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Predator psychology and mimicry evolution - a theoretical analysis
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0002-8708-8097
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The evolution of Müllerian mimicry depends on many factors, among which predator psychology is the most important one. Predator avoidance learning, generalization and discrimination are primary selective agents during the evolutionary process. This thesis investigates an issue that has been a matter of debate since the 19th century; the question of how a mutant of a potential mimic population can escape the apostatic selection caused by predators that neither recognize it as a member of its own population, nor as being similar to its future model. In paper I, we investigate one of the ideas concerning this issue. Fisher stated that mimicry can evolve gradually by the displacement of an adaptive peak in a fitness landscape. We find this to be a plausible scenario, under certain conditions regarding predator generalization. In paper II, we further investigate the gradual evolutionary process and the implications of different generalization gradients. We find that the gradual process might be even more general than has previously been assumed and that abundant genetic variation in prey populations is an important factor in combination with predator generalization. In paper III, we examine another suggested solution to the problem of apostatic selection, the so-called two-step process, which can be problematic to extend to multiple prey traits. We find that the two-step process works for multidimensional traits provided that predators use feature-based generalization. The selective landscape of mimicry evolution is also shaped by the cost-benefit relationships for models and mimics. In paper IV we explore this matter, by applying the Rescorla-Wagner theory of learning to mimicry. We find that if variation in prey unpalatability gives rise to surprise, the learning rate is increased. This leads to unexpected kinds of mimicry that are more mutualistic than Müllerian mimicry has previously been assumed to be.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2009. , 34 p.
Keyword [en]
Müllerian mimicry, two-step evolution, gradual evolution, mutualism, predator psychology
National Category
Ecology
Research subject
Ethology
Identifiers
URN: urn:nbn:se:su:diva-29056ISBN: 978-91-7155-903-6 (print)OAI: oai:DiVA.org:su-29056DiVA: diva2:229002
Public defence
2009-09-25, Nordenskiöldsalen, Geovetenskapens hus, Svante Arrhenius väg 8 C, 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. Available from: 2009-09-03 Created: 2009-08-10 Last updated: 2014-10-13Bibliographically approved
List of papers
1. Müllerian mimicry: an examination of Fisher's theory of gradual evolutionary change
Open this publication in new window or tab >>Müllerian mimicry: an examination of Fisher's theory of gradual evolutionary change
2005 (English)In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 272, 2269-2275 p.Article in journal (Refereed) Published
Abstract [en]

In 1927, Fisher suggested that Müllerian mimicry evolution could be gradual and driven by predator generalization. A competing possibility is the so-called two-step hypothesis, entailing that Müllerian mimicry evolves through major mutational leaps of a less-protected species towards a better-protected, which sets the stage for coevolutionary fine-tuning of mimicry. At present, this hypothesis seems to be more widely accepted than Fisher’s suggestion. We conducted individual-based simulations of communities with predators and two prey types to assess the possibility of Fisher’s process leading to a common prey appearance. We found that Fisher’s process worked for initially relatively similar appearances. Moreover, by introducing a predator spectrum consisting of several predator types with different ranges of generalization, we found that gradual evolution towards mimicry occurred also for large initial differences in prey appearance. We suggest that Fisher’s process together with a predator spectrum is a realistic alternative to the two-step hypothesis and, furthermore, that it has fewer problems with purifying selection.  We also examined factors influencing gradual evolution towards mimicry and found that not only the relative benefits from mimicry but also the mutational schemes of the prey types matter.

Keyword
Müllerian mimicry, two-step hypothesis, predator spectrum, advergence, coevolution
Research subject
Zoology
Identifiers
urn:nbn:se:su:diva-29085 (URN)10.1098/rspb.2005.3227 (DOI)
Available from: 2009-08-11 Created: 2009-08-11 Last updated: 2017-12-13Bibliographically approved
2. Evolutionary implications of the form of predator generalisation for aposematic signals and mimicry in prey
Open this publication in new window or tab >>Evolutionary implications of the form of predator generalisation for aposematic signals and mimicry in prey
2008 (English)In: Evolution: International Journal of Organic Evolution, ISSN 1558-5646, Vol. 62, no 11, 2913-2921 p.Article in journal (Refereed) Published
Abstract [en]

Generalization is at the heart of many aspects of behavioral ecology; for foragers it can be seen as an essential feature of learning about potential prey, because natural populations of prey are unlikely to be perfectly homogenous. Aposematic signals are considered to aid predators in learning to avoid a class of defended prey. Predators do this by generalizing between the appearance of prey they have previously sampled and the appearance of prey they subsequently encounter. Mimicry arises when such generalization occurs between individuals of different species. Our aim here is to explore whether the specific shape of the generalization curve can be expected to be important for theoretical predictions relating to the evolution of aposematism and mimicry. We do this by a reanalysis and development of the models provided in two recent papers. We argue that the shape of the generalization curve, in combination with the nature of genetic and phenotypic variation in prey traits, can have evolutionary significance under certain delineated circumstances. We also demonstrate that the process of gradual evolution of Müllerian mimicry proposed by Fisher is particularly efficient in populations with a rich supply of standing genetic variation in mimetic traits.

