Taste and pheromonal inputs govern the regulation of time investment for mating by sexual experience in male Drosophila melanogaster.

Males have finite resources to spend on reproduction. Thus, males rely on a 'time investment strategy' to maximize their reproductive success. For example, male Drosophila melanogaster extends their mating duration when surrounded by conditions enriched with rivals. Here we report a different form of behavioral plasticity whereby male fruit flies exhibit a shortened duration of mating when they are sexually experienced; we refer to this plasticity as 'shorter-mating-duration (SMD)'. SMD is a plastic behavior and requires sexually dimorphic taste neurons. We identified several neurons in the male foreleg and midleg that express specific sugar and pheromone receptors. Using a cost-benefit model and behavioral experiments, we further show that SMD behavior exhibits adaptive behavioral plasticity in male flies. Thus, our study delineates the molecular and cellular basis of the sensory inputs required for SMD; this represents a plastic interval timing behavior that could serve as a model system to study how multisensory inputs converge to modify interval timing behavior for improved adaptation.

Selection for evasive mimicry imposed by an arthropod predator.

It has long been hypothesized that a species that is relatively easy to catch by predators may face selection to resemble a species that is harder to catch. Several experiments using avian predators have since supported this 'evasive mimicry' hypothesis. However, the sudden movement of artificial evasive prey in each of the above experiments may have startled the predators, generating an avoidance response unrelated to difficulty of capture. Additionally in the above experiments the catchability of prey was all or nothing, while in nature predators may occasionally catch evasive prey or fail to catch slower species, which might inhibit learning. Here, using mantids as predators, we conducted an experimental test of the evasive mimicry hypothesis that circumvents these limitations, using live painted calyptrate flies with modified evasive capabilities as prey. We found that mantids readily learned to avoid pursuing the more evasive prey types. Warning signals based on evasiveness and their associated mimicry may be widespread phenomena in nature. These findings not only further support its plausibility but demonstrate that even arthropod predators can select for it.

The evolution and ecology of multiple antipredator defences.

Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such "defence portfolios" that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade-offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.

Climate-induced phenological shifts in a Batesian mimicry complex.

Climate-induced changes in spatial and temporal occurrence of species, as well as species traits such as body size, each have the potential to decouple symbiotic relationships. Past work has focused primarily on direct interactions, particularly those between predators and prey and between plants and pollinators, but studies have rarely demonstrated significant fitness costs to the interacting, coevolving organisms. Here, we demonstrate that changing phenological synchrony in the latter part of the 20th century has different fitness outcomes for the actors within a Batesian mimicry complex, where predators learn to differentiate harmful "model" organisms (stinging Hymenoptera) from harmless "mimics" (hoverflies, Diptera: Syrphidae). We define the mimetic relationships between 2,352 pairs of stinging Hymenoptera and their Syrphidae mimics based on a large-scale citizen science project and demonstrate that there is no relationship between the phenological shifts of models and their mimics. Using computer game-based experiments, we confirm that the fitness of models, mimics, and predators differs among phenological scenarios, creating a phenologically antagonistic system. Finally, we show that climate change is increasing the proportion of mimetic interactions in which models occur first and reducing mimic-first and random patterns of occurrence, potentially leading to complex fitness costs and benefits across all three actors. Our results provide strong evidence for an overlooked example of fitness consequences from changing phenological synchrony.

The anti-predation benefit of flash displays is related to the distance at which the prey initiates its escape.

Flash behaviour is widespread in the animal kingdom and describes the exposure of a hidden conspicuous signal as an animal flees from predators. Recent studies have demonstrated that the signal can enhance survivorship by leading pursuing predators into assuming the flasher is also conspicuous at rest. Naturally, this illusion will work best if potential predators are ignorant of the flasher's resting appearance, which could be achieved if the prey flees while the predator is relatively far away. To test this hypothesis, we compared the survival of flashing and non-flashing computer-generated prey with different flight initiation distances (FIDs) using humans as model predators. This experiment found that flash displays confer a survivorship advantage only to those prey with a long FID. A complementary phylogenetic analysis of Australian bird species supports these results: after controlling for body size, species with putative flashing signals had longer FIDs than those without. Species with putative flashing signals also tended to be larger, as demonstrated in other taxa. The anti-predation benefit of flash displays is therefore related to the nature of escape behaviour. Since birds with hidden signals tend to flee at a distance, the flash display here is unlikely to function by startling would-be predators.

State-Dependent Decision-Making by Predators and Its Consequences for Mimicry.

