The evolutionary stability of automimicry

Internal defences such as toxins cannot be detected from a distance by a predator, and are likely to be costly to produce and maintain. Populations of well-defended prey may therefore be vulnerable to invasion from rare 'cheater' mutants that do not produce the toxin themselves but obtain some protection from their resemblance to their better defended conspecifics (automimicry). Although it is well established that well-defended and weakly defended morphs may coexist stably in protected dimorphisms, recent theoretical work suggests that such dimorphisms would not be resistant to invasion by novel mutants with defence levels intermediate to those present. Given that most defences (including toxins) are likely to be continuous traits, this implies that automimicry may tend to be a transitory phenomenon, and thus less likely to explain variation in defence levels in nature. In contrast to this, we show that automimicry can also be evolutionarily stable for continuous traits, and that it may evolve under a wide range of conditions. A recently developed geometric method allows us to determine directly from a trade-off curve whether an evolutionarily stable defence dimorphism is at all possible, and to make some qualitative inferences about the ecological conditions that may favour it.     

A field demonstration of the costs and benefits of group living to edible and defended prey

Both theoretical and laboratory research suggests that many prey animals should live in a solitary, dispersed distribution unless they lack repellent defences such as toxins, venoms and stings. Chemically defended prey may, by contrast, benefit substantially from aggregation because spatial localization may cause rapid predator satiation on prey toxins, protecting many individuals from attack. If repellent defences promote aggregation of prey, they also provide opportunities for new social interactions; hence the consequences of defence may be far reaching for the behavioural biology of the animal species. There is an absence of field data to support predictions about the relative costs and benefits of aggregation. We show here for the first time using wild predators that edible, undefended artificial prey do indeed suffer heightened death rates if they are aggregated; whereas chemically defended prey may benefit substantially by grouping. We argue that since many chemical defences are costly to prey, aggregation may be favoured because it makes expensive defences much more effective, and perhaps allows grouped individuals to invest less in chemical defences.     

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.     

How can automimicry persist when predators can preferentially consume undefended mimics?

It is common for species that possess toxins or other defences to advertise these defences to potential predators using aposematic ("warning") signals. There is increasing evidence that within such species, there are individuals that have reduced or non-existent levels of defence but still signal. This phenomenon (generally called automimicry) has been a challenge to evolutionary biologists because of the need to explain why undefended automimics do not gain such as a fitness advantage by saving the physiological costs of defence that they increase in prevalence within the population, hence making the aposematic signal unreliable. The leading theory is that aposematic signals do not stop all predatory attacks but rather encourage predators to attack cautiously until they have identified the defence level of a specific individual. They can then reject defended individuals and consume the undefended. This theory has recently received strong empirical support, demonstrating that high-accuracy discrimination appears possible. However, this raises a new evolutionary problem: if predators can perfectly discriminate the defended from the undefended and preferentially consume the latter, then how can automimicry persist? Here, we present four different mechanisms that can allow non-trivial levels of automimics to be retained within a population, even in the extreme case where predators can differentiate defended from undefended individuals with 100% accuracy. These involve opportunity costs to the predator of sampling carefully, temporal fluctuation in predation pressure, predation pressure being correlated with the prevalence of automimicry, or developmental or evolutionary constraints on the availability of defence. These mechanisms generate predictions as to the conditions where we would expect aposematically signalling populations to feature automimicry and those where we would not.     

Frequency-dependent taste-rejection by avian predation may select for defence chemical polymorphisms in aposematic prey

Chemically defended insects advertise their unpalatability to avian predators using conspicuous aposematic coloration that predators learn to avoid. Insects utilize a wide variety of different compounds in their defences, and intraspecific variation in defence chemistry is common. We propose that polymorphisms in insect defence chemicals may be beneficial to insects by increasing survival from avian predators. Birds learn to avoid a colour signal faster when individual prey possesses one of two unpalatable chemicals rather than all prey having the same defence chemical. However, for chemical polymorphisms to evolve within a species, there must be benefits that allow rare chemical morphs to increase in frequency. Using domestic chicks as predators and coloured crumbs for prey, we provide evidence that birds taste and reject proportionally more of the individuals with rare defence chemicals than those with common defence chemicals. This indicates that the way in which birds attack and reject prey could enhance the survival of rare chemical morphs and select for chemical polymorphism in aposematic species. This is the first experiment to demonstrate that predators can directly influence the form taken by prey's chemical defences.     

