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Current Biology
Magazine
R350 Current Biology 25, R345–R361, May 4, 2015 ©2015 Elsevier Ltd All rights reserved
Aposematism
Bibiana Rojas
1,
*, Janne Valkonen
1
,
and Ossi Nokelainen
2
What is aposematism? The word
comes from the Greek apo (away) and
sema (sign) and describes a strategy
whereby animals warn predators about
their unprofitability. It consists of two
elements: a primary defence, such as
distinctive colours, odours or sounds,
that operates before the predator attacks;
and a secondary defence, be it chemical,
morphological or behavioural that make
prey unprofitable for predators. For
example, the bright colours of many
animals, such as poison frogs and wood
tiger moths, warn predators about their
toxic or distasteful chemical defences.
When predators encounter and attack
them in the wild, the prey will provoke
a bad experience that the predator
will learn to associate with the prey’s
colouration. As a result, predators will
start to avoid defended prey. After several
Quick guide
being conspicuous might be lower in
environments where alternative prey is
abundant, given that most predators
prefer familiar over unfamiliar food
objects. Aposematism has presumably
evolved several independent times, as
suggested by its occurrence in many
groups of animals.
What are the theoretical assumptions
about aposematism, and why is
variation in warning signals puzzling?
In order to work for the aposematic
animal, signals have to be clear and easy
to learn and remember for predators.
Warning signals thus should evolve
to be conspicuous and distinct. The
more individuals bearing the warning
signal, the more effective, easier to
learn and memorable the signal will be
for predators. Essentially, successful
aposematism relies on strength
in numbers. In fact, aposematism
could have been initially favoured in
aggregations of defended prey. Predators
presumably also learn more easily to
avoid one signal rather than several, and
that their learning depends on the rate
of unpleasant encounters with defended
generations of coevolution, aposematic
animals are often conspicuous and
distinctive (Figure 1), but not all
conspicuous animals are aposematic.
Likewise, not all aposematic species are
overtly conspicuous (Figure 1) and, thus,
aposematism should be considered as
a continuum of conspicuousness and
secondary defence rather than as an
unconditional anti-predator strategy.
How does aposematism evolve?
Although it has been studied since the
times of Wallace and Darwin, the origin
and evolution of aposematism is not
yet fully understood. Despite being
clear evidence of natural selection,
aposematism is somehow a paradoxical
adaptation. It is unclear how the first
conspicuous individuals were able
to survive and reproduce such that
predators would encounter them often
enough to be able to learn about their
unprofitability. Conspicuousness, as
well as chemical defence, may have
increased gradually. Alternatively,
both defences could have been
selected for other reasons (e.g. sexual
selection). Moreover the initial cost of
Figure 1. Aposematic animals.
Top left: dyeing poison frog (Dendrobates tinctorius); top center: female of the wood tiger moth (Parasemia plantaginis); top right: coral snake
(Micrurus surinamensis); Bottom left: Brazil’s lancehead (Bothrops brazili) is not overtly conspicuous to us, but both the patterns and head shape
of some vipers can function as warning signals to predators; bottom center: firebug (Pyrrhocoris apterus); bottom right: common wasp (Vespula
vulgaris). (Photos: Bibiana Rojas; wasp: Tom Houslay).
Current Biology
Magazine
Current Biology 25, R345–R361, May 4, 2015 ©2015 Elsevier Ltd All rights reserved R351
prey. Thus, selection is expected to
favour uniform warning signals and
suppress variation. Nevertheless,
warning signal variation is evident across
the natural world. The mechanisms
maintaining this puzzling variation are
still poorly understood, but it is thought
that this may arise for various reasons.
Some warning signals may serve
other purposes, such as intra-specific
signalling, or be a response to different
selective pressures which would trade-off
with the pressure exerted by predators.
