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Learning of salient prey traits explains Batesian mimicry evolution
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0002-5884-8894
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0002-3445-3759
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0003-4719-487X
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Number of Authors: 52018 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 72, no 3, p. 531-539Article in journal (Refereed) Published
Abstract [en]

Batesian mimicry evolution involves an initial major mutation that produces a rough resemblance to the model, followed by smaller improving changes. To examine the learning psychology of this process, we applied established ideas about mimicry in Papilio polyxenes asterius of the model Battus philenor. We performed experiments with wild birds as predators and butterfly wings as semiartificial prey. Wings of hybrids of P. p. asterius and Papilio machaon were used to approximate the first mutant, with melanism as the hypothesized first mimetic trait. Based on previous results about learning psychology and imperfect mimicry, we predicted that: melanism should have high salience (i.e., being noticeable and prominent), meaning that predators readily discriminate a melanistic mutant from appearances similar to P. machaon; the difference between the first mutant and the model should have intermediate salience to allow further improvement of mimicry; and the final difference in appearance between P. p. asterius and B. philenor should have very low salience, causing improvement to level off. Our results supported both the traditional hypothesis and all our predictions about relative salience. We conclude that there is good agreement between long-held ideas about how Batesian mimicry evolves and recent insights from learning psychology about the role of salience in mimicry evolution.

Place, publisher, year, edition, pages
2018. Vol. 72, no 3, p. 531-539
Keywords [en]
Discrimination learning, generalization, mimicry evolution, salience, two-step hypothesis
National Category
Biological Sciences
Research subject
Ethology
Identifiers
URN: urn:nbn:se:su:diva-154788DOI: 10.1111/evo.13418ISI: 000427676800008PubMedID: 29315519OAI: oai:DiVA.org:su-154788DiVA, id: diva2:1198255
Available from: 2018-04-17 Created: 2018-04-17 Last updated: 2022-02-26Bibliographically 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)
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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: 2022-02-28Bibliographically approved

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Kazemi, BaharanGamberale-Stille, GabriellaWiklund, ChristerLeimar, Olof

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