Apostatic selection

Last updated August 07, 2023

Apostatic selection is a form of negative frequency-dependent selection. It describes the survival of individual prey animals that are different (through mutation) from their species in a way that makes it more likely for them to be ignored by their predators. It operates on polymorphic species, species which have different forms. In apostatic selection, the common forms of a species are preyed on more than the rarer forms, giving the rare forms a selective advantage in the population.^[1] It has also been discussed that apostatic selection acts to stabilize prey polymorphisms.

The term "apostatic selection" was introduced in 1962 by Bryan Clarke in reference to predation on polymorphic grove snails and since then it has been used as a synonym for negative frequency-dependent selection.^[2] The behavioural basis of apostatic selection was initially neglected, but was eventually established by A.B Bond.^[3]

Apostatic selection can also apply to the predator if the predator has various morphs. There are multiple concepts that are closely linked with apostatic selection. One is the idea of prey switching, which is another term used to look at a different aspect of the same phenomenon, as well as the concept of a search image. Search images are relevant to apostatic selection as it is how a predator is able to detect an organism as a possible prey. Apostatic selection is important in evolution because it can sustain a stable equilibrium of morph frequencies, and hence maintains large amounts of genetic diversity in natural populations.^[4]

It is important to note however, that a rare morph being present in a population does not always mean that apostatic selection will occur, as the rare morph could be targeted at a higher rate. From a predator's view, being able to select for rare morphs actually increases the predator's own fitness.^[5]

Prey switching

In prey switching, predators switch from primary prey to an alternative food source for various reasons.^[6] This is related to apostatic selection because when a rare morph is being selected for, it is going to increase in abundance in a specific population until it becomes recognized by a predator. Prey switching, therefore, seems to be a result of apostatic selection. Prey switching is related to prey preference as well as the abundance of the prey.^[6]

Effects on populations

It has also been determined that apostatic selection causes stabilization of prey polymorphisms due to the limitations of predators' behaviour.^[7] Since the common prey type is more abundant, they should be able to produce more offspring and grow exponentially, at a faster rate then those with the rare morph since they are in much smaller numbers. However, due to the fact that the common morph is preyed upon more frequently, it diminishes their expected rate of reproduction, thus maintaining the population in stable amounts of common and rare morphs.^[7] Essentially, unless an environmental change or an evolutionary change in predator or prey occurs, a stable equilibrium is produced.

Search image

A search image is what an individual uses in order to detect their prey. For the predator to detect something as prey, it must fit their criteria. The rare morph of a species may not fit the search image, and thus not be seen as prey. This gives the rare morphs an advantage, as it takes time for the predator to learn a new search image.^[8] Search image shift require multiple encounters with the new form of prey, and since a rare morph is typically not encountered multiple times, especially in a row, the prey is left undetected. An example of this is how a Blue tit searches for insect prey using a search image, leaving scarcer types of prey untouched. Predatory birds such as insect-eating tits (Parus) sometimes look only for a single cryptic type of prey even though there are other equally palatable cryptic prey present at lower density.^[9] Luuk Tinbergen proposed that this was because the birds formed a search image, a typical image of a prey that a predator can remember and use to spot prey when that image is common.^[10] Having a search image can be beneficial because it increases proficiency of a predator in finding a common morph type.^[11]

Hypothesis for polymorphism

Apostatic selection serves as a hypothesis for the persistence of polymorphism in a population because of the variation it maintains in prey. Apostatic selection has been referred to as "selection for variation in its own sake".^[11] It has been used as an explanation for many types of polymorphism in various species, including diversity in tropical insects. The selective pressure for tropical insects to look as distinct as possible is high because the insects that appear to have the lowest density in a population are the ones that are preyed on the least.^[12]

Environmental mechanisms

In order for apostatic selection to occur, and for the rare morph to have an advantage, a variety of criteria need to be met. First, there needs to be polymorphism present. In addition, the prey cannot be present in equal proportions, since then there would not be a benefit to being able to detect either one.^[13] This is related to frequency-dependent predation, where as the predator obtains the greatest advantage from having a search image for the most common type of prey. This causes the most common form of the prey to be the most vulnerable.^[14] Changes in prey detection by predators do occur, but the speed in which they occur and the flexibility of a predator's search image depend on the environment.