Why are defensive toxins so variable? An evolutionary perspective

Defensive toxins are widely used by animals, plants and micro-organisms to deter natural enemies. An important characteristic of such defences is diversity both in the quantity of toxins and the profile of specific defensive chemicals present. Here we evaluate evolutionary and ecological explanations for the persistence of toxin diversity within prey populations, drawing together a range of explanations from the literature, and adding new hypotheses. We consider toxin diversity in three ways: (1) the absence of toxicity in a proportion of individuals in an otherwise toxic prey population (automimicry); (2) broad variation in quantities of toxin within individuals in the same population; (3) variation in the chemical constituents of chemical defence. For each of these phenomena we identify alternative evolutionary explanations for the persistence of variation. One important general explanation is diversifying (frequency- or density-dependent) selection in which either costs of toxicity increase or their benefits decrease with increases in the absolute or relative abundance of toxicity in a prey population. A second major class of explanation is that variation in toxicity profiles is itself nonadaptive. One application of this explanation requires that predator behaviour is not affected by variation in levels or profiles of chemical defence within a prey population, and that there are no cost differences between different quantities or forms of toxins found within a population. Finally, the ecology and life history of the animal may enable some general predictions about toxin variation. For example, in animals which only gain their toxins in their immature forms (e.g. caterpillars on host plants) we may expect a decline in toxicity during adult life (or at least no change). By contrast, when toxins are also acquired during the adult form, we may for example expect the converse, in which young adults have less time to acquire toxicity than older adults. One major conclusion that we draw is that there are good reasons to consider within-species variation in defensive toxins as more than mere ecological noise. Rather there are a number of compelling evolutionary hypotheses which can explain and predict variation in prey toxicity.     

Disengtangling the evolution of weak warning signals: high detection risk and low production costs of chemical defences in gregarious pine sawfly larvae

Evolution of costly secondary defences for a cryptic prey is puzzling, if the prey is already well protected by camouflage. However, if the chemical defence is not sufficient to deter all predators, selection can favour low signal intensity in defended prey. Alternatively, if the costs of chemical defence are low or cost-free, chemical defences can be expected to evolve also for non-signalling prey, particularly if conspicuous signalling is costly. We tested these assumptions with pine sawfly larvae (Neodiprion sertifer and Diprion pini) that are cryptically coloured and chemically defended with resin acids sequestered from their host plant (Pinus sp.). Larvae feed in large aggregations, which we hypothesise could function as a signal of unprofitability. Our results show that even though the birds found N. sertifer larvae unprofitable in the controlled laboratory assays, they continued attacking and consuming them in the wild. When we tested the signal value of aggregation we found that a large group size did not offer protection for a defended larva: the survival was higher in groups of 10 individuals compared to groups of 50, suggesting increased detectability costs for individuals in larger groups. Finally, we tested how costly the production and maintenance of a chemical defence is for D. pini larvae by manipulating the resin acid content of the diet. We did not find any life history or immunological costs of the chemical defence for the larvae. In contrast, pupal weights were higher on the high resin diet than on the low resin diet. Also, larvae were able to produce higher amounts of defence fluids on the high diet than on the low diet. Thus, our result suggests high detectability costs and low production costs of defences could explain why some unprofitable species have not evolved conspicuous signals.     

Temporal shift of diet in alternative cannibalistic morphs of the tiger salamander

Evolutionary theory predicts that alternative trophic morphologies are adaptive because they allow a broad use of resources in heterogeneous environments. The development of a cannibal morphology is expected to result in cannibalism and high individual fitness, but conflicting results show that the situation is more complex. The goal of the present study was to increase our understanding of the ultimate benefits of a cannibalistic polyphenism by determining temporal changes in the feeding habits and biomass intake in a population of tiger salamanders ( Ambystoma tigrinum nebulosum ). Cannibals in this species develop a larger head than typicals and have prominent teeth, both useful for consuming large prey. Although cannibalism was only detected in cannibal morphs, large temporal variation in resource partitioning was found between morphs. The two morphs always differed in their foraging habits, but cannibalism mainly occurred immediately after the ontogenetic divergence between morphs. Cannibals shifted their foraging later to a more planktivorous diet (i.e. the primarily prey of the typical morph). Cannibals also obtained more prey biomass than typicals. These results indicate that the cannibalistic morph is advantageous over the typical development, but that these advantages vary ontogenetically. Although the results obtained are consistent with models predicting the maintenance of cannibalism polyphenism in natural populations, they show that the foraging tactics utilized by cannibal morphs, and the fitness consequences accrued by such tactics, are likely to be more complex and dynamic than previous studies have suggested.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 373–382.     

