Pattern edges improve predator learning of aposematic signals

Some defended prey animals can switch on their normally hidden aposematic signals. This switching may occur in reaction to predators’ approach (pre-attack signals) or attack (post-attack signals). Switchable aposematism has been relatively poorly studied, but we can expect that it might bring a variety of benefits to an aposmetic organism. First, the switching could startle the predators (deimatism). Second, it could facilitate aversive learning. Third, it could minimize exposure or energetic expense, as the signal can be switched off. These potential benefits might offset costs of developing, maintaining and utilizing the switchable traits. Here we focused on the third benefit of switchability, the cost-saving aspect, and developed an individual-based computer simulation of predators and prey. In 88,128 model runs, we observed evolution of permanent, pre-attack, or post-attack aposematic signals of varying strength. We found that, in general, the pre-attack switchable aposematism may require moderate predator learning speed, high basal detectability, and moderate to high signal cost. On the other hand, the post-attack signals may arise under slow predator learning, low basal detectability and high signal cost. When predator population turnover is fast, it may lead to evolution of post-attack aposematic signals that are not conforming to the above tendency. We also suggest that a high switching cost may exert different selection pressure on the pre-attack than the post-attack switchable strategies. To our knowledge, these are the first theoretical attempts to systematically explore the evolution of switchable aposematism relative to permanent aposematism in defended prey. Our simulation model is capable of addressing additional questions beyond the scope of this article, and we open the simulation software, program manual and source code for free public use.

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Aposematism

10.1093/oso/9780199688678.003.0007 ◽

2018 ◽

Cited By ~ 2

Author(s):

Graeme D. Ruxton ◽

William L. Allen ◽

Thomas N. Sherratt ◽

Michael P. Speed

Keyword(s):

Secondary Effects ◽

Warning Coloration ◽

Common Features ◽

Initial Evolution ◽

The Common ◽

Aposematic Signals

Aposematism is the pairing of two kinds of defensive phenotype: an often repellent secondary defence that typically renders prey unprofitable to predators if they attack them and some evolved signal that indicates the presence of that defence. Aposematic signals often work to modify the behaviours of predators both before and during attacks. Warning coloration, for example, may increase wariness and hence improve the chances that a chemically defended prey is released unharmed after an attack. An aposematic signal may therefore first tend to reduce the probability that a predator commences attack (a primary defence) and then (as a component of secondary defence) reduce the probability that the prey is injured or killed during any subsequent attack. In this chapter we will consider both the primary and the secondary effects of aposematic signals on prey protection. We begin first by describing the common features of aposematic signals and attempting to show the wide use to which aposematic signalling is deployed across animals (and perhaps plants too). We then review the interesting evolutionary issues aposematic signals raise, including their initial evolution and their integration with sexual and other signals. We also discuss important ecological, co-evolutionary, and macroevolutionary consequences of aposematism.

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Stabilizing selection on individual pattern elements of aposematic signals

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.0926 ◽

2017 ◽

Vol 284 (1861) ◽

pp. 20170926 ◽

Cited By ~ 17

Author(s):

Anne E. Winters ◽

Naomi F. Green ◽

Nerida G. Wilson ◽

Martin J. How ◽

Mary J. Garson ◽

...

Keyword(s):

Pattern Analysis ◽

Marine Organism ◽

Warning Signal ◽

Colour Pattern ◽

Stabilizing Selection ◽

Warning Signals ◽

Fish Predator ◽

Selection For ◽

Aposematic Signals ◽

Behavioural Experiments

Warning signal variation is ubiquitous but paradoxical: low variability should aid recognition and learning by predators. However, spatial variability in the direction and strength of selection for individual elements of the warning signal may allow phenotypic variation for some components, but not others. Variation in selection may occur if predators only learn particular colour pattern components rather than the entire signal. Here, we used a nudibranch mollusc, Goniobranchus splendidus , which exhibits a conspicuous red spot/white body/yellow rim colour pattern, to test this hypothesis. We first demonstrated that secondary metabolites stored within the nudibranch were unpalatable to a marine organism. Using pattern analysis, we demonstrated that the yellow rim remained invariable within and between populations; however, red spots varied significantly in both colour and pattern. In behavioural experiments, a potential fish predator, Rhinecanthus aculeatus , used the presence of the yellow rims to recognize and avoid warning signals. Yellow rims remained stable in the presence of high genetic divergence among populations. We therefore suggest that how predators learn warning signals may cause stabilizing selection on individual colour pattern elements, and will thus have important implications on the evolution of warning signals.

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THE EFFECTS OF PREDATOR LEARNING, FORGETTING, AND RECOGNITION ERRORS ON THE EVOLUTION OF WARNING COLORATION

Evolution ◽

10.1111/j.0014-3820.2000.tb00077.x ◽

2000 ◽

Vol 54 (3) ◽

pp. 751-763 ◽

Cited By ~ 59

Author(s):

Maria R. Servedio

Keyword(s):

Warning Coloration ◽

Predator Learning ◽

Recognition Errors

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Living in mixed species groups promotes predator learning in degraded habitats

Scientific Reports ◽

10.1038/s41598-021-98224-0 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Douglas P. Chivers ◽

Mark I. McCormick ◽

Eric P. Fakan ◽

Randall P. Barry ◽

Maud C. O. Ferrari

Keyword(s):

