Cryptic female Strawberry poison frogs experience elevated predation risk when associating with an aposematic partner

Population divergence in sexual signals may lead to speciation through prezygotic isolation. Sexual signals can change solely due to variation in the level of natural selection acting against conspicuousness. However, directional mate choice (i.e., favoring conspicuousness) across different environments may lead to gene flow between populations, thereby delaying or even preventing the evolution of reproductive barriers and speciation. In this study, we test whether natural selection through predation upon mate‐choosing females can favor corresponding changes in mate preferences. Our study system, Oophaga pumilio, is an extremely color polymorphic neotropical frog with two distinctive antipredator strategies: aposematism and crypsis. The conspicuous coloration and calling behavior of aposematic males may attract both cryptic and aposematic females, but predation may select against cryptic females choosing aposematic males. We used an experimental approach where domestic fowl were encouraged to find digitized images of cryptic frogs at different distances from aposematic partners. We found that the estimated survival time of a cryptic frog was reduced when associating with an aposematic partner. Hence, predation may act as a direct selective force on female choice, favoring evolution of color assortative mating that, in turn, may strengthen the divergence in coloration that natural selection has generated.     

Warning signals are seductive: Relative contributions of color and pattern to predator avoidance and mate attraction in Heliconius butterflies

Visual signaling in animals can serve many uses, including predator deterrence and mate attraction. In many cases, signals used to advertise unprofitability to predators are also used for intraspecific communication. Although aposematism and mate choice are significant forces driving the evolution of many animal phenotypes, the interplay between relevant visual signals remains little explored. Here, we address this question in the aposematic passion‐vine butterfly Heliconius erato by using color‐ and pattern‐manipulated models to test the contributions of different visual features to both mate choice and warning coloration. We found that the relative effectiveness of a model at escaping predation was correlated with its effectiveness at inducing mating behavior, and in both cases wing color was more predictive of presumptive fitness benefits than wing pattern. Overall, however, a combination of the natural (local) color and pattern was most successful for both predator deterrence and mate attraction. By exploring the relative contributions of color versus pattern composition in predation and mate preference studies, we have shown how both natural and sexual selection may work in parallel to drive the evolution of specific animal color patterns.     

Conditions for the spread of conspicuous warning signals: a numerical model with novel insights

The initial evolution of conspicuous warning signals presents an evolutionary problem because selection against rare conspicuous signals is presumed to be strong, and new signals are rare when they first arise. Several possible solutions have been offered to solve this apparent evolutionary paradox, but disagreement persists over the plausibility of some of the proposed mechanisms. In this paper, we construct a deterministic numerical simulation model that allows us to derive the strength of selection on novel warning signals in a wide range of biologically relevant situations. We study the effects of predator psychology (learning, rate of mistaken attacks, and neophobia) on selection. We also study the how prey escape, predation intensity, number of predators, and abundance of different prey types affects selection. The model provides several important results. Selection on novel warning signals is number rather than frequency dependent. In most cases, there exists a threshold number of aposematic individuals below which aposematism is selected against and above which aposematism is selected for. Signal conspicuousness (which increases detection rate) and distinctiveness (which allows predator to distinguish defended from nondefended prey) have opposing effects on evolution of warning signals. A more conspicuous warning signal cannot evolve unless it makes the prey more distinctive from palatable prey, reducing mistaken attacks by predators. A novel warning signal that is learned quickly can spread from lower abundance more easily than a signal that is learned more slowly. However, the relative rate at which the resident signal and the novel signal are learned is irrelevant for the spread of the novel signal. Long-lasting neophobia can facilitate the spread of novel warning signals. Individual selection via the ability of defended prey to escape from predator is not likely to facilitate evolution of conspicuous warning signals if both the resident (cryptic) morph and the novel morph have the same escape probability. Predation intensity (defined as the proportion of palatable prey eaten by the predator) has a strong effect on selection. More intense predation results in strong selection against rare signals, but also strong selective advantage to common signals. The threshold number of aposematic individuals is lower when predation is intense. Thus, the evolution of warning signals may be more likely in environments where predation is intense. The effect of numbers of predators depends on whether predation intensity also changes. When predation intensity is constant, increasing numbers of predators raises the threshold number of aposematic individuals, and thus makes evolution of aposematism more difficult. If predation intensity increases in parallel with number of predators, the threshold number of aposematic individuals does not change much, but selection becomes more intense on both sides of the threshold.     

