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Biased generalization of salient traits drives the evolution of warning signals
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology.
Number of Authors: 42018 (English)In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 285, no 1877, article id 20180283Article in journal (Refereed) Published
Abstract [en]

The importance of receiver biases in shaping the evolution of many signalling systems is widely acknowledged. Here, we show that receiver bias can explain which traits evolve to become warning signals. For warning coloration, a generalization bias for a signalling trait can result from predators learning to discriminate unprofitable from profitable prey. However, because the colour patterns of prey are complex traits with multiple components, it is crucial to understand which of the many aspects of prey appearance evolve into signals. We provide experimental evidence that the more salient differences in prey traits give rise to greater generalization bias, corresponding to stronger selection towards trait exaggeration. Our results are based on experiments with domestic chickens as predators in a Skinner-box-like setting, and imply that the difference in appearance between profitable and unprofitable prey that is most rapidly learnt produces the greatest generalization bias. As a consequence, certain salient traits of unprofitable prey are selected towards exaggeration to even higher salience, driving the evolution of warning coloration. This general idea may also help to explain the evolution of many other striking signalling traits found in nature.

Place, publisher, year, edition, pages
2018. Vol. 285, no 1877, article id 20180283
Keywords [en]
aposematism, learning, generalization, peak shift, salience, signalling
National Category
Biological Sciences
Research subject
Ethology
Identifiers
URN: urn:nbn:se:su:diva-156661DOI: 10.1098/rspb.2018.0283ISI: 000430868100012PubMedID: 29669901OAI: oai:DiVA.org:su-156661DiVA, id: diva2:1213233
Available from: 2018-06-04 Created: 2018-06-04 Last updated: 2018-06-11Bibliographically approved
In thesis
1. Evolution of Mimicry and Aposematism Explained: Salient Traits and Predator Psychology
Open this publication in new window or tab >>Evolution of Mimicry and Aposematism Explained: Salient Traits and Predator Psychology
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Aposematic species have evolved conspicuous warning signals, such as bright colors and striking patterns, to deter predators. Some edible and harmless species take advantage of this deterrent effect by mimicking their appearance. Mimicry is a great example of how natural selection produces remarkable adaptations. However, while some species evolve a very close similarity to their models to effectively avoid attacks, others are successful in doing so despite an incomplete similarity, i.e. imperfect mimicry. In some cases, it is surprising how such a crude disguise can fool predators. Why and how imperfect mimicry can persist has been much discussed and considered as a problem for the theory of natural selection. It is therefore of great interest to understand what makes it possible.

Predator psychology is an important factor in the evolution of aposematism and mimicry. In the past decades it has been suggested that certain components of prey appearance are more important to predators than others during prey assessment. We developed this idea by incorporating concepts from associative learning, and presented a new approach to explain imperfect mimicry. Our general hypothesis is that prey traits have different salience to predators. Certain traits are perceived as highly salient and are thus used primarily in the discrimination and generalization of prey, while traits with low salience are overshadowed and not used in the assessment. The salience of a trait can depend on how conspicuous or discriminable it is in the particular context, and can vary due to for example previous predator experience.

We tested our ideas with wild blue tits and domestic chickens as predators, and artificial and semi-natural prey stimuli. In paper I we found that the trait that was perceived as most salient (color) was the one used to discriminate and generalize between prey. Mimics of that specific trait were highly avoided, despite differences in the other traits. We also found that salience is relative and context dependent (paper II). In a context where two traits were perceived as similarly salient, mimicry of a single trait offered intermediate protection, while mimicry of both offered high protection. In another context, the traits were perceived differently salient, and mimicry of one trait was enough for high protection. In paper III we tested a proposed scenario for the initiation of mimicry evolution in the edible butterfly mimic Papilio polyxenes asterius to its noxious model Battus philenor. The results showed that a partial similarity with the model in the salient black wing color offered intermediate protection from attacks, despite a general dissimilarity.

This thesis investigates the major questions of imperfect mimicry: the initial step of mimicry evolution, the persistence of imperfect mimicry, and variation in mimic-model similarity. We conclude that mimicry evolution can begin in a non-mimetic species that acquires similarity to a model species in a high-salience trait. When multiple traits have similar salience, multi-trait mimicry is needed for higher protection. Mimicry can remain imperfect if the differences are in traits with low salience, and therefore under low or no selection pressure to change.

To complete the picture, we showed that predators can have a biased generalization toward a more pronounced version of a salient trait (paper IV). The evolution of aposematism could therefore be explained by gradual enhancement of salient traits.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University, 2017. p. 57
Keywords
imperfect mimicry, mimicry evolution, predator learning, discrimination, generalization, salience, overshadowing, aposematism, warning signal evolution, generalization bias, peak shift
National Category
Behavioral Sciences Biology
Research subject
Ethology
Identifiers
urn:nbn:se:su:diva-148488 (URN)978-91-7797-037-8 (ISBN)978-91-7797-038-5 (ISBN)
Public defence
2017-12-01, Vivi Täckholmssalen, NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 3: Accepted. Paper 4: Manuscript.

Available from: 2017-11-08 Created: 2017-10-26 Last updated: 2018-06-11Bibliographically approved

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