AbstractThe mimicry of one species by another provides one of the most celebrated examples of evolution by natural selection. Edible Batesian mimics deceive predators into believing they may be defended, whereas defended Müllerian mimics have evolved a shared warning signal, more rapidly educating predators to avoid them. However, it may benefit hungry predators to attack defended prey, while the benefits of learning about unfamiliar prey depends on the future value of this information. Previous energetic state-dependent models of predator foraging behavior have assumed complete knowledge, while informational state-dependent models have assumed fixed levels of hunger. Here, we identify the optimal decision rules of predators accounting for both energetic and informational states. We show that the nature of mimicry is qualitatively and quantitatively affected by both sources of state dependence. Associative learning weakens the extent of parasitic mimicry by edible prey because naive predators often attack defended models. More importantly, mimicry among equally highly defended prey may be parasitic or mutualistic depending on the ecological context (e.g., the source of mimics and the abundance of alternative prey). Finally, mimicry by prey with intermediate defenses corresponds to Batesian or Müllerian mimicry depending on whether the mimic is profitable to attack by hungry predators, but it is not a special case of mimicry.

Prey with hidden colour defences benefit from their similarity to aposematic signals.

Some camouflaged animals hide colour signals and display them only transiently. These hidden colour signals are often conspicuous and are used as a secondary defence to warn or startle predators (deimatic displays) and/or to confuse them (flash displays). The hidden signals used in these displays frequently resemble typical aposematic signals, so it is possible that prey with hidden signals have evolved to employ colour patterns of a form that predators have previously learned to associate with unprofitability. Here, we tested this hypothesis by conducting two experiments that examined the effect of predator avoidance learning on the efficacy of deimatic and flash displays. We found that the survival benefits of both deimatic and flash displays were substantially higher against predators that had previously learned to associate the hidden colours with unprofitability than against naive predators. These findings help explain the phenological patterns we found in 1568 macro-lepidopteran species on three continents: species with hidden signals tend to occur later in the season than species without hidden signals.

Consistent Associations between Body Size and Hidden Contrasting Color Signals across a Range of Insect Taxa.

While there have been a number of recent advances in our understanding of the evolution of animal color patterns, much of this work has focused on color patterns that are constantly displayed. However, some animals hide functional color signals and display them only transiently through behavioral displays. These displays are widely employed as a secondary defense following detection when fleeing (flash display) or when stationary (deimatic display). Yet if displays of hidden colors are so effective in deterring predation, why have not all species evolved them? An earlier study suggested that the hidden antipredatory color signals in insects are more likely to have evolved in species with large size because either (or both) (i) large cryptic prey are more frequently detected and pursued or (ii) hidden color signals in large prey are more effective in deterring predation than in small prey. These arguments should apply universally to any prey that use hidden signals, so the association between large size and hidden contrasting color signals should be evident across diverse groups of prey. In this study, we tested this prediction in five different groups of insects. Using phylogenetically controlled analysis to elucidate the relationship between body size and color contrast between forewings and hind wings, we found evidence for the predicted size-color contrast associations in four different groups of insects, namely, Orthoptera, Phasmatidae, Mantidae, and Saturniidae, but not in Sphingidae. Collectively, our study indicates that body size plays an important role in explaining variation in the evolution of hidden contrasting color signals in insects.

A comparative analysis of the evolution of imperfect mimicry.

Although exceptional examples of adaptation are frequently celebrated, some outcomes of natural selection seem far from perfect. For example, many hoverflies (Diptera: Syrphidae) are harmless (Batesian) mimics of stinging Hymenoptera. However, although some hoverfly species are considered excellent mimics, other species bear only a superficial resemblance to their models and it is unclear why this is so. To evaluate hypotheses that have been put forward to explain interspecific variation in the mimetic fidelity of Palearctic Syrphidae we use a comparative approach. We show that the most plausible explanation is that predators impose less selection for mimetic fidelity on smaller hoverfly species because they are less profitable prey items. In particular, our findings, in combination with previous results, allow us to reject several key hypotheses for imperfect mimicry: first, human ratings of mimetic fidelity are positively correlated with both morphometric measures and avian rankings, indicating that variation in mimetic fidelity is not simply an illusion based on human perception; second, no species of syrphid maps out in multidimensional space as being intermediate in appearance between several different hymenopteran model species, as the multimodel hypothesis requires; and third, we find no evidence for a negative relationship between mimetic fidelity and abundance, which calls into question the kin-selection hypothesis. By contrast, a strong positive relationship between mimetic fidelity and body size supports the relaxed-selection hypothesis, suggesting that reduced predation pressure on less profitable prey species limits the selection for mimetic perfection.