For example, in the colour polymorphic
wood tiger moth (Parasemia plantaginis),
yellow males are generally better
defended from predators. In contrast,
under some circumstances, white males
are more successful at mating and have
higher flying activity, which might help
them find emerging females quicker or
compensate behaviourally for a less
efficient anti-predator colouration. In
cold environments, increased black wing
pattern elements bring thermoregulatory
benefits to these moths, but at the cost
of reduced warning coloration (white
or yellow). Recently, local predator
communities have also been shown
to aid in the maintenance of warning
signal variation. Hence, it is likely
that different properties of warning
colouration become costly or beneficial in
changing environments. Finally, it cannot
be discarded that the variation is not
adaptive, but the product of hybridisation
or drift.
Are warning signals honest?
According to the ‘handicap principle’,
signals that provide reliable information
about an individual’s quality should
be selected for. Such signals must
be costly for the signaller and, thus,
unaffordable for low-quality individuals.
Warning signals can be honest, if they are
reliable indicators of prey unprofitability.
Therefore, secondary defences may
vary as well, and this variation may by
no means be less relevant. For example,
in the strawberry poison frog (Oophaga
pumilio) great variation in toxicity among
populations is positively correlated
with conspicuousness. Likewise, in
the seven-spot ladybird (Coccinella
septempunctata), the amount of coloured
pigments correlates positively with the
level of chemical defences. At least for
the ladybirds, this correlation seems
to depend on resource availability.
This means that there can be costs
associated with the production of primary
or secondary defences, or both, that may
affect the effectiveness of aposematism.
Are there cheaters? Yes. When
predators learn to avoid a warning
signal that is shared among aposematic
individuals, organisms of other species
may mimic that signal and get protection
benefits without investing in secondary
defences or predator education. In
Batesian mimicry, a palatable organism
is protected by its resemblance to an
unpalatable one. Thus, Batesian mimics
should not be considered aposematic,
because they lack a secondary defence.
The increase of Batesian mimics in a
population decreases the efficacy of the
signal, because predators start to ignore
it as it becomes less reliable. Maybe the
most well known Batesian mimics are
hoverflies, which resemble wasps and
bees. In Müllerian mimicry, on the other
hand, two or more aposematic animals
have evolved a similar appearance
that is avoided by predators. Textbook
examples include the famous Heliconius
butterflies and dart poison frogs in the
Ranitomeya imitator complex. In fact,
mimicry is one of the first and strongest
pieces of evidence for Darwinian natural
selection.
Where can I find out more?
Alatalo, R.V., and Mappes, J. (1996). Tracking
the evolution of warning signals. Nature 382,
708–710.
Cott, H.B. (1940). Adaptive Colouration in Animals.
(Methuen, London).
Endler, J.A. (1991). Interactions between
predators and prey. In Behavioural Ecology.
An Evolutionary Approach, J.R. Krebs and
N.B. Davies, eds. (Cambridge University Press:
Cambridge).
Guilford, T., and Dawkins, M.S. (1993). Are warning
colors handicaps? Evolution 47, 400–416.
Härlin, C., and Härlin, M. (2003). Towards a
historization of aposematism. Evol. Ecol. 17,
197–212.
Mappes, J., Marples, N., and Endler, J.A. (2005). The
complex business of survival by aposematism.
Trends Ecol. Evol. 20, 598–603.
Poulton, E.B. (1890). The Colours of Animals: Their
Meaning and Use. (Kegan Paul, Trench, Trubner:
London), pp. 558–612.
Ruxton, G.D., Sherratt, T.N., and Speed, M.P. (2004).
Avoiding Attack: The Evolutionary Ecology of
Crypsis, Warning Signals and Mimicry. (Oxford
University Press: Oxford).
Stevens, M., and Ruxton, G.D. (2012). Linking the
evolution and form of warning coloration in
nature. Proc. Roy. Soc. Biol. Sci. 279, 417–426.
1
Centre of Excellence in Biological
Interactions, Department of Biology and
Environmental Science, University of
Jyväskylä, Finland.
2
Department of Zoology,
University of Cambridge, UK.
*E-mail: bibiana.rojas@jyu.fi
Deaf white cats
Andrej Kral
1
and Stephen G. Lomber
2
What are deaf white cats? The term
‘deaf white cat’ is used to describe
domestic cats with completely white
fur (short-hair or long-hair) that
have no functional hearing; they
typically have blue eyes (Figure 1A).
