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Evolution of Mimicry and Aposematism Explained: Salient Traits and Predator Psychology
Stockholms universitet, Naturvetenskapliga fakulteten, Zoologiska institutionen.
2017 (engelsk)Doktoravhandling, med artikler (Annet vitenskapelig)
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.

sted, utgiver, år, opplag, sider
Stockholm: Department of Zoology, Stockholm University , 2017. , s. 57
Emneord [en]
imperfect mimicry, mimicry evolution, predator learning, discrimination, generalization, salience, overshadowing, aposematism, warning signal evolution, generalization bias, peak shift
HSV kategori
Forskningsprogram
etologi
Identifikatorer
URN: urn:nbn:se:su:diva-148488ISBN: 978-91-7797-037-8 (tryckt)ISBN: 978-91-7797-038-5 (digital)OAI: oai:DiVA.org:su-148488DiVA, id: diva2:1152974
Disputas
2017-12-01, Vivi Täckholmssalen, NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (engelsk)
Opponent
Veileder
Merknad

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 3: Accepted.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

Tilgjengelig fra: 2017-11-08 Laget: 2017-10-26 Sist oppdatert: 2018-06-11bibliografisk kontrollert
Delarbeid
1. Stimulus Salience as an Explanation for Imperfect Mimicry
Åpne denne publikasjonen i ny fane eller vindu >>Stimulus Salience as an Explanation for Imperfect Mimicry
2014 (engelsk)Inngår i: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 24, nr 9, s. 965-969Artikkel i tidsskrift (Fagfellevurdert) Published
Abstract [en]

The theory of mimicry explains how a mimic species gains advantage by resembling a model species [1-3]. Selection for increased mimic-model similarity should then result in accurate mimicry, yet there are many surprising examples of poor mimicry in the natural world [4-8]. The existence of imperfect mimics remains a major unsolved conundrum. We propose and experimentally test a novel explanation of the phenomenon. We argue that predators perceive prey as having several traits, but that the traits differ in their importance for learning. When predators learn to discriminate prey, high-salience traits overshadow other traits, leaving them under little or no selection for similarity, and allow imperfect mimicry to succeed. We tested this idea experimentally, using blue tits as predators and artificial prey with three prominent traits: color, pattern, and shape. We found that otherwise imperfect color mimics were avoided about as much as perfect mimics, whereas pattern and shape mimics did not gain from their similarity to the model. All traits could separately be perceived and learned by the predators, but the color trait was learned at a higher rate, implying that it had higher salience. We conclude that difference in salience between components of prey appearance is of major importance in explaining imperfect mimicry.

HSV kategori
Forskningsprogram
etologi
Identifikatorer
urn:nbn:se:su:diva-106441 (URN)10.1016/j.cub.2014.02.061 (DOI)000335542300032 ()
Merknad

AuthorCount:4;

Tilgjengelig fra: 2014-08-05 Laget: 2014-08-04 Sist oppdatert: 2017-11-08bibliografisk kontrollert
2. Multi-trait mimicry and the relative salience of individual traits
Åpne denne publikasjonen i ny fane eller vindu >>Multi-trait mimicry and the relative salience of individual traits
2015 (engelsk)Inngår i: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 282, nr 1818, artikkel-id 20152127Artikkel i tidsskrift (Fagfellevurdert) Published
Abstract [en]

Mimicry occurs when one species gains protection from predators by resembling an unprofitable model species. The degree of mimic-model similarity is variable in nature and is closely related to the number of traits that the mimic shares with its model. Here, we experimentally test the hypothesis that the relative salience of traits, as perceived by a predator, is an important determinant of the degree of mimic-model similarity required for successful mimicry. We manipulated the relative salience of the traits of a two-trait artificial model prey, and subsequently tested the survival of mimics of the different traits. The unrewarded model prey had two colour traits, black and blue, and the rewarded prey had two combinations of green, brown and grey shades. Blue tits were used as predators. We found that the birds perceived the black and blue traits similarly salient in one treatment, and mimic-model similarity in both traits was then required for high mimic success. In a second treatment, the blue trait was the most salient trait, and mimic-model similarity in this trait alone achieved high success. Our results thus support the idea that similar salience of model traits can explain the occurrence of multi-trait mimicry.

Emneord
salience, discrimination learning, generalization, overshadowing, imperfect mimicry, evolution, multi-component signals
HSV kategori
Forskningsprogram
etologi
Identifikatorer
urn:nbn:se:su:diva-122229 (URN)10.1098/rspb.2015.2127 (DOI)000364850200019 ()26511051 (PubMedID)
Forskningsfinansiär
Swedish Research Council
Tilgjengelig fra: 2015-10-28 Laget: 2015-10-28 Sist oppdatert: 2017-11-08bibliografisk kontrollert
3. Learning of salient prey traits explains Batesian mimicry evolution
Åpne denne publikasjonen i ny fane eller vindu >>Learning of salient prey traits explains Batesian mimicry evolution
Vise andre…
2018 (engelsk)Inngår i: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 72, nr 3, s. 531-539Artikkel i tidsskrift (Fagfellevurdert) 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.

Emneord
Discrimination learning, generalization, mimicry evolution, salience, two-step hypothesis
HSV kategori
Forskningsprogram
etologi
Identifikatorer
urn:nbn:se:su:diva-154788 (URN)10.1111/evo.13418 (DOI)000427676800008 ()29315519 (PubMedID)
Tilgjengelig fra: 2018-04-17 Laget: 2018-04-17 Sist oppdatert: 2018-06-11bibliografisk kontrollert
4. Biased generalization of salient traits drives the evolution of warning signals
Åpne denne publikasjonen i ny fane eller vindu >>Biased generalization of salient traits drives the evolution of warning signals
2018 (engelsk)Inngår i: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 285, nr 1877, artikkel-id 20180283Artikkel i tidsskrift (Fagfellevurdert) 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.

Emneord
aposematism, learning, generalization, peak shift, salience, signalling
HSV kategori
Forskningsprogram
etologi
Identifikatorer
urn:nbn:se:su:diva-156661 (URN)10.1098/rspb.2018.0283 (DOI)000430868100012 ()29669901 (PubMedID)
Tilgjengelig fra: 2018-06-04 Laget: 2018-06-04 Sist oppdatert: 2018-06-11bibliografisk kontrollert

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