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.     

Density-dependent effects of prey defences

In this study, we show that the protective advantage of a defence depends on prey density. For our investigations, we used the predator-prey model system Chaoborus-Daphnia pulex. The prey, D. pulex, forms neckteeth as an inducible defence against chaoborid predators. This morphological response effectively reduces predator attack efficiency, i.e. number of successful attacks divided by total number of attacks. We found that neckteeth-defended prey suffered a distinctly lower predation rate (prey uptake per unit time) at low prey densities. The advantage of this defence decreased with increasing prey density. We expect this pattern to be general when a defence reduces predator success rate, i.e. when a defence reduces encounter rate, probability of detection, probability of attack, or efficiency of attack. In addition, we experimentally simulated the effects of defences which increase predator digestion time by using different sizes of Daphnia with equal vulnerabilities. This type of defence had opposite density-dependent effects: here, the relative advantage of defended prey increased with prey density. We expect this pattern to be general for defences which increase predator handling time, i.e. defences which increase attacking time, eating time, or digestion time. Many defences will have effects on both predator success rate and handling time. For these defences, the predator’s functional response should be decreased over the whole range of prey densities. Received: 15 September 1999 / Accepted: 23 December 1999     

Defence Cheats Can Degrade Protection of Chemically Defended Prey

Many species defend themselves against enemies using repellent chemicals. An important but unanswered question is why investment in chemical defence is often variable within prey populations. One explanation is that some prey benefit by cheating, paying no costs of defence, but gaining a reduced attack rate because of the presence of defended conspecifics. Two important assumptions about predator behaviour must be met to explain cheating as a stable strategy: first, predators increase attack rates as cheats increase in frequency; second, defended prey survive attacks better than non‐defended conspecifics. We lack data from wild predators that evaluate these hypotheses. Here, we examine how changes in the frequency of non‐defended ‘cheats’ affect predation by wild birds on a group of otherwise defended prey. We presented mealworm larvae that were either edible (‘cheats’) or unpalatable (bitter tasting), and varied the proportion of cheats from 0 to 1 by increments of 0.25. We found strong frequency‐dependent effects on the birds' foraging behaviour, with the proportion of prey attacked increasing nonlinearly with the frequency of cheats. We did not, however, observe that birds taste‐rejected defended prey at the site of capture. One explanation is that wild birds may not assess prey palatability at the site of capture, but do this elsewhere. If so, defended and undefended prey may pay high costs of initial attack and relocation away from ecologically favourable locations. Alternatively, defended prey may not be taste‐rejected because with acute time constraints, wild birds do not have time to make fine‐grained decisions during feeding. We discuss the data in relation to the evolutionary ecology of prey defences.     

Inducible defences are a stabilizing factor for predator and prey populations: a field experiment

1. Based on mathematical models, antipredator defence mechanisms are commonly believed to have stabilizing effects on communities. However, empirical data are still lacking. 2. We tested stabilizing effects of an inducible vertical migration defence in two Daphnia pulex clones in a 5‐week field enclosure experiment. A defended (migrated down into darker water layers in the presence of fish chemicals in both laboratory and field experiments) and non‐defended (no ability to react to fish chemicals) clone were directly exposed to fish predators and compared to control enclosures (no fish). 3. In the absence of planktivorous fish, both defended and non‐defended clones exhibited boom‐and‐bust dynamics, probably owing to over‐exploitation of the food source. Predation almost led to extinction of the non‐defended Daphnia clone during the experiment and the fish, deprived of food, lost weight. However, the population density of the defended clone was stable and it did not over‐exploit the algal food source, while there was a continuous supply of food to the fish, which consequently gained weight. 4. We conclude that both consumptive and non‐consumptive (also called non‐lethal or trait‐mediated) predator effects, coupled with prey defences, are key contributors to prey stability. This has a positive effect on both the predator and the food organism of the prey.     