Predation Risk ◽

Abiotic Factors ◽

Alarm Cues ◽

Learning Mechanisms ◽

Trade Offs ◽

Chemical Alarm Cues ◽

Pomacentrus Amboinensis ◽

Predator Foraging ◽

Predator Learning ◽

Predator Odour

AbstractLiving in mix-species aggregations provides animals with substantive anti-predator, foraging and locomotory advantages while simultaneously exposing them to costs, including increased competition and pathogen exposure. Given each species possess unique morphology, competitive ability, parasite vulnerability and predator defences, we can surmise that each species in mixed groups will experience a unique set of trade-offs. In addition to this unique balance, each species must also contend with anthropogenic changes, a relatively new, and rapidly increasing phenomenon, that adds further complexity to any system. This complex balance of biotic and abiotic factors is on full display in the exceptionally diverse, yet anthropogenically degraded, Great Barrier Reef of Australia. One such example within this intricate ecosystem is the inability of some damselfish to utilize their own chemical alarm cues within degraded habitats, leaving them exposed to increased predation risk. These cues, which are released when the skin is damaged, warn nearby individuals of increased predation risk and act as a crucial associative learning tool. Normally, a single exposure of alarm cues paired with an unknown predator odour facilitates learning of that new odour as dangerous. Here, we show that Ambon damselfish, Pomacentrus amboinensis, a species with impaired alarm responses in degraded habitats, failed to learn a novel predator odour as risky when associated with chemical alarm cues. However, in the same degraded habitats, the same species learned to recognize a novel predator as risky when the predator odour was paired with alarm cues of the closely related, and co-occurring, whitetail damselfish, Pomacentrus chrysurus. The importance of this learning opportunity was underscored in a survival experiment which demonstrated that fish in degraded habitats trained with heterospecific alarm cues, had higher survival than those we tried to train with conspecific alarm cues. From these data, we conclude that redundancy in learning mechanisms among prey guild members may lead to increased stability in rapidly changing environments.

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The fish that cried wolf: the role of parental care in novel predator recognition in juvenile convict cichlids (Amatitlania siquia)

Behaviour ◽

10.1163/1568539x-00003381 ◽

2016 ◽

Vol 153 (8) ◽

pp. 963-980 ◽

Cited By ~ 1

Author(s):

Layla Al-Shaer ◽

Timothy Paciorek ◽

Zachary Carroll ◽

Murray Itzkowitz

Keyword(s):

Antipredator Behaviour ◽

Unique Form ◽

Treatment Groups ◽

Convict Cichlids ◽

Predator Learning ◽

Parental Ability ◽

Experimental Group ◽

Predator Odour ◽

Amatitlania Siquia

This study tested if convict cichlids (Amatitlania siquia) with prior predator experience could socially transfer their predator knowledge to their offspring. Prior to reproduction, pairs were assigned to either an experimental or control associative learning treatment, and given novel predator odour from a wolf cichlid (Parachromis dovii) paired with either alarm cue or water respectively. We hypothesized that upon re-exposure to the odour, experimental pairs would socially transfer their acquired predator knowledge to their naïve offspring, which in turn would exhibit antipredator behaviour. While fry from both treatment groups did not show a difference in shoal formation, there is some evidence to suggest a trend in the experimental group regarding parental ability to transfer information to offspring and influence shoal behaviour. When tested individually, experimental fry decreased their activity more than control fry in the presence of the predator odour. This study provides evidence of a unique form of predator learning between parents and offspring, suggesting that biparental care may also serve to provide offspring with information about the habitat into which they are born.

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Advergence in Müllerian mimicry: the case of the poison dart frogs of Northern Peru revisited

Biology Letters ◽

10.1098/rsbl.2011.0039 ◽

2011 ◽

Vol 7 (5) ◽

pp. 796-800 ◽

Cited By ~ 15

Author(s):

Mathieu Chouteau ◽

Kyle Summers ◽

Victor Morales ◽

Bernard Angers

Keyword(s):

Nuclear Dna ◽

Phenotypic Variability ◽

Model Species ◽

Müllerian Mimicry ◽

Mitochondrial Haplotypes ◽

Ranitomeya Imitator ◽

Northern Peru ◽

Mullerian Mimicry ◽

Aposematic Signals ◽

Rule Out

Whether the evolution of similar aposematic signals in different unpalatable species (i.e. Müllerian mimicry) is because of phenotypic convergence or advergence continues to puzzle scientists. The poison dart frog Ranitomeya imitator provides a rare example in support of the hypothesis of advergence: this species was believed to mimic numerous distinct model species because of high phenotypic variability and low genetic divergence among populations. In this study, we test the evidence in support of advergence using a population genetic framework in two localities where R. imitator is sympatric with different model species, Ranitomeya ventrimaculata and Ranitomeya variabilis . Genetic analyses revealed incomplete sorting of mitochondrial haplotypes between the two model species. These two species are also less genetically differentiated than R. imitator populations on the basis of both mitochondrial and nuclear DNA comparisons. The genetic similarity between the model species suggests that they have either diverged more recently than R. imitator populations or that they are still connected by gene flow and were misidentified as different species. An analysis of phenotypic variability indicates that the model species are as variable as R. imitator . These results do not support the hypothesis of advergence by R. imitator . Although we cannot rule out phenotypic advergence in the evolution of Müllerian mimicry, this study reopens the discussion regarding the direction of the evolution of mimicry in the R. imitator system.

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