Assortative mating in poison-dart frogs based on an ecologically important trait

The origin of new species can be influenced by both deterministic and stochastic factors. Mate choice and natural selection may be important deterministic causes of speciation (as opposed to the essentially stochastic factors of geographic isolation and genetic drift). Theoretical models predict that speciation is more likely when mate choice depends on an ecologically important trait that is subject to divergent natural selection, although many authors have considered such mating/ecology pleiotropy, or "magic-traits" to be unlikely. However, phenotypic signals are important in both mate choice and ecological processes such as avoiding predation. In chemically defended species, it may be that the phenotypic characteristics influencing mate choice are the same signals being used to transmit a warning to potential predators, although few studies have demonstrated this in wild populations. We tested for assortative mating between two color morphs of the Strawberry Poison-Dart Frog, Dendrobates pumilio, a group with striking geographic variation in aposematic color patterns. We found that females significantly prefer individuals of their own morph under two different light treatments, indicating strong assortative mating based on multiple coloration cues that are also important ecological signals. This study provides a rare example of one phenotypic trait affecting both ecological viability and nonrandom mating, indicating that mating/ecology pleiotropy is plausible in wild populations, particularly for organisms that are aposematically colored and visually orienting.     

THE DUAL BENEFITS OF APOSEMATISM: PREDATOR AVOIDANCE AND ENHANCED RESOURCE COLLECTION

Theories of aposematism often focus on the idea that warning displays evolve because they work as effective signals to predators. Here, we argue that aposematism may instead evolve because, by enhancing protection, it enables animals to become more exposed and thereby gain resource‐gathering benefits, for example, through a wider foraging niche. Frequency‐dependent barriers (caused by enhanced conspicuousness relative to other prey and low levels of predator education) are generally assumed to make the evolution of aposematism particularly challenging. Using a deterministic, evolutionary model we show that aposematic display could evolve relatively easily if it enabled prey to move more freely around their environments, or become exposed in some other manner that provides fitness benefits unrelated to predation risk. Furthermore, the model shows that the traits of aposematic conspicuousness and behavior which lead to raised exposure positively affect each other, so that the optimal level of both tends to increase when the traits exist together, compared to when they exist in isolation. We discuss the ecological and evolutionary consequences of aposematism. One conclusion is that aposematism could be a key evolutionary innovation, because by widening habitat use it may promote adaptive radiation as a byproduct of enhanced ecological opportunity.     

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.     

Inbreeding and courtship calling in the cricket Teleogryllus commodus

Male field crickets produce two acoustic signals for mating: advertisement calls and courtship calls. While the importance of advertisement calling in mate attraction is well understood, the function of courtship calling is less clear. Here, we tested if the courtship call of male crickets Teleogryllus commodus signals aspects of male quality by comparing the calls of inbred and outbred males. We examined the effect of one generation of full sibling mating on fine‐scale call structure, along with several life history traits. Inbreeding reduced nymph survival but had no significant effect on weight or development time. Inbreeding resulted in a small but significant change in two of the six call parameters measured. We then tested if inbreeding affects call trait combinations that are important to females by using the results of a previous selection analysis to compare the multivariate attractiveness of the calls of inbred and outbred males. There was no difference. We conclude that the courtship call of T. commodus is not a reliable signal of aspects of male quality that are affected by inbreeding (which generally reduces fitness‐enhancing traits). It might, however, signal components of male fitness that are not affected by changes in heterozygosity.     

Are aposematic signals honest? A review

We explore the relevance of honest signalling theory to the evolution of aposematism. We begin with a general consideration of models of signal stability, with a focus on the Zahavian costly signalling framework. Next, we review early models of signalling in the context of aposematism (some that are consistent and some inconsistent with costly honest signalling). We focus on controversies surrounding the idea that aposematic signals are handicaps in a Zahavian framework. Then, we discuss how the alignment of interests between signaller and predator influences the evolution of aposematism, highlight the distinction between qualitative and quantitative honesty and review theory and research relevant to these categories. We also review recent theoretical treatments of the evolution of aposematism that have focused on honest signalling as well as empirical research on a variety of organisms, including invertebrates and frogs. Finally, we discuss future directions for empirical and theoretical research in this area.     