Parameterising a public good: how experiments on predation can be used to predict cheat frequencies

Chemical defence is superficially easy to understand as a means for individuals to protect themselves from enemies. The evolution of chemical defence is however potentially complex because such defences may cause the generation of a public good, protecting members of the population as a whole as well as individuals that deploy toxins defensively. If a public good of protection exists, it may be exploited and degraded by “cheats” that do not invest in defence. This can in turn lead to complex frequency (and density) dependent effects in toxin evolution. To investigate this we used ecologically relevant predators (Great tits, Parus major) and examined how individual and public benefits vary depending on the frequency of non-defended “cheating” prey and their spatial distribution. We found that the public benefit, of reduced attack probability, increased with increasing frequency of defended individuals. In contrast the individual benefit of chemical defence, measured as increased chance of rejection during an attack before injury, did not vary with the frequency of defended forms. Hence the selective dynamics of these two levels of benefits responded differently to the frequency of defended forms. Surprisingly, given the strong associations of chemical defences and grouping in animals, large aggregations did not help individuals in the group regardless of their defence status. The explanation for the result, may be that in our experiment birds did not have information about other potential aggregations (i.e. set up was sequential) and thus their giving up density was lower compared to the situations where set ups were simultaneous. We use behavioural data of our predators to construct a simple model of toxin evolution which can make quantitative predictions about the frequencies to which defence cheats evolve. We use this model to discuss how toxin evolution can be investigated in the wild and in laboratory settings.     

Better the devil you know: avian predators find variation in prey toxicity aversive

Toxic prey that signal their defences to predators using conspicuous warning signals are called ‘aposematic’. Predators learn about the toxic content of aposematic prey and reduce their attacks on them. However, through regulating their toxin intake, predators will include aposematic prey in their diets when the benefits of gaining the nutrients they contain outweigh the costs of ingesting the prey''s toxins. Predators face a problem when managing their toxin intake: prey sharing the same warning signal often vary in their toxicities. Given that predators should avoid uncertainty when managing their toxin intake, we tested whether European starlings (Sturnus vulgaris) preferred to eat fixed-defence prey (where all prey contained a 2% quinine solution) to mixed-defence prey (where half the prey contained a 4% quinine solution and the other half contained only water). Our results support the idea that predators should be more ‘risk-averse’ when foraging on variably defended prey and suggest that variation in toxicity levels could be a form of defence.     

Linking herbivore-induced defences to population dynamics

1. Theoretical studies have shown that inducible defences have the potential to affect population stability and persistence in bi‐ and tritrophic food chains. Experimental studies on such effects of prey defence strategies on the dynamics of predator–prey systems are still rare. We performed replicated population dynamics experiments using the herbivorous rotifer Brachionus calyciflorus and four strains of closely related algae that show different defence responses to this herbivore. 2. We observed herbivore populations to fluctuate at a higher frequency when feeding on small undefended algae. During these fluctuations minimum rotifer densities remained sufficiently high to ensure population persistence in all the replicates. The initial growth of rotifer populations in this treatment coincided with a sharp drop in algal density. Such a suppression of algae by herbivores was not observed in the other treatments, where algae were larger due to induced or permanent defences. In these treatments we observed rotifer population densities to first rise and then decline. The herbivore went extinct in all replicates with large permanently defended algae. The frequency of herbivore extinctions was intermediate when algae had inducible defences. 3. A variety of alternative mechanisms could explain differential herbivore persistence in the different defence treatments. Our analysis showed the density and fraction of highly edible algal particles to better explain herbivore persistence and extinctions than total algal density, the fraction of highly inedible food particles or the accumulation of herbivore waste products or autotoxins. 4. We argue that the rotifers require a minimum fraction and density of edible food particles for maintenance and reproduction. We conjecture that induced defences in algae may thus favour larger zooplankton species such as Daphnia spp. that are less sensitive to shifts in their food size spectrum, relative to smaller zooplankton species, such as rotifers and in this way contributes to the structuring of planktonic communities.     

Morphological correlates of ant eating in horned lizards (Phrynosoma)

The North American horned lizards ( Phrynosoma ) represent a morphologically specialized group of ant-eating lizards. Although variation in dietary fidelity is observed among the species, all appear to possess morphological specializations thought to be related to their ant-eating diets. Previous studies have examined morphological specialization in Phrynosoma , but they have not taken into account the phylogenetic relationships of its member species. In the present study, the morphological characteristics of the head, jaws and teeth that are thought to be important in prey capture and prey processing were examined to test whether variation in cranial morphology is associated with diet in lizards of the genus Phrynosoma . It is suggested that lizards of the genus Phrynosoma are indeed morphologically specialized and that ant-eating is associated with reduced dentition and an overall reduction in the robustness of morphological structures important in prey processing. Although this trend holds for the highly myrmecophagous species of Phrynosoma , a robust cranial morphology is apparent in the short-horned lizard clade ( Phrynosoma ditmarsi , Phrynosoma douglasii , Phrynosoma hernandesi , Phrynosoma orbiculare ), implying the ability to process a variety of dietary items. The present study suggests that additional feeding specializations exist within an already specialized clade (i.e. the short-horned lizard clade) and highlights the need for more detailed dietary and behavioural studies of feeding behaviour in this uniquely specialized group of lizards.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 13–24.     