Body size affects the evolution of eyespots in caterpillars.

Many caterpillars have conspicuous eye-like markings, called eyespots. Despite recent work demonstrating the efficacy of eyespots in deterring predator attack, a fundamental question remains: Given their protective benefits, why have eyespots not evolved in more caterpillars? Using a phylogenetically controlled analysis of hawkmoth caterpillars, we show that eyespots are associated with large body size. This relationship could arise because (i) large prey are innately conspicuous; (ii) large prey are more profitable, and thus face stronger selection to evolve such defenses; and/or (iii) eyespots are more effective on large-bodied prey. To evaluate these hypotheses, we exposed small and large caterpillar models with and without eyespots in a 2 × 2 factorial design to avian predators in the field. Overall, eyespots increased prey mortality, but the effect was particularly marked in small prey, and eyespots decreased mortality of large prey in some microhabitats. We then exposed artificial prey to naïve domestic chicks in a laboratory setting following a 2 × 3 design (small or large size × no, small, or large eyespots). Predators attacked small prey with eyespots more quickly, but were more wary of large caterpillars with large eyespots than those without eyespots or with small eyespots. Taken together, these data suggest that eyespots are effective deterrents only when both prey and eyespots are large, and that innate aversion toward eyespots is conditional. We conclude that the distribution of eyespots in nature likely results from selection against eyespots in small caterpillars and selection for eyespots in large caterpillars (at least in some microhabitats).

Mimicry among Unequally Defended Prey Should Be Mutualistic When Predators Sample Optimally.

Understanding the conditions under which moderately defended prey evolve to resemble better-defended prey and whether this mimicry is parasitic (quasi-Batesian) or mutualistic (Müllerian) is central to our understanding of warning signals. Models of predator learning generally predict quasi-Batesian relationships. However, predators' attack decisions are based not only on learning alone but also on the potential future rewards. We identify the optimal sampling strategy of predators capable of classifying prey into different profitability categories and contrast the implications of these rules for mimicry evolution with a classical Pavlovian model based on conditioning. In both cases, the presence of moderately unprofitable mimics causes an increase in overall consumption. However, in the case of the optimal sampling strategy, this increase in consumption is typically outweighed by the increase in overall density of prey sharing the model appearance (a dilution effect), causing a decrease in mortality. It suggests that if predators forage efficiently to maximize their long-term payoff, genuine quasi-Batesian mimicry should be rare, which may explain the scarcity of evidence for it in nature. Nevertheless, we show that when moderately defended mimics are profitable to attack by hungry predators, then they can be parasitic on their models, just as classical Batesian mimics are.

Body size affects the evolution of hidden colour signals in moths.

Many cryptic prey have also evolved hidden contrasting colour signals which are displayed to would-be predators. Given that these hidden contrasting signals may confer additional survival benefits to the prey by startling/intimidating predators, it is unclear why they have evolved in some species, but not in others. Here, we have conducted a comparative phylogenetic analysis of the evolution of colour traits in the family Erebidae (Lepidoptera), and found that the hidden contrasting colour signals are more likely to be found in larger species. To understand why this relationship occurs, we present a general mathematical model, demonstrating that selection for a secondary defence such as deimatic display will be stronger in large species when (i) the primary defence (crypsis) is likely to fail as its body size increases and/or (ii) the secondary defence is more effective in large prey. To test the model assumptions, we conducted behavioural experiments using a robotic moth which revealed that survivorship advantages were higher against wild birds when the moth has contrasting hindwings and large size. Collectively, our results suggest that the evolutionary association between large size and hidden contrasting signals has been driven by a combination of the need for a back-up defence and its efficacy.

Costs of Learning and the Evolution of Mimetic Signals.

Predators must use the appearance of their prey to decide whether it is likely to be defended. Most theory assumes that predators have completed learning about prey appearance, yet we do not understand how predators learn which aspects of appearance to use for classifying prey. If sampling prey can be risky, predators might forgo opportunities to learn about the relationship between prey appearance and defense. Using Bayesian inference and dynamic programming, we modeled how the immediate risks and future rewards of learning about prey appearance influence how predators learn. In addition, we explored how variation in predator learning affects the evolution of mimicry, which occurs when two prey evolve to share a common signal to predators. We found that when learning about prey with distinct appearances was expensive, optimal predators tended to lump them into the same category or exhibit an unwillingness to sample at all (neophobia). This resulted in a reduction in selection for defensive mimicry. However, the same predator behavior favored the evolution of aggressive mimicry, because in that case, mimics benefited from being sampled. When prey were very rare and costs of sampling them were high, predators exhibited neophobia, refusing to attack. This behavior could forestall the evolution of mimicry and instead select for polymorphism.

