Evolution of individual variation in a competitive trait: a theoretical analysis.

When competitive traits are costly, negative frequency dependence can maintain genetic variance. Most theoretical studies examining this problem assume binary polymorphisms, yet most trait variation in wild populations is continuous. We propose that continuous trait variation can result from continuous variation in resource quality and that, specifically, the shape of the resource distribution determines trait maintenance. We used an individual-based model to test which conditions favour the stable maintenance of variation and which cause temporal fluctuations in trait values. This approach, inspired by contrasting outcomes of previous studies regarding variance and fluctuations in trait values, clearly showed a decisive role played by the shape of resource distributions. Under extreme conditions, e.g., the absence of resource variation or with very scarce resources for weak competitors, traits evolved to a single non-competitive or highly competitive strategy, respectively. Most other distributions led to strong temporal fluctuations on trait values or the maintenance of stable, standing variation. Our results thus explain the contradicting outcomes of previous theoretical studies and, at the same time, provide hypotheses to explain the maintenance of genetic variation and individual differences. We suggest ways to empirically test the proposed effects of resource variation on trait maintenance.

Who innovates? Abundance of novel and familiar food changes which animals are most persistent.

Novel behaviours are the raw material of cultural evolution, yet we do not have a clear picture of when they are likely to arise. I use a state-dependent model to examine how individual age and energy reserves interact with the abundance of known and novel prey to promote dietary innovation (incorporating a new food item into the diet). I measure innovativeness as persistence in attempting to capture novel prey. I find a trend towards greater persistence among younger individuals. Decreased abundance of known prey and increased abundance of novel prey also favour persistence. However, many exceptions to these trends occur. These exceptions are critical because they may explain inconsistencies among studies of animal innovation. Care must be taken in experiments to control for multiple factors relevant to an animal's energy budget and foraging opportunities. We may learn more about innovation in experimental contexts by (i) manipulating the abundance of novel and familiar food resources, (ii) directly measuring animal age and condition, and-where possible-(iii) fitting nonlinear models to innovative behaviour. Results indicate that selection for persistence may also favour neophilia.

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.

Social Learning of Innovations in Dynamic Predator-Prey Systems.

AbstractWe investigate the social transmission of innovations between predators. We focus on two classic predator-prey models. We assume that innovations increase predator attack rates or conversion efficiencies or that innovations reduce predator mortality or handling time. We find that a common outcome is the destabilization of the system. Destabilizing effects include increasing oscillations or limit cycles. Particularly, in more realistic systems (where prey are self-limiting and predators have a type II functional response), destabilization occurs because of overexploitation of the prey. Whenever instability increases the risk of extinction, innovations that benefit individual predators may not have positive long-term effects on predator populations. Additionally, instability could maintain behavioral variability among predators. Interestingly, when predator populations are low despite coexisting with prey populations near their carrying capacity, innovations that could help predators better exploit their prey are least likely to spread. Precisely how unlikely this is depends on whether naive individuals need to observe an informed individual interact with prey to learn the innovation. Our findings help illuminate how innovations could affect biological invasions, urban colonization, and the maintenance of behavioral polymorphisms.

The Effect of Predator Population Dynamics on Batesian Mimicry Complexes.

AbstractUnderstanding Batesian mimicry is a classic problem in evolutionary biology. In Batesian mimicry, a defended species (the model) is mimicked by an undefended species (the mimic). Prior theories have emphasized the role of predator behavior and learning as well as evolution in model-mimic complexes but have not examined the role of population dynamics in potentially governing the relative abundances and even persistence of model-mimic systems. Here, we examined the effect of the population dynamics of predators and alternative prey on the prevalence of warning-signaling prey composed of models and mimics. Using optimal foraging theory and signal detection theory, we found that the inclusion of predator and alternative prey population dynamics could reverse traditional theoretical predictions: as alternative prey increase in numbers, mimics suffer because larger populations of predators are maintained, resulting in apparent competition. Under some circumstances, apparent competition affects model populations as well, although not as severely as it affects mimics. Our results bear on the intriguing puzzle that in nature warning signals are relatively scarce, yet experiments suggest that such signals can be highly advantageous. The availability of alternative prey and numerical responses by predators can overwhelm advantages observed in experiments to keep warning signals in model-mimic systems relatively scarce.

Why aren't warning signals everywhere? On the prevalence of aposematism and mimicry in communities.