Correlated evolution of aquatic prey-capture strategies in European and American natricine snakes

The evolution of aquatic prey-capture strategies in snakes has been suggested as a model system for the study of convergence. However, hypotheses of correlated evolution of prey-capture strategy with different aspects of foraging niche have never been tested quantitatively. Whereas a considerable amount of data is available for North American species, data for European species are scarce. In this study we combine original data on prey-capture strategies and strike velocities for European natricines with data for North American Natricinae obtained from the literature. We did not find any evidence for correlated evolution between prey-capture strategy and strike velocity with diet, but there was a significant correlation with prey density. Thus, our study suggests that prey density, rather than diet, played an important role in the evolution of the different prey-capture strategies and strike velocities of natricine snakes.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 73–83.     

Avian predators taste-reject aposematic prey on the basis of their chemical defence

Avian predators learn to avoid defended insects on the basis of their conspicuous warning coloration. In many aposematic species, the level of chemical defence varies, with some individuals being more defended than others. Sequestration and production of defence chemicals is often costly and therefore less defended individuals enjoy the benefits of the warning signal without paying the full costs of chemical production. This is a fundamental theoretical problem for the evolutionary stability of aposematism, since less defended individuals appear to be at a selective advantage. However, if predators sample aposematic prey and selectively reject individuals on the basis of their chemical investment, aposematism could become evolutionarily stable. Previous research aimed at testing whether birds can use taste to discriminate between palatable and unpalatable prey has been confounded by other experimental factors. Here, we show that birds can taste and reject prey entirely on the basis of an individual's level of chemical defence and more importantly, they can make decisions on whether or not to consume a defended individual based upon their level of chemical investment. We discuss these results in relation to the evolution of aposematism, mimicry and defence chemistry.     

Testing Müllerian mimicry: an experiment with wild birds

Experiments with wild birds feeding on pastry 'prey' were performed to test competing theories of Müllerian mimicry Conventional theories predict that all resemblances between defended prey will be mutually advantageous and, hence, Müllerian. In contrast, unconventional theories predict that, if there are inequalities in defences between mimetic species, the less well-defended prey may dilute the protection of the better defended species in a quasi-Batesian manner. This unconventional prediction follows from an assumption that birds learn about the edibilities of prey using rules of Pavlovian learning. We report on two experiments, each lasting 40 days, which showed that a moderately defended prey can dilute the protection of a better defended mimic in a quasi-Batesian fashion, but can add protection to a mimic which has the same moderate levels of defence. These results match predictions of unconventional theories of mimicry and go some way to resolving the long-running arguments over the nature of Müllerian mimicry.     

Phylogenetic analysis of Zygaenoidea small-subunit rRNA structural variation implies initial oligophagy on cyanogenic host plants in larvae of the moth genus Zygaena (Insecta: Lepidoptera)

Cyanogenesis, the release of toxic cyanide from living cells, plays an important role in the defence system of certain plant (e.g. Fabaceae) and animal (e.g. Zygaenidae) taxa. The larvae of a significant number of Zygaena moth species (Zygaenidae) preferentially feed on cyanogenic Fabaceae and some of them are able to sequester cyanogenic compounds of their host plants. Using secondary structure variation of the small-subunit rRNA, we tested the currently accepted evolutionary hypothesis explaining species diversification in the genus Zygaena . We derived secondary structures considering evidence from covariation patterns and thermodynamic folding and applied structural information in a phylogenetic analysis. Contrary to previous assumptions, our results suggest that the use of cyanogenic larval host plants is an ancient trait and that the ability to feed on cyanogenic plants was probably already present in the most recent common ancestor of Zygaena . The utilization of acyanogenic plants in Zygaena species appears to be the result of a single secondary, reverse, larval host-plant shift. © 2006 The Linnean Society of London, Zoological Journal of the Linnean Society , 2006, 147 , 367–381.