pottery in particular. This contribution postulates that some elements of the black-onred pottery of the Early Ceramic Period of Araucanía in central-southern Chile and of Patagonia in northwestern Argentina, seek to highlight amphibiomorphic characteristics such as exophthalmia (protruding eyes) and aposematism (brilliant coloring and brightness of the vessel by using an engobe decoration). Based on the ethnohistorical data of the area, it is also proposed that these vessels could be linked to the exclusive use of highly toxic substances. Finally, the results allowed us to explore the close ecological interaction between human groups and woodlands.

Parental phenotype not predator cues influence egg warning coloration and defence levels

In species that advertise their toxicity to predators through visual signals, there is considerable variation among individuals in both signal appearance and levels of defence. Parental effects, a type of nongenetic inheritance, may play a key role in creating and maintaining this within-species diversity in aposematic signals; however, a comprehensive test of this notion is lacking. Using the ladybird Adalia bipunctata, we assessed how egg coloration and defence level (concentration of the toxic alkaloid (-)-adaline) is influenced both by simulated predation risk in the egg-laying environment and by parental phenotype (coloration and toxin level). We found that egg toxin level and colour were predicted by parental phenotype but were not altered in response to cues of egg predators. Egg luminance (lightness) was positively correlated with paternal elytral luminance, while maternal toxin level positively predicted egg toxin level. In response to egg predator cues, ladybird mothers altered the timing of laying and total egg number, but not egg toxin level or colour. It appears therefore that in A. bipunctata variation between individuals of the same morph in the colour and toxin level of the eggs they lay, that is, egg aposematic phenotype, is more strongly influenced by individual variation in parental aposematic traits than by environmental cues of egg predation risk. Furthermore, these results provide the first indication that, in a warningly coloured species, male coloration may play a dual role as predator deterrent and indicator of paternal quality, influencing maternal investment in offspring.

Nonpreference ofCeratomia catalpae(Lepidoptera: Sphingidae) to Invertebrate Predators

Aposematic traits such as bright contrasting coloration and gregarious feeding are often signals to predators that a potential prey is unpalatable. Larvae of Ceratomia catalpae (Boisduval) (Lepidoptera: Sphingidae), the catalpa sphinx, show aposematic traits and sequester catalpol, a secondary compound from their host plant Catalpa spp. (Bignoniaceae). Catalpol sequestration by other caterpillar species has been shown to deter both invertebrate and vertebrate predators, but the palatability of C. catalpae has not been explicitly tested. Choice tests were performed with spiders (Hogna carolinensis Walckenaer, Araneae: Lycosidae) and predatory hemipterans (Podisus maculiventris [Say], Hemiptera: Pentatomidae). These tests showed that predators naive to both C. catalpae and the alternate prey Trichoplusia ni (Hubner) (Lepidoptera: Noctuidae) and Manduca sexta (L.) (Lepidoptera: Sphingidae) preferred the alternate species, and that P. maculiventris that were exposed previously to T. ni also preferred T. ni. In nonchoice tests, P. maculiventris grew significantly more slowly upon C. catalpae compared to M. sexta. These results suggest that C. catalpae, like other caterpillars that sequester catalpol, is less palatable to invertebrate predators compared to nonsequestering caterpillar species.

Aposematism and crypsis in a rodent: antipredator defence of the Norwegian lemming

Aposematism is unusual in herbivorous mammals, and exceptions help clarify its ecology and evolution. The Norwegian lemming differs from other rodents in colouration and behaviour. One hypothesis is that its black, yellow and white colours, loud calls and ferocious defence reduce predation by conspicuous aposematism. Another hypothesis is that the colouration is cryptic. These alternatives are tested in a detectability experiment comparing lemmings and sympatric grey-sided voles. All 18 observers detected a higher proportion of the lemmings, corroborating conspicuousness. Unlike smaller rodents, Norwegian lemmings often call from a distance at predators. The aposematism hypothesis predicts that cryptically coloured Alaskan brown lemmings will not call. In the field, Norwegian lemmings gave antipredator calls at a human observer in 36 of 110 encounters, but brown lemmings did so in only 1 of 39 cases. Most Norwegian lemmings called if surprised within a few metres but froze or fled silently farther away, relying on crypsis against distant predators. Small juveniles called as often as adults, a possible case of auto-mimicry. In an earlier experiment, Norwegian lemmings, in contrast with grey-sided voles, aggressively resisted attacks by a major avian predator of rodents. The tests corroborate the hypotheses that (1) distinctive, contrast-rich colouration, antipredator calls and threat postures of the Norwegian lemming form a multimodal suit of aposematic traits, warning predators that this is a more dangerous prey than the smaller sympatric voles, and (2) discriminability from undefended species is an important adaptive reason for conspicuous distinctness of many aposematic signals.