If the frequency of the different prey types continuously changes, the predator may not be able to change its behavior at a rate that will provide an advantage.^[13] In these situations, the predators who are able to change their search image rapidly or have a flexible search image are able to survive. In relation to apostatic selection, rapid changes in prey frequencies can decrease the advantage of the rare morph if their predators have a broad search image or are able to rapidly change their search image.^[13] However, rapid changes in polymorphism frequencies can also be an advantage to the prey with the rare morph. Since long periods of time are generally required for natural selection to act on predators, the degree of flexibility in their search image ^[3] may not be able to be changed over a short time frame.^[13] Therefore, quickly arising rare morphs are favored by apostatic selection if the predators are not able to change their behavior and search image in a short time frame. Thus, this is a biological process that is victim to evolutionary time delay.

Apostatic selection is strongest in environments in which prey with the rare morphism match their background.^[3]

Behavioural basis of apostatic selection

It has been suggested that in frequency-dependent predation, the number of encounters with the prey shapes the predator's ability to detect prey. This is based on the assumption that when the predator is learning foraging behaviour, it is going to obtain the common form of prey most frequently. Since the predator learns from what is most frequently captured, the most common morph is what is identified as prey.^[3] Foraging behaviour is shaped by the learned preference, thus causing apostatic selection and conferring a fitness benefit on the rare prey morphs.^[3] From this, it was concluded that search image formation and adaption is the mechanism that causes the most common prey type to be most easily distinguished from its environment, and thus be eaten more frequently than rarer types.

Experimental evidence

Various types of experiments have been done to look into apostatic selection. Some involve artificial prey because it is easier to control external variables in a simulated environment, though using wild specimens increases the study's external validity. Often a computer screen simulation program is used on animals, such as birds of prey, to detect prey selection.^[15] Another type looks into how apostatic selection can act on the predator as well as the prey, as predator plumage polymorphism can also be influenced by apostatic selection. They hypothesized that a mutant predator morph will become more abundant in a population due to apostatic selection because the prey will not be able to recognize it as often as the common predator morph.^[16] Apostatic selection has been observed in both humans and animals, proving that it is not exclusive to lower organisms, and the cognition it requires is applicable to all organisms which display learning. Though a lot of this work has been experimental and lab controlled, there are some examples of it happening in both wild specimens and in the natural habitat of the species.

In hawks, almost all polymorphism is found on their ventral side. It allows for less common coloration to be favored since it will be recognized the least.^[11] Polymorphism is established by foraging strategies, creating opportunities for apostatic selection.^[16] Because of the different morphs and the varying selection on them, prey perception bias maintains prey polymorphism due to apostatic selection.^[15]

Apostatic selection can be reflected in Batesian mimicry. Aposematism and apostatic selection is used to explain defensive signaling like Batesian mimicry in certain species.^[17] A paper by Pfenning et al., 2006 looks into this concept. In allopatric situations, situations where separate species overlap geographically, mimic phenotypes have high fitness and are selected for when their model is present, but when it is absent, they suffer intense predation. In Pfenning's article it was suggested that this is caused by apostatic selection because strength of selection is higher on the mimics that have their original model present.^[18]

In Batesian mimicry, if the mimic is less common than the model, then the rare mimic phenotype is selected for because the predator has continued reinforcement that the prey is harmful or unpalatable. As the mimic becomes more common than the model, the situation reverses and the mimic is preyed upon more often. Therefore, dishonest signals in prey can be selected for or against depending on predation pressure.^[17]

An example of apostatic selection by birds was observed by Allen and Clarke (1968) in ground-dwelling passerines when they presented wild birds in their natural habitat with artificial, dimorphic prey.^[19] The two colors of prey were presented in 9:1 ratios, and then the prey were switched so both colors had an opportunity to be over or underrepresented.^[19] In all four of the passerine species that were observed, the more common morph of the artificial prey was consumed more frequently regardless of its color.^[19] This study also had a second component in which they allowed the birds to become familiar with one color of the prey, and then presented the dimorphic prey in equal amounts. In this case, the passerines consumed more of the prey that they were accustomed too.^[19] This is consistent with the idea that the search image influences apostatic selection: the familiar form that has been encountered more frequently is the preferred prey.

Apostatic selection has also been studied in cichlid fish, which presents a rare polymorphism: the gold ('Midas') colour morph. Torres-Dowall et al. (2017) discussed how apostatic selection is a plausible mechanism for the maintenance of this Midas morph. They concluded that the rare morph is established by a difference in the predator's probability of detecting the Midas morph.^[20] One limitation of this study was that the morphs in the wild were not able to be manipulated.