Frequency-dependent selection on female morphs driven by premating interactions with males.

Species showing color polymorphisms-the presence of two or more genetically determined color morphs within a single population-are excellent systems for studying the selective forces driving the maintenance of genetic diversity. Despite a shortage of empirical evidence, it is often suggested that negative frequency-dependent mate preference by males (or diet choice by predators) results in fitness benefits for the rare female morph (or prey type). Moreover, most studies have focused on the male (or predator) behavior in these systems and largely overlooked the importance of female (or prey) resistance behavior. Here, we provide the first explicit test of the role of frequency-dependent and frequency-independent intersexual interactions in female polymorphic damselflies. We identify the stage of the mating sequence when frequency-dependent selection is likely to act by comparing indexes of male mate preference when the female has little (females presented on sticks), moderate (females in cages), and high (females free to fly in the field) ability to avoid male mating attempts. Frequency-dependent male preferences were found only in those experiments where females had little ability to resist male harassment, indicating that premating interactions most likely drive negative frequency-dependent selection in this system. In addition, by separating frequency-dependent male mating preference from the baseline frequency-independent component, we reconcile the seemingly contradictory results of previous studies and highlight the roles of both forms of selection in maintaining the polymorphism at a given equilibrium. We conclude that considering interactions among all players-here, males and females-is crucial to fully understanding the mechanisms underlying the maintenance of genetic polymorphisms in the wild.

Live fast, die old: no evidence of reproductive senescence or costs of mating in a damselfly (Odonata: Zygoptera).

Recent examples of actuarial senescence in wild insect populations have challenged the long-held assumption that the brevity of wild insect life spans precludes senescence. We investigate age-related patterns in mating behaviour in adults of a short-lived damselfly, Coenagrion puella and the implications of this mating. Using capture histories for 1033 individuals over two field seasons, we conduct both pooled and stratified analyses of variations in breeding activity. Pooled analyses suggest that there is strong age-related variation in the probability of being present at the mating rendezvous. However, no age-related variation was observed in the probability of mating. Stratified approaches confirmed a general pattern of age-related declines in survival probability, but provided only equivocal evidence of an effect of age on transition between temporary breeding states. Mating males and females showed greater survival than non-mating individuals, possibly as a consequence of higher body condition. Older males that were not currently breeding were less likely to commence breeding on the next day, but showed no patterns in breeding cessation. Overall, transitions between both breeding states declined with age, suggesting that males that breed tend to continue breeding while those that do not breed continue to be unsuccessful. Female mating rates were consistently high across all ages with no age-related decline apparent. While previous research has demonstrated actuarial senescence in this population, as does this study, we find little evidence of either age-related declines in reproductive behaviour or breeding-related declines in survival, which might indicate functional senescence or costs of mating, respectively. Indeed, the greater survival in mating individuals of both sexes suggests that variations in individual quality may mediate both reproductive success and longevity. Contrary to recent studies, we found no compelling evidence for reproductive senescence or a cost of mating in an important and well-studied model odonate. The possible link between condition and ageing suggests that individual quality needs to be taken into account when studying senescence. We recommend the use of multistrata models for the future investigation of these phenomena.

The relationship between morphological and behavioral mimicry in hover flies (Diptera: Syrphidae).

Palatable (Batesian) mimics of unprofitable models could use behavioral mimicry to compensate for the ease with which they can be visually discriminated or to augment an already close morphological resemblance. We evaluated these contrasting predictions by assaying the behavior of 57 field-caught species of mimetic hover flies (Diptera: Syrphidae) and quantifying their morphological similarity to a range of potential hymenopteran models. A purpose-built phylogeny for the hover flies was used to control for potential lack of independence due to shared evolutionary history. Those hover fly species that engage in behavioral mimicry (mock stinging, leg waving, wing wagging) were all large wasp mimics within the genera Spilomyia and Temnostoma. While the behavioral mimics assayed were good morphological mimics, not all good mimics were behavioral mimics. Therefore, while the behaviors may have evolved to augment good morphological mimicry, they do not advantage all good mimics.

Why fruit rots: theoretical support for Janzen's theory of microbe-macrobe competition.