Maternal effects and warning signal honesty in eggs and offspring of an aposematic ladybird beetle

Summary The eggs of oviparous species are often subject to intense predation pressure. One parental strategy to deter predators is to produce eggs that are laced with noxious chemicals and are conspicuously coloured (i.e. aposematism). Ladybird eggs are conspicuously coloured and contain alkaloids; these traits are believed to function in concert as visual signal and chemical defence, respectively, to deter predators. However, it remains unclear whether such aposematic signals reveal the strength (rather than simply the existence) of chemical defences. Furthermore, additional functions of egg pigments and toxins could apply; in particular, mothers might deposit such resources into eggs to aid the development of offspring or to provide resources that could contribute to aposematic traits in offspring. We bred wild‐caught seven‐spot ladybird beetles (Coccinella septempunctata) in the laboratory and then measured relationships between egg coloration and toxin concentrations (i.e. the alkaloids precoccinelline and coccinelline). We also measured relationships between egg carotenoids and egg coloration, and between egg coloration and toxin levels, and the elytra coloration and toxin concentrations of offspring at eclosion for a subset of eggs that were allowed to develop. Egg carotenoids predicted egg colour saturation. In turn, egg colour saturation and hue positively predicted egg concentrations of precoccinelline. However, there were no significant relationships between egg coccinelline concentration and any measure of egg coloration. In recently eclosed adults of both sexes, elytra saturation was significantly explained by variation in egg saturation and hue. Finally, body concentrations of coccinelline were significantly explained by variation in elytra hue. These results suggest that the coloration of C. septempunctata eggs is a reliable signal of the strength of chemical defences contained therein, but in addition, maternal investment of pigments and toxins into eggs may serve to influence the reliability of aposematic signalling in resultant offspring.

Not all colors are equal: predation and color polytypism in the aposematic poison frog Oophaga pumilio

Aposematic organisms are not predicted to show high levels of warning signal diversity because they are expected to be under stabilizing selection to decrease costs of ‘educating’ predators about their unpalatability. However, systematic changes in warning signals (polytypism) can be expected if they represent adaptations to local predators. The aposematic strawberry poison frog (Oophaga pumilio) is red throughout its mainland distribution in Costa Rica and Panama, but displays high levels of warning signal diversity in the Bocas del Toro Archipelago of Panama. Both coloration and spot pattern vary in a polytypic sense. Sexual selection contributes to maintaining the polytypism, but little work has investigated the potential influence of predation. We used unspotted models of O. pumilio to determine if predation might help explain the color polytypism on Isla Colon in the Bocas del Toro Archipelago of Panama. We tested whether attack rates differed among the red mainland morph, green/yellow Isla Colon morph, and the brown control. We found that frog color significantly predicted being attacked. The local green Isla Colon models were attacked more than foreign red or brown models. No difference in attack rate existed between red and brown control models. Our results suggest that the red mainland morph possesses a more effective warning signal, even when it is not the local morph. Honest signaling of unpalatability, neophobia, and the use of search images by local predators are potential explanations. Similarity of the brown model to other local poison frogs might explain the lower attack rate compared to previous work. The attack rate was lower on Isla Colon compared to mainland Costa Rica, which supports the hypothesis that less overall predation in the Bocas del Toro Archipelago may contribute to the overall warning signal diversity in O. pumilio there by relaxing selection for aposematic traits.