It is estimated that in the overall
cat population, 5% are white, and
a subpopulation of these are blue
eyed. As early as 1868, Charles
Darwin noted in his book The
Variation of Animals and Plants under
Domestication that “white cats, if they
have blue eyes, are almost always
deaf”. This observation has been
substantiated in many subsequent
studies. Deafness identified in white
cats can be bilateral (both ears), or,
less frequently, unilateral (one ear)
with residual hearing in the opposite
ear.
What makes deaf white cats so
interesting? Any mammal can fail to
develop functional hearing. In many
species, such as domestic cats and
dogs, there is a higher incidence of
deafness in animals with a white coat.
The association between white coat
and deafness is greatest in white cats
with blue eyes. Animals bred for this
trait are a natural model for human
congenital deafness. Consequently,
deaf white cats are ideal for
studying the effects of hearing loss
on development and function of
the auditory system. Furthermore,
studies examining this animal model
have demonstrated the beneficial
effects of hearing restoration with
cochlear prosthetics (implants).
These experiments were essential for
evidence-based recommendations on
the treatment of congenital deafness
in children. Today, approximately
400,000 hearing impaired individuals
world-wide benefit from cochlear
implants in their daily life. Given the
present rate of implantation, the
number of people using cochlear
implants is projected to reach one
million in 2020. Overall, the cochlear
implant is the most successful
neuroprosthetic device.
Quick guide
... Prey appearance is rarely fixed, and can vary in complex and dynamic ways (Endler & Mappes, 2004;Mappes et al., 2005;Rojas et al., 2015). For example, functional changes in the appearance of prey body colour and shape to predators can be affected by predator behaviour, such as the distance from which predators view their prey. ...
Article
Deimatic behaviour is performed by prey when attacked by predators as part of an antipredator strategy. The behaviour is part of a sequence that consists of several defences, for example they can be preceded by camouflage and followed by a hidden putatively aposematic signal that is only revealed when the deimatic behaviour is performed. When displaying their hidden signal, mountain katydids (Acripeza reticulata) hold their wings vertically, exposing striking red and black stripes with blue spots and oozing an alkaloid-rich chemical defence derived from its Senecio diet. Understanding differences and interactions between deimatism and aposematism has proven problematic, so in this study we isolated the putative aposematic signal of the mountain katydid's antipredator strategy to measure its survival value in the absence of their deimatic behaviour. We manipulated two aspects of the mountain katydid's signal, colour pattern and whole body shape during display. We deployed five kinds of clay models, one negative control and four katydid-like treatments, in 15 grids across part of the mountain katydid's distribution to test the hypothesis that their hidden signal is aposematic. If this hypothesis holds true, we expected that the models, which most closely resembled real katydids would be attacked the least. Instead, we found that models that most closely resembled real katydids were the most likely to be attacked. We suggest several ideas to explain these results, including that the deimatic phase of the katydid's display, the change from a camouflaged state to exposing its hidden signal, may have important protective value.
... The evolution of aposematism, i.e the co-occurrence of conspicuous coloration and defensive mechanisms, is fascinating and poorly understood, despite intensive research over many decades (e.g., [1][2][3][4][5]). Whether an apparently bright and conspicuous colour pattern is aposematic (i.e., it has primarily a warning function) rather than serving intraspecific communication or even camouflage [1,6,7] and how warning colour integrates with the evolution of other phenotypic characters [8] are intriguing questions that can only be answered by subjecting a variety of animal systems to experimental (e.g., [9][10][11], phylogenetic (e.g., [12]), and genomic research (e.g., [13]). ...