Warning signals are a striking example of natural selection present in almost every ecological community - from Nordic meadows to tropical rainforests, defended prey species and their mimics ward off potential predators before they attack. Yet despite the wide distribution of warning signals, they are relatively scarce as a proportion of the total prey available, and more so in some biomes than others. Classically, warning signals are thought to be governed by positive density-dependent selection, i.e. they succeed better when they are more common. Therefore, after surmounting this initial barrier to their evolution, it is puzzling that they remain uncommon on the scale of the community. Here, we explore factors likely to determine the prevalence of warning signals in prey assemblages. These factors include the nature of prey defences and any constraints upon them, the behavioural interactions of predators with different prey defences, the numerical responses of predators governed by movement and reproduction, the diversity and abundance of undefended alternative prey and Batesian mimics in the community, and variability in other ecological circumstances. We also discuss the macroevolution of warning signals. Our review finds that we have a basic understanding of how many species in some taxonomic groups have warning signals, but very little information on the interrelationships among population abundances across prey communities, the diversity of signal phenotypes, and prey defences. We also have detailed knowledge of how a few generalist predator species forage in artificial laboratory environments, but we know much less about how predators forage in complex natural communities with variable prey defences. We describe how empirical work to address each of these knowledge gaps can test specific hypotheses for why warning signals exhibit their particular patterns of distribution. This will help us to understand how behavioural interactions shape ecological communities.

Sensory bias and signal detection trade-offs maintain intersexual floral mimicry.

Mimicry is common in interspecies interactions, yet conditions maintaining Batesian mimicry have been primarily tested in predator-prey interactions. In pollination mutualisms, floral mimetic signals thought to dupe animals into pollinating unrewarding flowers are widespread (greater than 32 plant families). Yet whether animals learn to both correctly identify floral models and reject floral mimics and whether these responses are frequency-dependent is not well understood. We tested how learning affected the effectiveness and frequency-dependence of imperfect Batesian mimicry among flowers using the generalist bumblebee, Bombus impatiens, visiting Begonia odorata, a plant species exhibiting intersexual floral mimicry. Unrewarding female flowers are mimics of pollen-rewarding male flowers (models), though mimicry to the human eye is imperfect. Flower-naive bees exhibited a perceptual bias for mimics over models, but rapidly learned to avoid mimics. Surprisingly, altering the frequency of models and mimics only marginally shaped responses by naive bees and by bees experienced with the distribution and frequency of models and mimics. Our results provide evidence both of exploitation by the plant of signal detection trade-offs in bees and of resistance by the bees, via learning, to this exploitation. Critically, we provide experimental evidence that imperfect Batesian mimicry can be adaptive and, in contrast with expectations of signal detection theory, functions largely independently of the model and mimic frequency. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

Biased predation could promote convergence yet maintain diversity within Müllerian mimicry rings of Oreina leaf beetles.

Müllerian mimicry is a classic example of adaptation, yet Müller's original theory does not account for the diversity often observed in mimicry rings. Here, we aimed to assess how well classical Müllerian mimicry can account for the colour polymorphism found in chemically defended Oreina leaf beetles by using field data and laboratory assays of predator behaviour. We also evaluated the hypothesis that thermoregulation can explain diversity between Oreina mimicry rings. We found that frequencies of each colour morph were positively correlated among species, a critical prediction of Müllerian mimicry. Predators learned to associate colour with chemical defences. Learned avoidance of the green morph of one species protected green morphs of another species. Avoidance of blue morphs was completely generalized to green morphs, but surprisingly, avoidance of green morphs was less generalized to blue morphs. This asymmetrical generalization should favour green morphs: indeed, green morphs persist in blue communities, whereas blue morphs are entirely excluded from green communities. We did not find a correlation between elevation and coloration, rejecting thermoregulation as an explanation for diversity between mimicry rings. Biased predation could explain within-community diversity in warning coloration, providing a solution to a long-standing puzzle. We propose testable hypotheses for why asymmetric generalization occurs, and how predators maintain the predominance of blue morphs in a community, despite asymmetric generalization.

Multiple models generate a geographical mosaic of resemblance in a Batesian mimicry complex.