How the ladybird got its spots: effects of resource limitation on the honesty of aposematic signals

Summary1. Prey species often possess defences (e.g. toxins) coupled with warning signals (i.e. aposematism). There is growing evidence that the expression of aposematic signals often varies within species and correlates with the strength of chemical defences. This has led to the speculation that such signals may be ‘honest’, with signal reliability ensured by the costliness of producing or maintaining aposematic traits.2. We reared larval seven‐spot ladybirds (Coccinella septempunctata) on a Low or High aphid diet and measured the effects on warning signal expression (elytral carotenoid pigmentation, conspicuousness, spot size), levels of defensive alkaloids (precoccinelline, coccinelline), and relationships between these traits.3. High‐diet individuals had greater total precoccinelline levels, and elytra carotenoid concentrations at adulthood which was detectable to a typical avian predator. However, larval diet did not significantly affect adult body mass or size, spot size or coccinelline levels.4. Elytra carotenoid concentrations correlated positively with total precoccinelline levels in both diet groups and sexes. However, the relationship between elytra carotenoid concentrations and total levels of coccinelline depended on sex: in both diet groups, elytra carotenoids and coccinelline levels were positively correlated in females, but negatively correlated in males. Spot size and coccinelline levels correlated positively in Low‐diet individuals, but negatively in High‐diet individuals.5. These results point to physiological linkages between components of aposematism, which are modulated by resource (i.e. food) availability and affect the honesty of signals. Developmental diet, but also sex, influenced the relationships between signals and toxin levels. Ladybirds are sexually size dimorphic, and thus in comparison with males, females may be more susceptible to resource limitation and more likely to be honest signallers.

APOSEMATIC SIGNAL VARIATION PREDICTS MALE-MALE INTERACTIONS IN A POLYMORPHIC POISON FROG

Many species use conspicuous "aposematic" signals to communicate unpalatability/unprofitability to potential predators. Although aposematic traits are generally considered to be classic examples of evolution by natural selection, they can also function in the context of sexual selection, and therefore comprise exceptional systems for understanding how conspicuous signals evolve under multifarious selection. We used males from a highly territorial poison frog species in a dichotomous choice behavioral test to conduct the first examination of how aposematic signal variation influences male-male interactions. Our results reveal two behavioral patterns: (1) male dorsal brightness influences the behaviors of male conspecifics such that males approach and call to brighter males more frequently and (2) a male's dorsal brightness predicts his own behavior such that bright males approach stimulus frogs faster, direct more calls to bright stimulus frogs, and exhibit lower advertising call pulse rates (a fitness-related trait). These findings indicate the potential for sexual selection by male-male competition to impact aposematic signal evolution.

The effect of metapopulation dynamics on the survival and spread of a novel, conspicuous prey

Animals that deploy chemical defences against predators often signal their unprofitability using bright colouration. This pairing of toxicity and conspicuous patterning is known as aposematism. Explaining the evolution and spread of aposematic traits in previously cryptic species has been the focus of much empirical and theoretical work over the last two decades. Existing research concerning the initial evolution of aposematism does not however properly consider that many aposematic species (such as members of the hymenoptera, the lepidoptera, and amphibia) are highly mobile. We argue in this paper that the evolution of aposematic displays is therefore often best understood within a metapopulation framework; hence in this paper we present the first explicit metapopulation model of the evolution of aposematism. Our most general finding is that migration tends to reduce the probability that an aposematic prey can increase from rarity and spread across a large population. Hence, the best case scenarios for the spread of aposematism required fixation of the aposematic form in one or more isolated sub-habitats prior to some event which subsequently enabled migration. We observed that changes in frequency of new aposematic forms within source habitats are likely to be nonmonotonic. First, aposematic prey tend to decline in frequency as they migrate outwards from the source habitat to neighbouring sink habitats, but subsequently they increase in relative abundance in the source, as the descendents of earlier migrants migrate back from newly converted sub-populations. This pattern of initial loss and subsequent gain between new source and neighbouring sink habitats is then repeated as the aposematic form spreads via a moving cline.

Characterizing the pigment composition of a variable warning signal of Parasemia plantaginis larvae