We present a formal model of Janzen's influential theory that competition for resources between microbes and vertebrates causes microbes to be selected to make these resources unpalatable to vertebrates. That is, fruit rots, seeds mould and meat spoils, in part, because microbes gain a selective advantage if they can alter the properties of these resources to avoid losing the resources to vertebrate consumers. A previous model had failed to find circumstances in which such a costly spoilage trait could flourish; here, we present a simple analytic model of a general situation where costly microbial spoilage is selected and persists. We argue that the key difference between the two models lies in their treatments of microbial dispersal. If microbial dispersal is sufficiently spatially constrained that different resource items can have differing microbial communities, then spoilage will be selected; however, if microbial dispersal has a strong homogenizing effect on the microbial community then spoilage will not be selected. We suspect that both regimes will exist in the natural world, and suggest how future empirical studies could explore the influence of microbial dispersal on spoilage.

Negative frequency-dependent selection or alternative reproductive tactics: maintenance of female polymorphism in natural populations.

BACKGROUND: Sex-limited polymorphisms have long intrigued evolutionary biologists and have been the subject of long-standing debates. The coexistence of multiple male and/or female morphs is widely believed to be maintained through negative frequency-dependent selection imposed by social interactions. However, remarkably few empirical studies have evaluated how social interactions, morph frequencies and fitness parameters relate to one another under natural conditions. Here, we test two hypotheses proposed to explain the maintenance of a female polymorphism in a species with extreme geographical variation in morph frequencies. We first elucidate how fecundity traits of the morphs vary in relation to the frequencies and densities of males and female morphs in multiple sites over multiple years. Second, we evaluate whether the two female morphs differ in resource allocation among fecundity traits, indicating alternative tactics to maximize reproductive output. RESULTS: We present some of the first empirical evidence collected under natural conditions that egg number and clutch mass was higher in the rarer female morph. This morph-specific fecundity advantage gradually switched with the population morph frequency. Our results further indicate that all investigated fecundity traits are negatively affected by relative male density (i.e. operational sex ratio), which confirms male harassment as selective agent. Finally, we show a clear trade-off between qualitative (egg mass) and quantitative (egg number) fecundity traits. This trade-off, however, is not morph-specific. CONCLUSION: Our reported frequency- and density-dependent fecundity patterns are consistent with the hypothesis that the polymorphism is driven by a conflict between sexes over optimal mating rate, with costly male sexual harassment driving negative frequency-dependent selection on morph fecundity.

Disruptive camouflage impairs object recognition.

Whether hiding from predators, or avoiding battlefield casualties, camouflage is widely employed to prevent detection. Disruptive coloration is a seemingly well-known camouflage mechanism proposed to function by breaking up an object's salient features (for example their characteristic outline), rendering objects more difficult to recognize. However, while a wide range of animals are thought to evade detection using disruptive patterns, there is no direct experimental evidence that disruptive coloration impairs recognition. Using humans searching for computer-generated moth targets, we demonstrate that the number of edge-intersecting patches on a target reduces the likelihood of it being detected, even at the expense of reduced background matching. Crucially, eye-tracking data show that targets with more edge-intersecting patches were looked at for longer periods prior to attack, and passed-over more frequently during search tasks. We therefore show directly that edge patches enhance survivorship by impairing recognition, confirming that disruptive coloration is a distinct camouflage strategy, not simply an artefact of background matching.

Signal detection models as contextual bandits.

Signal detection theory (SDT) has been widely applied to identify the optimal discriminative decisions of receivers under uncertainty. However, the approach assumes that decision-makers immediately adopt the appropriate acceptance threshold, even though the optimal response must often be learned. Here we recast the classical normal-normal (and power-law) signal detection model as a contextual multi-armed bandit (CMAB). Thus, rather than starting with complete information, decision-makers must infer how the magnitude of a continuous cue is related to the probability that a signaller is desirable, while simultaneously seeking to exploit the information they acquire. We explain how various CMAB heuristics resolve the trade-off between better estimating the underlying relationship and exploiting it. Next, we determined how naive human volunteers resolve signal detection problems with a continuous cue. As anticipated, a model of choice (accept/reject) that assumed volunteers immediately adopted the SDT-predicted acceptance threshold did not predict volunteer behaviour well. The Softmax rule for solving CMABs, with choices based on a logistic function of the expected payoffs, best explained the decisions of our volunteers but a simple midpoint algorithm also predicted decisions well under some conditions. CMABs offer principled parametric solutions to solving many classical SDT problems when decision-makers start with incomplete information.