Keyword
Generalization gradient, Müllerian mimicry, peak shift, warning signals
National Category
Ecology
Identifiers
urn:nbn:se:su:diva-14746 (URN)10.1111/j.1558-5646.2008.00485.x (DOI)000260348100015 ()
Available from: 2008-10-29 Created: 2008-10-29 Last updated: 2014-10-13Bibliographically approved
3. Feature theory and the two-step hypothesis of Müllerian mimicry evolution
Open this publication in new window or tab >>Feature theory and the two-step hypothesis of Müllerian mimicry evolution
2010 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 64, no 3, 810-822 p.Article in journal (Refereed) Published
Abstract [en]

The two-step hypothesis of Müllerian mimicry evolution states that mimicry starts with a major mutational leap between adaptive peaks, followed by gradual fine-tuning. The hypothesis was suggested to solve the problem of apostatic selection producing a valley between adaptive peaks, and appears reasonable for a one-dimensional phenotype. Extending the hypothesis to the realistic scenario of multidimensional phenotypes controlled by multiple genetic loci can be problematic, because it is unlikely that major mutational leaps occur simultaneously in several traits. Here we consider the implications of predator psychology on the evolutionary process. According to feature theory, single prey traits may be used by predators as features to classify prey into discrete categories. A mutational leap in such a trait could initiate mimicry evolution. We conducted individual-based evolutionary simulations in which virtual predators both categorize prey according to features and generalize over total appearances. We found that an initial mutational leap towards feature similarity in one dimension facilitates mimicry evolution of multidimensional traits. We suggest that feature-based predator categorization together with predator generalization over total appearances solves the problem of applying the two-step hypothesis to complex phenotypes, and provides a basis for a theory of the evolution of mimicry rings.

Keyword
Mimicry rings, categorization, generalization, predator psychology
National Category
Ecology
Research subject
Zoology
Identifiers
urn:nbn:se:su:diva-29062 (URN)10.1111/j.1558-5646.2009.00852.x (DOI)000274713800015 ()
Available from: 2009-08-10 Created: 2009-08-10 Last updated: 2017-12-13Bibliographically approved
4. Learning and the mimicry spectrum: from quasi-Bates to super-Müller
Open this publication in new window or tab >>Learning and the mimicry spectrum: from quasi-Bates to super-Müller
2008 (English)In: Animal Behaviour, ISSN 0003-3472, Vol. 76, no 5, 1591-1599 p.Article in journal (Refereed) Published
Abstract [en]

Müllerian mimicry is the mutualistic resemblance between two defended species, while Batesian mimicry is the parasitic resemblance between a palatable species (the mimic) and an unpalatable one (the model). These two kinds of mimicry are traditionally seen as extreme ends of a mimicry spectrum. For the range in between, it has been suggested that mimetic relations between unequally defended species could be parasitic, and this phenomenon has been referred to as quasi-Batesian mimicry. Where a mimetic relation is placed along the mimicry spectrum depends on the assumptions made about predator learning. In this work, we use a variant of the Rescorla-Wagner learning model for virtual predators to analyse the different possible components of the mimicry spectrum. Our model entails that the rate of associative learning is influenced by variation in the stimuli to be learned. Variable stimuli, i.e. unequal defences, can increase the predator learning rate and thus lead to an increased level of mutualism in a mimetic relation. In our analysis, we make use of the concepts of super-Müllerian mimicry, where the benefit of mimicry is even greater than in traditional Müllerian mimicry, and quasi-Müllerian mimicry, where mimicry by a palatable mimic is mutualistic. We suggest that these types of mimicry should be included in the mimicry spectrum along with Müllerian, Batesian and quasi-Batesian mimicry.

Keyword
Associative learning, mutualism, Müllerian mimicry, quasi-Batesian mimicry, Rescorla-Wagner model
National Category
Ecology
Identifiers
urn:nbn:se:su:diva-14644 (URN)10.1016/j.anbehav.2008.07.017 (DOI)000260118100016 ()
Available from: 2008-10-20 Created: 2008-10-20 Last updated: 2014-10-28Bibliographically approved

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