Summary 1. Aposematic animals advertise their defences to predators via warning signals that often are bright colours combined with black patterns. Predation is assumed to select for large pattern elements and conspicuousness of warning signals because this enhances avoidance learning of predators. However, conspicuousness of the colour pattern can vary among individuals of aposematic species, suggesting that warning signal expression may be constrained by opposing selection pressures. If effective warning signals are costly to produce, variation in signal expression may be maintained via physiological trade‐offs. To understand the costs of signalling that might underlay both physiological and ecological trade‐offs, it is crucial to identify the pigments involved in aposematic traits, how they or their precursors are acquired and how their production and/or deposition interact with other physiological processes. 2. We characterized the pigments responsible for the genetically and phenotypically variable orange‐black warning signal of the hairy larvae of an Arctiid moth, Parasemia plantaginis. We tested orange and black coloured hairs for the presence of six candidate pigment types using high‐performance liquid chromatography, spectral and solubility analyses. 3. After excluding the presence of carotenoids, ommochromes, pterins and pheomelanins in orange hairs, our results suggest that tiger moth larvae produce their orange warning signal by depositing both diet‐derived flavonoids and trace levels of synthesized eumelanin in their hairs. The nearby black hairs are coloured by eumelanin. 4. In light of previous studies, we conclude that although a large orange patch increases the 1larvae’s antipredator efficacy, variation in the size of orange patches within a population can be driven by scarcity of flavonoids in diet. However, traces of eumelanin found in the orange hairs of the larvae may also play a significant role in the maintenance of the signal pattern on poor quality diets. 5. The goal of the future studies will be to test the condition dependence of pigment deposition in aposematic colour patterns by directly manipulating relevant nutritional parameters such as dietary flavonoid or nitrogen content (i.e. amino acid content).

Sexual dimorphism and directional sexual selection on aposematic signals in a poison frog

It is commonly assumed that natural selection imposed by predators is the prevailing force driving the evolution of aposematic traits. Here, we demonstrate that aposematic signals are shaped by sexual selection as well. We evaluated sexual selection for coloration brightness in populations of the poison frog Oophaga [Dendrobates] pumilio in Panama's Bocas del Toro archipelago. We assessed female preferences for brighter males by manipulating the perceived brightness of spectrally matched males in two-way choice experiments. We found strong female preferences for bright males in two island populations and weaker or ambiguous preferences in females from mainland populations. Spectral reflectance measurements, coupled with an O. pumilio-specific visual processing model, showed that O. pumilio coloration was significantly brighter in island than in mainland morphs. In one of the island populations (Isla Solarte), males were significantly more brightly colored than females. Taken together, these results provide evidence for directional sexual selection on aposematic coloration and document sexual dimorphism in vertebrate warning coloration. Although aposematic signals have long been upheld as exemplars of natural selection, our results show that sexual selection should not be ignored in studies of aposematic evolution.

A parallel geographical mosaic of morphological and behavioural aposematic traits of the newt, Cynops pyrrhogaster (Urodela: Salamandridae)

Aposematic animals advertise their unprofitability to potential predators with conspicuous coloration, occasionally in combination with other life-history traits. Theory posits that selection on functionally interrelated aposematic characters promotes the unidirectional evolution of these characters, resulting in an increase or decrease in the effectiveness of the signal. To test whether this prediction applies on a microevolutionary scale, the intra- and interpopulational variations in aposematic coloration, behaviour (which enhances the effectiveness of the coloration) and body size of newts, Cynops pyrrhogaster (Urodela: Salamandridae), were investigated. A parallel geographical mosaic of variation in aposematic coloration and behaviour among populations, independent of body size, was found. Newts on islands displayed more conspicuous aposematic traits than those on the mainland, both morphologically and behaviourally. There was no significant relationship between variation in coloration and behaviour within populations. Male newts displayed more conspicuous coloration than females. Surveys of potential predators suggest that variable natural selection at a local scale, such as predation pressure, may primarily be responsible for the microevolution of variable aposematic traits in newts. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97, 613–622.

Aposematism: what should our starting point be?

The evolution of aposematism is considered to be a major evolutionary problem because if new aposematic forms emerged in defended cryptic populations, they would face the dual problems of rarity and conspicuousness. We argue that this commonly assumed starting point might not have wide validity. We describe a novel evolutionary computer model in which prey evolve secondary defences and become conspicuous by moving widely over a visually heterogeneous habitat. Unless crypsis imposes high opportunity costs (for instance, preventing prey from efficient foraging, thermoregulation and communication), costly secondary defences are not predicted to evolve at all. However, when crypsis imposes opportunity costs, prey evolve secondary defences that facilitate raised behavioural conspicuousness as prey exploit opportunities within their environment. Optimal levels of secondary defence and of behavioural conspicuousness increase with population sizes and the costs imposed by crypsis. When prey are already conspicuous by virtue of their behaviours, the evolution of aposematic appearances (bright coloration, etc.) is much easier to explain because aposematic traits add little further costs of conspicuousness, but can bring large benefits.