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The genus Brachycephalus is a fascinating group of miniaturized anurans from the Brazilian Atlantic Forest, comprising the conspicuous, brightly colored pumpkin-toadlets and the cryptic flea-toads. Pumpkin-toadlets are known to contain tetrodotoxins and therefore, their bright colors may perform an aposematic function. Previous studies based on a limited number of mitochondrial and nuclear-encoded markers supported the existence of two clades containing species of pumpkin-toadlet phenotype, but deep nodes remained largely unresolved or conflicting between data sets. We use new RNAseq data of 17 individuals from nine Brachycephalus species to infer their evolutionary relationships from a phylogenomic perspective. Analyses of almost 5300 nuclear-encoded ortholog protein-coding genes and full mitochondrial genomes confirmed the existence of two separate pumpkin-toadlet clades, suggesting the convergent evolution (or multiple reversals) of the bufoniform morphology, conspicuous coloration, and probably toxicity. In addition, the study of the mitochondrial gene order revealed that three species (B. hermogenesi, B. pitanga, and B. rotenbergae) display translocations of different tRNAs (NCY and CYA) from the WANCY tRNA cluster to a position between the genes ATP6 and COIII, showing a new mitochondrial gene order arrangement for vertebrates. The newly clarified phylogeny suggests that Brachycephalus has the potential to become a promising model taxon to understand the evolution of coloration, body plan and toxicity. Given that toxicity information is available for only few species of Brachycephalus, without data for any flea-toad species, we also emphasize the need for a wider screening of toxicity across species, together with more in-depth functional and ecological study of their phenotypes.
... Predation has driven the evolution of striking adaptations for defence among prey [1][2][3]. Few strategies are as widespread as aposematism which, in its best-studied form, is characterized by the coupling of chemical defences with conspicuous colour patterns as aversive 'warnings' to predators [4]. That such colours are qualitatively honest in signalling the presence of defences is an inherent feature of aposematism, and their evolutionary stability is a predictable consequence of the broad alignment of interests between signallers and receivers [5,6]. ...
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The combined use of noxious chemical defences and conspicuous warning colours is a ubiquitous anti-predator strategy. That such signals advertise the presence of defences is inherent to their function, but their predicted potential for quantitative honesty-the positive scaling of signal salience with the strength of protection-is the subject of enduring debate. Here, we systematically synthesized the available evidence to test this prediction using meta-analysis. We found evidence for a positive correlation between warning colour expression and the extent of chemical defences across taxa. Notably, this relationship held at all scales; among individuals, populations and species, though substantial between-study heterogeneity remains unexplained. Consideration of the design of signals revealed that all visual features, from colour to contrast, were equally informative of the extent of prey defence. Our results affirm a central prediction of honesty-based models of signal function and narrow the scope of possible mechanisms shaping the evolution of aposematism. They suggest diverse pathways to the encoding and exchange of information, while highlighting the need for deeper knowledge of the ecology of chemical defences to enrich our understanding of this widespread anti-predator adaptation.
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Differential predation on species with intraspecific colour variation has been explored in various systems and is often implicated as the driving force behind colour polymorphism maintenance. Here, investigation done on whether predation contributes to the maintenance of extensive colour variation in the Neotropical tortoise beetle, Chelymorpha alternans (Chrysomelidae). Recorded predation rates on different colour pattern phenotypes by three common, generalist invertebrate predators, and identified potential chemical signals of unpalatability. Predaceious mantids (Orthoptera, Mantidae) consumed no beetles, regardless of phenotype, whereas the giant orb‐weaving spider (Trichonephila clavipes; Araneidae) consumed all three beetle phenotypes. The carton‐nest ant, Azteca chartifex (Formicidae), displayed differential predation; the rufipennis phenotype of C. alternans was sometimes consumed, the metallic phenotype was never consumed, and the veraguensis phenotype was consumed in the first three encounters and subsequently discarded, suggesting a learned avoidance behaviour. Using gas chromatography–mass spectrometry, it was determined that cuticular hydrocarbon profiles were similar between the metallic and militaris‐a phenotypes. The rufipennis phenotype showed pronounced differences and displayed the greatest among‐individual variation in elytral cuticular profiles. Between‐phenotype variation in chemical cues, and differences in how predators receive those cues, may mediate predator response, and play a role in maintaining colour variation in this species. Color pattern phenotypes of Chelymorpha alternans experience different levels of predation which may be mediated by differences in contact chemical cues.