Related Research Articles

In evolutionary biology, mimicry is an evolved resemblance between an organism and another object, often an organism of another species. Mimicry may evolve between different species, or between individuals of the same species. Often, mimicry functions to protect a species from predators, making it an anti-predator adaptation. Mimicry evolves if a receiver perceives the similarity between a mimic and a model and as a result changes its behaviour in a way that provides a selective advantage to the mimic. The resemblances that evolve in mimicry can be visual, acoustic, chemical, tactile, or electric, or combinations of these sensory modalities. Mimicry may be to the advantage of both organisms that share a resemblance, in which case it is a form of mutualism; or mimicry can be to the detriment of one, making it parasitic or competitive. The evolutionary convergence between groups is driven by the selective action of a signal-receiver or dupe. Birds, for example, use sight to identify palatable insects and butterflies, whilst avoiding the noxious ones. Over time, palatable insects may evolve to resemble noxious ones, making them mimics and the noxious ones models. In the case of mutualism, sometimes both groups are referred to as "co-mimics". It is often thought that models must be more abundant than mimics, but this is not so. Mimicry may involve numerous species; many harmless species such as hoverflies are Batesian mimics of strongly defended species such as wasps, while many such well-defended species form Müllerian mimicry rings, all resembling each other. Mimicry between prey species and their predators often involves three or more species.

In biology, polymorphism is the occurrence of two or more clearly different morphs or forms, also referred to as alternative phenotypes, in the population of a species. To be classified as such, morphs must occupy the same habitat at the same time and belong to a panmictic population.

Frequency-dependent selection is an evolutionary process by which the fitness of a phenotype or genotype depends on the phenotype or genotype composition of a given population.

Balancing selection refers to a number of selective processes by which multiple alleles are actively maintained in the gene pool of a population at frequencies larger than expected from genetic drift alone. Balancing selection is rare compared to purifying selection. It can occur by various mechanisms, in particular, when the heterozygotes for the alleles under consideration have a higher fitness than the homozygote. In this way genetic polymorphism is conserved.

Batesian mimicry is a form of mimicry where a harmless species has evolved to imitate the warning signals of a harmful species directed at a predator of them both. It is named after the English naturalist Henry Walter Bates, after his work on butterflies in the rainforests of Brazil.

Anti-predator adaptations are mechanisms developed through evolution that assist prey organisms in their constant struggle against predators. Throughout the animal kingdom, adaptations have evolved for every stage of this struggle, namely by avoiding detection, warding off attack, fighting back, or escaping when caught.

The viceroy is a North American butterfly. It was long thought to be a Batesian mimic of the monarch butterfly, but since the viceroy is also distasteful to predators, it is now considered a Müllerian mimic instead.

Müllerian mimicry is a natural phenomenon in which two or more well-defended species, often foul-tasting and sharing common predators, have come to mimic each other's honest warning signals, to their mutual benefit. The benefit to Müllerian mimics is that predators only need one unpleasant encounter with one member of a set of Müllerian mimics, and thereafter avoid all similar coloration, whether or not it belongs to the same species as the initial encounter. It is named after the German naturalist Fritz Müller, who first proposed the concept in 1878, supporting his theory with the first mathematical model of frequency-dependent selection, one of the first such models anywhere in biology.

Ant mimicry or myrmecomorphy is mimicry of ants by other organisms. Ants are abundant all over the world, and potential predators that rely on vision to identify their prey, such as birds and wasps, normally avoid them, because they are either unpalatable or aggressive. Spiders are the most common ant mimics. Additionally, some arthropods mimic ants to escape predation, while others mimic ants anatomically and behaviourally to hunt ants in aggressive mimicry. Ant mimicry has existed almost as long as ants themselves; the earliest ant mimics in the fossil record appear in the mid Cretaceous alongside the earliest ants. Indeed one of the earliest, Burmomyrma, was initially classified as an ant.

Theridion grallator, also known as the Hawaiian happy-face spider, is a spider in the family Theridiidae that resides on the Hawaiian Islands. T. grallator gets its vernacular name of "Hawaiian happy-face spider" from the unique patterns superimposed on its abdomen, specifically those that resemble a human smiling face. T. grallator is particularly notable because of its wide range of polymorphisms that may be studied to allow a better understanding of evolutionary mechanisms. In addition to the variety of color polymorphisms present, T. grallator demonstrates the interesting quality of diet-induced color change, in which its appearance temporarily changes as it metabolizes various food items.

Prey detection is the process by which predators are able to detect and locate their prey via sensory signals. This article treats predation in its broadest sense, i.e. where one organism eats another.

Aggressive mimicry is a form of mimicry in which predators, parasites, or parasitoids share similar signals, using a harmless model, allowing them to avoid being correctly identified by their prey or host. Zoologists have repeatedly compared this strategy to a wolf in sheep's clothing. In its broadest sense, aggressive mimicry could include various types of exploitation, as when an orchid exploits a male insect by mimicking a sexually receptive female, but will here be restricted to forms of exploitation involving feeding. For example, indigenous Australians who dress up as and imitate kangaroos when hunting would not be considered aggressive mimics, nor would a human angler, though they are undoubtedly practising self-decoration camouflage. Treated separately is molecular mimicry, which shares some similarity; for instance a virus may mimic the molecular properties of its host, allowing it access to its cells. An alternative term, Peckhamian mimicry, has been suggested, but it is seldom used.