Predator experience on cryptic prey affects the survival of conspicuous aposematic prey

Initially, aposematism, which is an unprofitable trait, e.g. noxiousness conspicuously advertised to predators, appears to be a paradox since conspicuousness should increase predation by naive predators. However, reluctance of predators for eating novel prey (e.g. neophobia) might balance the initial predation caused by inexperienced predators. We tested the novelty effects on initial predation and avoidance learning in two separate conspicuousness levels of aposematic prey by using a 'novel world' method. Half of the wild great tits (Parus major) were trained to eat cryptic prey prior to the introduction of an aposematic prey, which potentially creates a bias against the aposematic morph. Both prey types were equally novel for control birds and they should not have shown any biased reluctance for eating an aposematic prey. Knowledge of cryptic prey reduced the expected initial mortality of the conspicuous morph to a random level whereas control birds initially ate the conspicuous morph according to the visibility risk. Birds learned to avoid conspicuous prey in both treatments but knowledge of cryptic prey did not increase the rate of avoidance learning. Predators' knowledge of cryptic prey did not reduce the predation of the less conspicuous aposematic prey and additionally predators did not learn to avoid the less conspicuous prey. These results indicate that predator psychology, which was shown as reluctance for attacking novel conspicuous prey, might have been important in the evolution of aposematism.     

Paradox lost: variable colour-pattern geometry is associated with differences in movement in aposematic frogs

Aposematic signal variation is a paradox: predators are better at learning and retaining the association between conspicuousness and unprofitability when signal variation is low. Movement patterns and variable colour patterns are linked in non-aposematic species: striped patterns generate illusions of altered speed and direction when moving linearly, affecting predators'' tracking ability; blotched patterns benefit instead from unpredictable pauses and random movement. We tested whether the extensive colour-pattern variation in an aposematic frog is linked to movement, and found that individuals moving directionally and faster have more elongated patterns than individuals moving randomly and slowly. This may help explain the paradox of polymorphic aposematism: variable warning signals may reduce protection, but predator defence might still be effective if specific behaviours are tuned to specific signals. The interacting effects of behavioural and morphological traits may be a key to the evolution of warning signals.     

Female greater wax moths reduce sexual display behavior in relation to the potential risk of predation by echolocating bats

Female greater wax moths Galleria mellonella display by wing fanning in response to bursts of ultrasonic calls produced bymales. The temporal and spectral characteristics of these callsshow some similarities with the echolocation calls of batsthat emit frequency-modulated (FM) signals. Female G. mellonellatherefore need to distinguish between the attractive signalsof male conspecifics, which may lead to mating opportunities,and similar sounds made by predatory bats. We therefore predictedthat (1) females would display in response to playbacks of male calls; (2) females would not display in response to playbacksof the calls of echolocating bats (we used the calls of Daubenton'sbat Myotis daubentonii as representative of a typical FM echolocatingbat); and (3) when presented with male calls and bat callsduring the same time block, females would display more whenperceived predation risk was lower. We manipulated predationrisk in two ways. First, we varied the intensity of bat callsto represent a nearby (high risk) or distant (low risk) bat.Second, we played back calls of bats searching for prey (lowrisk) and attacking prey (high risk). All predictions weresupported, suggesting that female G. mellonella are able todistinguish conspecific male mating calls from bat calls, andthat they modify display rate in relation to predation risk.The mechanism (s) by which the moths separate the calls ofbat and moth must involve temporal cues. Bat and moth signalsdiffer considerably in duration, and differences in durationcould be encoded by the moth's nervous system and used in discrimination.     

Behavioural elements reflect phenotypic colour divergence in a poison frog

The coexistence of both aposematic and cryptic morphs as different anti-predator strategies within a species seems to be an unusual phenomenon in nature. The strawberry poison frog, Oophaga pumilio, shows an astonishing colour diversity among populations in western Panama. In this study we selected a red and a green colour morph from two Panamanian islands (Isla Solarte and Isla Colón) for behavioural observations and measurements of conspicuousness. We found that red frogs were more visible to both conspecific frogs and potential predators than green frogs. Interestingly the difference in conspicuousness was most pronounced at the substrate that males used as principal calling places. Red males were more active and spent more time foraging than green males, which spent more time hidden. The association between conspicuousness of colouration and behaviour results in a more aposematic and a more cryptic anti-predator strategy. This is the first study which links differences in conspicuousness between animals on their natural backgrounds to differences in foraging as well as anti-predator behaviour and discusses the results in light of previous findings of toxicity analyses and potential costs and benefits of aposematism. To this end, our study adds a novel perspective for explaining extreme colour diversity between populations within an initially aposematic species.     