Preprint
Chemical defences often vary within and between populations both in quantity and quality, which is puzzling if prey survival is dependent on the strength of the defence. We investigated the within- and between-population variability in chemical defence of the wood tiger moth (Arctia plantaginis). The major components of its defences, SBMP (2secbutyl3methoxypyrazine) and IBMP (2isobutyl3methoxypyrazine) are volatiles that deter bird attacks. We expected the variation to reflect populations predation pressures and early-life conditions. To understand the role of the methoxypyrazines, we experimentally manipulated synthetic SBMP and IBMP and tested the birds reactions. We found a considerable variation in methoxypyrazine amounts and composition, both from wild-caught and laboratory-raised male moths. In agreement with the cost of defence hypothesis, the moths raised in the laboratory had a higher amount of pyrazines. We found that SBMP is more effective at higher concentrations and that IBMP is more effective only in combination with SBMP and at lower concentrations. Our results fit findings from the wild: the amount of SBMP was higher in the populations with higher predation pressure. Altogether, this suggests that, regarding pyrazine concentration, more is not always better, and highlights the importance of testing the efficacy of chemical defence and its components with relevant predators, rather than relying only on results from chemical analyses
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Aposematism and mimicry are complex phenomena which have been studied extensively; however, much of our knowledge comes from just a few focal groups, especially butterflies. Aposematic species combine a warning signal with a secondary defense that reduces their profitability as prey. Aculeate hymenopterans are an extremely diverse lineage defined by the modification of the ovipositor into a stinger which represents a potent defense against predators. Aculeates are often brightly colored and broadly mimicked by members of other arthropod groups including Diptera, Lepidoptera, Coleoptera, and Araneae. However, aculeates are surprisingly understudied as aposematic and mimetic model organisms. Recent studies have described novel pigments contributing to warning coloration in insects and identified changes in cis -regulatory elements as potential drivers of color pattern evolution. Many biotic and abiotic factors contribute to the evolution and maintenance of conspicuous color patterns. Predator distribution and diversity seem to influence the phenotypic diversity of aposematic velvet ants while studies on bumble bees underscore the importance of intermediate mimetic phenotypes in transition zones between putative mimicry rings. Aculeate hymenopterans are attractive models for studying sex-based intraspecific mimicry as male aculeates lack the defense conferred by the females’ stinger. In some species, evolution of male and female color patterns appears to be decoupled. Future studies on aposematic aculeates and their associated mimics hold great promise for unraveling outstanding questions about the evolution of conspicuous color patterns and the factors which determine the composition and distribution of mimetic communities.
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The conspicuous warning signal of aposematic animals is learned by their predators, and the resulting avoidance benefits both parties.1-4 Given evidence that birds can distinguish the profitability of prey from the environmental context in which they appear,5 aposematic insects' host plants might also provide an important cue to foraging predators.6 The aposematic cinnabar moth (Tyria jacobaeae) larva is a specialist on its ragwort (Senecio spp.) host plant,7 presenting a consistent environment with which it could be reliably associated. Additionally, ragwort's defensive toxins prevent non-specialist, profitable insects from feeding on it.8 Thus, avian predators may recognize cues from ragwort, most likely its conspicuous yellow flowers,9,10 and use this information to avoid cinnabars. To test this hypothesis, we exposed artificial cinnabar and non-signaling "caterpillar" targets to wild avian predation by presenting them on ragwort and non-toxic host plants. We also manipulated the presence or absence of ragwort flowers on hosts. In doing so, we show that both targets are better protected on the cinnabar's natural ragwort host and that birds use ragwort's distinctive yellow flowers as the cue to avoidance. Additionally, we found that naive predators do not make prey host foraging distinctions, indicating that this avoidance behavior is learned through experience. Our findings are among the first to suggest that a host plant's features act as an extended phenotype that signals the toxicity of the prey that live on it. This prey-host relationship may facilitate the initial evolution of toxicity in non-signaling prey, but also inhibit the evolution of aposematic signals themselves.