Prey switching is frequency-dependent predation, where the predator preferentially consumes the most common type of prey. The phenomenon has also been described as apostatic selection, however the two terms are generally used to describe different parts of the same phenomenon. Apostatic selection has been used by authors looking at the differences between different genetic morphs. In comparison, prey switching has been used when describing the choice between different species.

Papilio dardanus, the African swallowtail, mocker swallowtail or flying handkerchief, is a species of butterfly in the family Papilionidae. The species is broadly distributed throughout Sub-Saharan Africa. The British entomologist E. B. Poulton described it as "the most interesting butterfly in the world".

Chemical mimicry is a type of biological mimicry, involving the use of chemicals to dupe an operator. A chemical mimic dupes an operator by showing an adaptive chemical resemblance to an object of its environment and as a consequence receives selective advantage. In all cases of chemical mimicry it has been found that the mimicking species is the only species to benefit from the reaction with either costs or no effect on the duped species. This is by adapting to produce chemicals that will cause a desirable behavioural reaction in the species being deceived and a selective advantage to the mimic. Chemical mimicry exists within many of the different forms of mimicry such as aggressive, protective, Batesian, and Müllerian mimicry and can involve a number of different senses. Mimicking semiochemicals make up some of the most widely used forms of chemical mimicry, but is less apparent than more visual forms. As a result, this topic has been relatively neglected in research and literature. Two examples of organisms displaying chemical mimicry are: the mimicking of Noctuid pheromones by bolas spiders to lure prey; and the duping of insects within their own nests by mimicking their odours in order to enter and hide within the nest undetected.

Many types of polymorphism can be seen in the insect order Lepidoptera. Polymorphism is the appearance of forms or "morphs" differing in color and number of attributes within a single species. In Lepidoptera, polymorphism can be seen not only between individuals in a population but also between the sexes as sexual dimorphism, between geographically separated populations in geographical polymorphism and also between generations flying at different seasons of the year. It also includes the phenomenon of mimicry when mimetic morphs fly alongside non-mimetic morphs in a population of a particular species. Polymorphism occurs both at a specific level with heritable variation in the overall morphological design of individuals as well as in certain specific morphological or physiological traits within a species.

Insects have a wide variety of predators, including birds, reptiles, amphibians, mammals, carnivorous plants, and other arthropods. The great majority (80–99.99%) of individuals born do not survive to reproductive age, with perhaps 50% of this mortality rate attributed to predation. In order to deal with this ongoing escapist battle, insects have evolved a wide range of defense mechanisms. The only restraint on these adaptations is that their cost, in terms of time and energy, does not exceed the benefit that they provide to the organism. The further that a feature tips the balance towards beneficial, the more likely that selection will act upon the trait, passing it down to further generations. The opposite also holds true; defenses that are too costly will have a little chance of being passed down. Examples of defenses that have withstood the test of time include hiding, escape by flight or running, and firmly holding ground to fight as well as producing chemicals and social structures that help prevent predation.

Frequency-dependent foraging is defined as the tendency of an individual to selectively forage on a certain species or morph based on its relative frequency within a population. Specifically for pollinators, this refers to the tendency to visit a particular floral morph or plant species based on its frequency within the local plant community, even if nectar rewards are equivalent amongst different morphs. Pollinators that forage in a frequency-dependent manner will exhibit flower constancy for a certain morph, but the preferred floral type will be dependent on its frequency. Additionally, frequency-dependent foraging differs from density-dependent foraging as the latter considers the absolute number of certain morphs per unit area as a factor influencing pollinator choice. Although density of a morph will be related to its frequency, common morphs are still preferred when overall plant densities are high.

In evolutionary biology, mimicry in vertebrates is mimicry by a vertebrate of some model, deceiving some other animal, the dupe. Mimicry differs from camouflage as it is meant to be seen, while animals use camouflage to remain hidden. Visual, olfactory, auditory, biochemical, and behavioral modalities of mimicry have been documented in vertebrates.