Conspicuous visual signals do not coevolve with increased body size in marine sea slugs

Many taxa use conspicuous colouration to attract mates, signal chemical defences (aposematism) or for thermoregulation. Conspicuousness is a key feature of aposematic signals, and experimental evidence suggests that predators avoid conspicuous prey more readily when they exhibit larger body size and/or pattern elements. Aposematic prey species may therefore evolve a larger body size due to predatory selection pressures, or alternatively, larger prey species may be more likely to evolve aposematic colouration. Therefore, a positive correlation between conspicuousness and body size should exist. Here, we investigated whether there was a phylogenetic correlation between the conspicuousness of animal patterns and body size using an intriguing, understudied model system to examine questions on the evolution of animal signals, namely nudibranchs (opisthobranch molluscs). We also used new ways to compare animal patterns quantitatively with their background habitat in terms of intensity variance and spatial frequency power spectra. In studies of aposematism, conspicuousness is usually quantified using the spectral contrast of animal colour patches against its background; however, other components of visual signals, such as pattern, luminance and spectral sensitivities of potential observers, are largely ignored. Contrary to our prediction, we found that the conspicuousness of body patterns in over 70 nudibranch species decreased as body size increased, indicating that crypsis was not limited to a smaller body size. Therefore, alternative selective pressures on body size and development of colour patterns, other than those inflicted by visual hunting predators, may act more strongly on the evolution of aposematism in nudibranch molluscs.     

Rapid population divergence linked with co-variation between coloration and sexual display in strawberry poison frogs

The likelihood of speciation is assumed to increase when sexually selected traits diverge together with ecologically important traits. According to sexual selection theory, the evolution of exaggerated display behavior is driven by increased mating success, but limited by natural selection, for example, through predation. However, the evolution of aposematic coloration (i.e., an ecologically important trait) could relieve the evolution of exaggerated display behavior from the bound of predation, resulting in joint divergence in aposematic coloration and sexual display behavior between populations. We tested this idea by examining conspicuousness, using color contrasts between individuals and their native backgrounds, and sexual display of 118 males from genetically diverged populations of the Strawberry poison frog, Dendrobates pumilio. Our results show that the level of conspicuousness of the population predicts the sexual display behavior of males. Males from conspicuous populations used more exposed calling sites. We argue that changes in aposematic coloration may rapidly cause not only postmating isolation due to poorly adapted hybrids, but also premating isolation through shifts in mating behaviors.     

Linking the evolution and form of warning coloration in nature

Many animals are toxic or unpalatable and signal this to predators with warning signals (aposematism). Aposematic appearance has long been a classical system to study predator–prey interactions, communication and signalling, and animal behaviour and learning. The area has received considerable empirical and theoretical investigation. However, most research has centred on understanding the initial evolution of aposematism, despite the fact that these studies often tell us little about the form and diversity of real warning signals in nature. In contrast, less attention has been given to the mechanistic basis of aposematic markings; that is, ‘what makes an effective warning signal?’, and the efficacy of warning signals has been neglected. Furthermore, unlike other areas of adaptive coloration research (such as camouflage and mate choice), studies of warning coloration have often been slow to address predator vision and psychology. Here, we review the current understanding of warning signal form, with an aim to comprehend the diversity of warning signals in nature. We present hypotheses and suggestions for future work regarding our current understanding of several inter-related questions covering the form of warning signals and their relationship with predator vision, learning, and links to broader issues in evolutionary ecology such as mate choice and speciation.     

Warning displays in spiny animals: one (more) evolutionary route to aposematism

To date, theoretical or laboratory simulations of aposematic evolution in prey animals have focused narrowly on internally stored chemical defense as the source of unprofitability and ignore aposematic advertisement of physical defenses such as spines (and defensive hairs, claws, etc.). This has occurred even though aposematism in spiny animals has been recognized since the 19th century. In this paper we present the first detailed theoretical consideration of aposematism in spiny animals, focusing on questions of initial evolution, costs of display, and coevolution of displays with defenses. Using an individual-based evolutionary model, we found that spines (or similar physical defenses) can easily evolve without aposematism, but when spines do evolve, aposematic displays can also easily evolve if they help to make the prey animal distinctive and if they draw attention to the physical threat. When aposematic displays evolve, they cause reduced investment in costly spines, so that, in addition to signaling unprofitability, aposematic display may enhance the cost-effectiveness of antipredator defenses (one exception to this conclusion is if the display is itself as costly as the defense). For animals with stinging spines, combining physical and chemical defense, the evolution of aposematic display may lead to reduced investment in the toxin compared to the spine. This occurs because spines act as both secondary (repellent) defenses and as primary defenses (their own visible, honest advertisement), whereas internally stored toxins only (generally) act as repellent secondary defenses. We argue that conspicuous aposematism in spines functions as an attention-getting mechanism, whereas conspicuous aposematic display in purely toxic animals may be explained by signal reliability arguments. Finally, one (more) route by which aposematism may initially evolve is by spiny rather than purely chemically defended species, spreading to species with other forms of secondary defense as the signal becomes common.     