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Many organisms have evolved adaptations to increase the odds of survival of their offspring. Parental care has evolved several times in animals including ectotherms. In amphibians, ~ 10% of species exhibit parental care. Among these, poison frogs (Dendrobatidae) are well-known for their extensive care, which includes egg guarding, larval transport, and specialized tadpole provisioning with trophic eggs. At least one third of dendrobatids displaying aposematism by exhibiting warning coloration that informs potential predators about the presence of defensive skin toxins. Aposematism has a central role in poison frog diversification, including diet specialization, and visual and acoustic communication; and it is thought to have impacted their reproductive biology as well. We tested the latter association using multivariate phylogenetic methods at the family level. Our results show complex relationships between aposematism and certain aspects of the reproductive biology in dendrobatids. In particular, aposematic species tend to use more specialized tadpole-deposition sites, such as phytotelmata, and ferry fewer tadpoles than non-aposematic species. We propose that aposematism may have facilitated the diversification of microhabitat use in dendrobatids in the context of reproduction. Furthermore, the use of resource-limited tadpole-deposition environments may have evolved in tandem with an optimal reproductive strategy characterized by few offspring, biparental care, and female provisioning of food in the form of unfertilized eggs. We also found that in phytotelm-breeders, the rate of transition from cryptic to aposematic phenotype is 17 to 19 times higher than vice versa. Therefore, we infer that the aposematism in dendrobatids might serve as an umbrella trait for the evolution and maintenance of their complex offspring-caring activities.
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Insects have evolved various types of antipredator defenses. For example, many insects have evolved crypsis, and exhibit cryptic body colors and shapes for hiding from predators. Other insects produce toxins as a form of chemical defense against predators, and some toxic insects are aposematic, with conspicuous body colors for advertising their toxins. Insects can also develop hairs, spines or hard exoskeletons as morphological defenses to protect themselves from predation. In addition, insects can evolve behavioral defenses, in which insects exhibit autotomy or dropping, or feign death. This study investigated which predator types evoke these types of defenses, through a review of the effectiveness of antipredator defenses in insects against carnivorous animals that are commonly used as model predators in studies. These predators include other insects, spiders, fish, frogs, lizards, birds and mammals. The results provide the first step for clarifying the evolutionary drivers of antipredator defenses in insects. The following aspects should be considered for future studies: multiple predator species and sufficient replication, alternative prey and predator models, and tolerance to predators in insects. Insects have evolved various types of anti‐predator defenses. This study investigated which predator types evoke defenses, through a review of the effectiveness of anti‐predator defenses in insects against carnivorous animals that are commonly used as model predators in studies. The results provide the first step for clarifying the evolutionary drivers of anti‐predator defenses in insects.
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Aposematism is one of the oldest phenomena in evolutionary biology and still a major puzzle to biologists. Despite its evolutionary nature, most attempts to understand aposematism are devoid of phylogenetic components. In addition, most studies that do take phylogeny into account need to bring the analysis even further. We argue that in order to fully understand aposematism we must have a clear picture of the evolutionary history behind present behaviours. In this paper we frame aposematism in a phylogenetic context and argue that most studies still are wanting in terms of demonstrating aposematism. Aposematism is not an end product but rather evolutionary scenarios including character transformations as well as prey–predator interactions. Finally, we suggest that, regardless how we restrict the concept of aposematism, knowing the directions of events facilitate all kinds of comparisons with a promise of uniting functional and evolutionary aspects into a historization of aposematism.
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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.
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Full-text available
EVOLUTIONARYstudies are hampered by a lack of experimental ways in which to test past events such as the origination of aposematism1-7, whereby unpalatable or poisonous prey signal their unprofitability, often by being warningly coloured. Inexperienced predators do learn to avoid unpalatable prey as a result of such signals8-10, but in addition there may be an inherited cautiousness about attacking when common or conspicuous warning signals are evident11-16. As current predators are not naive in the evolutionary sense, it is still not resolved3-7,17,18 whether aposematism originated only in aggregations of prey19,20 or among solitary prey as well21-23. Here we explore this controversy in evolutionarily naive predators by creating a novel world with warning signals not found in the environment. Initially, the aggregation of prey favoured the warning signals supporting Fisher's view24 of kin aggregations as the evolutionary starting point of aposematism. However, once predators had experienced warning signals, pre-existing avoidance seemed to facilitate evolution of Müllerian mimicry complexes25 with similar types of signals even among solitary prey.