Batesian mimics-benign species that receive protection from predation by resembling a dangerous species-often occur with multiple model species. Here, we examine whether geographical variation in the number of local models generates geographical variation in mimic-model resemblance. In areas with multiple models, selection might be relaxed or even favour imprecise mimicry relative to areas with only one model. We test the prediction that model-mimic match should vary with the number of other model species in a broadly distributed snake mimicry complex where a mimic and a model co-occur both with and without other model species. We found that the mimic resembled its model more closely when they were exclusively sympatric than when they were sympatric with other model species. Moreover, in regions with multiple models, mimic-model resemblance was positively correlated with the resemblance between the model and other model species. However, contrary to predictions, free-ranging natural predators did not attack artificial replicas of imprecise mimics more often when only a single model was present. Taken together, our results suggest that multiple models might generate a geographical mosaic in the degree of phenotype matching between Batesian mimics and their models.

Evaluating the utility of camera traps in field studies of predation.

Artificial prey techniques-wherein synthetic replicas of real organisms are placed in natural habitats-are widely used to study predation in the field. We investigated the extent to which videography could provide additional information to such studies. As a part of studies on aposematism and mimicry of coral snakes (Micrurus) and their mimics, observational data from 109 artificial snake prey were collected from video-recording camera traps in three locations in the Americas (terra firme forest, Tiputini Biodiversity Station, Ecuador; premontane wet forest, Nahá Reserve, Mexico; longleaf pine forest, Southeastern Coastal Plain, North Carolina, USA). During 1,536 camera days, a total of 268 observations of 20 putative snake predator species were recorded in the vicinity of artificial prey. Predators were observed to detect artificial prey 52 times, but only 21 attacks were recorded. Mammals were the most commonly recorded group of predators near replicas (243) and were responsible for most detections (48) and attacks (20). There was no difference between avian or mammalian predators in their probability of detecting replicas nor in their probability of attacking replicas after detecting them. Bite and beak marks left on clay replicas registered a higher ratio of avian:mammalian attacks than videos registered. Approximately 61.5% of artificial prey monitored with cameras remained undetected by predators throughout the duration of the experiments. Observational data collected from videos could provide more robust inferences on the relative fitness of different prey phenotypes, predator behavior, and the relative contribution of different predator species to selection on prey. However, we estimate that the level of predator activity necessary for the benefit of additional information that videos provide to be worth their financial costs is achieved in fewer than 20% of published artificial prey studies. Although we suggest future predation studies employing artificial prey to consider using videography as a tool to inspire new, more focused inquiry, the investment in camera traps is unlikely to be worth the expense for most artificial prey studies until the cost:benefit ratio decreases.

How cognitive biases select for imperfect mimicry: a study of asymmetry in learning with bumblebees.

Imperfect mimicry presents a paradox of incomplete adaptation - intuitively, closer resemblance should improve performance. Receiver psychology can often explain why mimetic signals do not always evolve to match those of their models. Here, we explored the influence of a pervasive and powerful cognitive bias where associative learning depends upon an asymmetric interaction between the cue (stimulus) and consequence (reinforcer), such as in rats, which will associate light and tone with shock, and taste with nausea, but not the converse. Can such biases alter selection for mimicry? We designed an artificial mimicry system where bees foraged on artificial flowers, so that colours could be switched between rewarding or aversive. We found that when the colour blue was paired with a sucrose reward, other cues were ignored, but not when blue was paired with aversive compounds. We also tested the hypothesis that costs of errors affect how receivers sample imperfect mimics. However, costs of errors did not affect bee visits to imperfect mimics in our study. We propose a novel hypothesis for imperfect mimicry, in which the pairing between specific cues and reinforcers allows an imperfect mimic to resemble multiple models simultaneously. Generally, our results emphasize the importance of receiver psychology for the evolution of signal complexity and specificity.

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.

Batesian mimicry promotes pre- and postmating isolation in a snake mimicry complex.

We evaluated whether Batesian mimicry promotes early-stage reproductive isolation. Many Batesian mimics occur not only in sympatry with their model (as expected), but also in allopatry. As a consequence of local adaptation within both sympatry (where mimetic traits are favored) and allopatry (where nonmimetic traits are favored), divergent, predator-mediated natural selection should disfavor immigrants between these selective environments as well as any between-environment hybrids. This selection might form the basis for both pre- and postmating isolation, respectively. We tested for such selection in a snake mimicry complex by placing clay replicas of sympatric, allopatric, or hybrid phenotypes in both sympatry and allopatry and measuring predation attempts. As predicted, replicas with immigrant phenotypes were disfavored in both selective environments. Replicas with hybrid phenotypes were also disfavored, but only in a region of sympatry where previous studies have detected strong selection favoring precise mimicry. By fostering immigrant inviability and ecologically dependent selection against hybrids (at least in some habitats), Batesian mimicry might therefore promote reproductive isolation. Thus, although Batesian mimicry has long been viewed as a mechanism for convergent evolution, it might play an underappreciated role in fueling divergent evolution and possibly even the evolution of reproductive isolation and speciation.