Identifying the ecological conditions that select for intermediate levels of aposematic signalling

Chemically defended species often have conspicuous signals that warn potential predators of these defences. Recent evidence suggests that some such aposematic prey are not as conspicuous as possible, even though increased conspicuousness would bring additional anti-predator benefits. Here we present a simple model to explore the generality of these observations. Our model predicts that optimal fitness will often be achieved at an intermediate level of conspicuousness and not simply by maximising conspicuousness. This comes about because of the ubiquitous trade-off that increased conspicuousness has an ecological cost in increasing the encounter rate with predators, as well as a benefit in terms of enhancing learned aversion by predators of defended prey. However, importantly, we also predict that a small deviation away from maximal crypsis generally causes a decrease in fitness, even if a larger deviation would lead to an intermediate level of conspicuousness that maximises fitness. Hence, further consideration of whether intermediate levels of aposematism are as common in nature as predicted in this model will require consideration of the underlying evolution of appearance, and the plausibility of evolution across the fitness trough, from maximal crypsis to an intermediate level of aposematism.     

Primate copulation calls and postcopulatory female choice

Females in some species of Old World monkeys and apes vocalizeafter copulation, but the function of these vocalizations isnot clear. In this article, we examine the hypothesis that copulationcalls are a form of postcopulatory female choice. Accordingto this hypothesis, copulation calls are honest signals of fertility(i.e., ovulation) that are used by females to encourage mateguarding by their preferred mating partners and reduce the likelihoodof sperm competition. Evidence in favor of this hypothesis isreviewed and discussed in relation to other hypotheses. We suggestthat the evolution of female copulation calls in primates islinked to the evolution of other female mating signals suchas exaggerated sexual swellings, the potential for sperm competition,and the opportunity for precopulatory female mate choice.     

Protection by association: evidence for aposematic commensalism

Aposematism is a well known and widely used strategy for reducing predation by conspicuous signalling of unprofitability. However, the increased conspicuousness could make this strategy costly if there are no secondary defences to back the signal up. This has made the elucidation of the evolutionary mechanisms for aposematism and that of the closely‐related Batesian and Mullerian mimicry difficult. The present study aims to test whether cryptic and nondefended prey could reduce their predation risk by grouping with aposematic and defended prey. To do this, we used groups of artificial baits that were either cryptic and palatable or conspicuous and unpalatable, along with the corresponding control treatments. These were then presented in mixed and homogeneous treatment groups within a field setting and the local wild bird assemblage was allowed to select and remove baits at will. The results obtained show that undefended non‐aposematic prey can benefit by grouping with aposematic prey, with no evidence that predation rates for aposematic prey were adversely affected by this association. These results provide insights into the evolution of Batesian mimicry. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 81–89.     

INBREEDING AND ADVERTISEMENT CALLING IN THE CRICKET TELEOGRYLLUS COMMODUS: LABORATORY AND FIELD EXPERIMENTS

If sexually selected traits reveal a male's heterozygosity or condition to females, then such traits should exhibit declines with inbreeding. We tested this by examining the effect of inbreeding on advertisement calling in male crickets Teleogryllus commodus. We investigated the effect of one generation of full‐sibling mating on calling effort and fine‐scale call structure. Inbreeding reduced calling effort but had no effect on call structure. We then compared the attractiveness of inbred and outbred calls in the field by monitoring how many wild females were attracted to each call type. From the field data, we conducted a selection analysis to identify the major axes of linear and nonlinear multivariate sexual selection on call structure. A comparison of multivariate attractiveness of inbred and outbred calls along each major axis of selection revealed no difference in attractiveness. Our results suggest that inbred male calls have a fine‐scale structure that is no less attractive to females than that of outbred calls. However, because inbred males call less often, and female T. commodus prefer males with a higher calling effort, inbred males will suffer reductions in mating success. Females who base mate choice on call rate are therefore using a signal correlated with male heterozygosity and/or condition.