Article
Full-text available
The theory of warning signals dates back to Wallace but is still confusing, controversial and complex. Because predator avoidance of warningly coloured prey (aposematism) is based upon learning and reinforcement, it is difficult to understand how initially rare conspicuous forms subsequently become common. Here, we discuss several possible resolutions to this apparent paradox. Many of these ideas have been largely ignored as a result of implicit assumptions about predator behaviour and assumed lack of variation in the predators, prey and the predation process. Considering the spatial and temporal variation in and mechanisms of behaviour of both predators and prey will make it easier to understand the process and evolution of aposematism.
Article
The handicap theory, in which the cost of waste guarantees honest advertising, is being used increasingly in solutions to the problems of biological signal evolution. However, it is usually applied to systems which are insufficiently understood to allow testing against alternative theories. In particular, the ability of the handicap theory to explain the design of signals has never been properly tested. We test its ability to explain signal design features in an unusually well studied area of biological signalling: warning coloration and mimicry. Since a full handicap model proves immediately unrealistic, we modify the model to incorporate realistic assumptions about predator learning. Using this model we explicitly compare the handicap theory with a purely "conventional" signalling model and with a null model. Predictions relating to three key design features (conspicuousness, pattern similarity, and Batesian mimicry) are compared, and tested against available data. Although many predictions remain to be tested adequately, we conclude that: (i) conspicuousness is most plausibly explained by the conventional signalling theory that ascribes the function of conspicuous coloration to signal efficacy rather than waste; (ii) pattern similarity, within and between species, is unlikely to be the result of the need to produce similar degrees of conspicuousness, as predicted by the handicap theory, but is plausibly explained as the result of pattern generalization amongst discriminating predators, as predicted by the conventional signalling theory; and (iii) Batesian mimicry is predicted by the conventional signalling theory, but not the handicap theory. Therefore the handicap theory fails to provide an adequate explanation of the main design features of at least one major signalling system.
Article
The handicap theory, in which the cost of waste guarantees honest advertising, is being used increasingly in solutions to the problems of biological signal evolution. However, it is usually applied to systems which are insufficiently understood to allow testing against alternative theories. In particular, the ability of the handicap theory to explain the design of signals has never been properly tested. We test its ability to explain signal design features in an unusually well studied area of biological signalling: warning coloration and mimicry. Since a full handicap model proves immediately unrealistic, we modify the model to incorporate realistic assumptions about predator learning. Using this model we explicitly compare the handicap theory with a purely "conventional" signalling model and with a null model. Predictions relating to three key design features (conspicuousness, pattern similarity, and Batesian mimicry) are compared, and tested against available data. Although many predictions remain to be tested adequately, we conclude that: (i) conspicuousness is most plausibly explained by the conventional signalling theory that ascribes the function of conspicuous coloration to signal efficacy rather than waste; (ii) pattern similarity, within and between species, is unlikely to be the result of the need to produce similar degrees of conspicuousness, as predicted by the handicap theory, but is plausibly explained as the result of pattern generalization amongst discriminating predators, as predicted by the conventional signalling theory; and (iii) Batesian mimicry is predicted by the conventional signalling theory, but not the handicap theory. Therefore the handicap theory fails to provide an adequate explanation of the main design features of at least one major signalling system.
Avoiding Attack: The Evolutionary Ecology of Crypsis
  • G D Ruxton
  • T N Sherratt
  • M P Speed
Ruxton, G.D., Sherratt, T.N., and Speed, M.P. (2004). Avoiding Attack: The Evolutionary Ecology of Crypsis, Warning Signals and Mimicry. (Oxford University Press: Oxford).