Mimicry's palette: widespread use of conserved pigments in the aposematic signals of snakes.

Mimicry, where one species resembles another species because of the selective benefits of sharing a common signal, is especially common in snakes. Snakes might be particularly prone to evolving mimicry if all species share some of the same proximate mechanisms that can be used to produce aposematic/mimetic signals. We evaluated this possibility by examining color pigments in 11 species of snakes from four different families, three species of which participate in a coral snake mimicry complex involving convergence in coloration. We found that all 11 species used combinations of two pteridine pigments and melanin in their coloration, regardless of whether or not they were mimics. Furthermore, the presence or absence of red pteridines was strongly correlated with the relative excitation of medium- and long-wavelength photoreceptors in birds, thereby linking shared pigmentation to perception of those pigments by likely agents of selection. Thus, precise color mimicry might be relatively easy to evolve among snakes owing to symplesiomorphies in pigmentation.

Imperfect mimicry and the limits of natural selection.

Mimicry--when one organism (the mimic) evolves a phenotypic resemblance to another (the model) due to selective benefits--is widely used to illustrate natural selection's power to generate adaptations. However, many putative mimics resemble their models imprecisely, and such imperfect mimicry represents a specific challenge to mimicry theory and a general one to evolutionary theory. Here, we discuss 11 nonmutually exclusive hypotheses for imperfect mimicry. We group these hypotheses according to whether imperfect mimicry reflects: an artifact of human perception, which is not shared by any naturally occurring predators and therefore is not truly an instance of imperfect mimicry; genetic, developmental or time-lag constraints, which (temporarily) prevent a response to selection for perfect mimicry; relaxed selection, where imperfect mimicry is as adaptive as perfect mimicry; or tradeoffs, where imperfect mimicry is (locally) more adaptive than perfect mimicry. We find that the relaxed selection hypothesis has garnered the most support. However, because only a few study systems have thus far been comprehensively evaluated, the relative contributions of the various hypotheses toward explaining the evolution of imperfect mimicry remain unclear. Ultimately, clarifying why imperfect mimicry exists should provide critical insights into the limits of natural selection in producing complex adaptations.

Predator cognition permits imperfect coral snake mimicry.

Batesian mimicry is often imprecise. An underexplored explanation for imperfect mimicry is that predators might not be able to use all dimensions of prey phenotype to distinguish mimics from models and thus permit imperfect mimicry to persist. We conducted a field experiment to test whether or not predators can distinguish deadly coral snakes (Micrurus fulvius) from nonvenomous scarlet kingsnakes (Lampropeltis elapsoides). Although the two species closely resemble one another, the order of colored rings that encircle their bodies differs. Despite this imprecise mimicry, we found that L. elapsoides that match coral snakes in other respects are not under selection to match the ring order of their model. We suggest that L. elapsoides have evolved only those signals necessary to deceive predators. Generally, imperfect mimicry might suffice if it exploits limitations in predator cognitive abilities.

High-model abundance may permit the gradual evolution of Batesian mimicry: an experimental test.

In Batesian mimicry, a harmless species (the 'mimic') resembles a dangerous species (the 'model') and is thus protected from predators. It is often assumed that the mimetic phenotype evolves from a cryptic phenotype, but it is unclear how a population can transition through intermediate phenotypes; such intermediates may receive neither the benefits of crypsis nor mimicry. Here, we ask if selection against intermediates weakens with increasing model abundance. We also ask if mimicry has evolved from cryptic phenotypes in a mimetic clade. We first present an ancestral character-state reconstruction showing that mimicry of a coral snake (Micrurus fulvius) by the scarlet kingsnake (Lampropeltis elapsoides) evolved from a cryptic phenotype. We then evaluate predation rates on intermediate phenotypes relative to cryptic and mimetic phenotypes under conditions of both high- and low-model abundances. Our results indicate that where coral snakes are rare, intermediate phenotypes are attacked more often than cryptic and mimetic phenotypes, indicating the presence of an adaptive valley. However, where coral snakes are abundant, intermediate phenotypes are not attacked more frequently, resulting in an adaptive landscape without a valley. Thus, high-model abundance may facilitate the evolution of Batesian mimicry.