References

↑ Oxford University Press. (2013). Oxford Reference. Retrieved 21 November 2013, from Apostatic Selection: http://www.oxfordreference.com/view/10.1093/oi/authority.20110803095419471
↑ Clarke, B. 1962. Balanced polymorphism and the diversity of sympatric species. Pp. 47–70 in D. Nichols ed. Taxonomy and Geography. Systematics Association, Oxford.
1 2 3 4 5 Cooper, J.M (May 1984). "Apostatic Selection on Prey that Match the Background". Biological Journal of the Linnean Society. 23 (2–3): 221–228. doi:10.1111/j.1095-8312.1984.tb00140.x.
↑ Allen, J.A. (1988) Frequency-dependent selection by predators. Philos. T. Roy. Soc. B 319, 485–503
↑ Rutz, Christian (8 May 2012). "Predator Fitness Increases with Selectivity for Odd Prey". Current Biology. 22 (9): 820–824. doi: 10.1016/j.cub.2012.03.028 . PMID 22503502.
1 2 Suryan, R., Irons, D., & Benson, J. (2000). Prey Switching and Variable Foraging Strategies of Black-Legged Kittiwakes and the Effect on Reproductive Success. The Condor, 374–384.
1 2 Bond, A.B (15 August 2007). "The Evolution of Color Polymorphism: Crypticity, Searching Images, and Apostatic Selection". Annual Review of Ecology, Evolution, and Systematics. 38: 489–514. doi:10.1146/annurev.ecolsys.38.091206.095728.
↑ Fraser, B.A; Hughes, K.A; Tosh, D.N; Rodd, F.H (October 2013). "The role of learning by a predator, Rivulus hartii, in the rare‐morph survival advantage in guppies". Journal of Evolutionary Biology. 26 (12): 2597–2605. doi:10.1111/jeb.12251. PMID 24118199.
↑ Dukas, Reuven, Kamil, Alan. (2000). Limited attention: the constraint underlying search image. Behavioral Ecology, 192–199.
↑ Tinbergen, L. (1960). The natural control of insects in pine woods. Factors influencing the intensity of predation by songbirds. Arch. Neerl. Zool. 13:265–343.
1 2 3 Paulson, D. (2013). Predator Polymorphism and Apostatic Selection. Society for the Study of Evolution, 269–277.
↑ Rand, A. S. (1967). Predator–prey interactions and the evolution of aspect diversity. Atas do Simposio sobre a Biota Amaz6nica 5 (Zool.): 73–83.
1 2 3 4 Merilaita, Sami; Ruxton, Graeme (January 2009). "Optimal apostatic selection: how should predators adjust to variation in prey frequencies?". Animal Behaviour. 77: 239–245. doi:10.1016/j.anbehav.2008.09.032. S2CID 53175552.
↑ Horst, Jonathan; Venable, D.L (January 2018). "Frequency‐dependent seed predation by rodents on Sonoran Desert winter annual plants". Ecology. 99 (1): 196–203. doi: 10.1002/ecy.2066 . PMID 29083479.
1 2 Bond, A., & Kamil, A. (1998). Apostatic selection by blue jays produces balanced polymorphism in virtual prey. Nature, 594–596.
1 2 Fowlie, M., & Kruger, O. (2003). The Evolution of plumage polymorphism in birds of prey and owls: the apostatic selection hypothesis revisited. Journal of Evolutionary Biology, 577–583.
1 2 Matthews, E. G. (1997). Signal-based frequency-dependent defense strategies and the evolution of mimicry. The American Naturalist, 213–222.
↑ Pfenning, D., Harper, G., Brumo, A., Harcombe, W., & Pfenning, K. (2007). Population differences in predation on batesian mimics in allopatry with their model. Behavioral Ecology and Sociobiology, 505–511.
1 2 3 4 Allen, John A.; Clarke, Bryan (November 1968). "Evidence of Apostatic Selection by Wild Passerines". Nature. 220 (5166): 501–502. Bibcode:1968Natur.220..501A. doi:10.1038/220501a0. PMID 5686173. S2CID 4201444.
↑ Torres-Dowall, Julian; Golcher-Benavides, Jimena; Machado-Schiaffino, Gonzalo; Meyer, Axel (September 2017). "The role of rare morph advantage and conspicuousness in the stable gold‐dark colour polymorphism of a crater lake Midas cichlid fish". Journal of Animal Ecology. 86 (5): 1044–1053. doi: 10.1111/1365-2656.12693 . PMID 28502118.

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[1] Oxford University Press. (2013). Oxford Reference. Retrieved 21 November 2013, from Apostatic Selection: http://www.oxfordreference.com/view/10.1093/oi/authority.20110803095419471

[2] Clarke, B. 1962. Balanced polymorphism and the diversity of sympatric species. Pp. 47–70 in D. Nichols ed. Taxonomy and Geography. Systematics Association, Oxford.

[:1-3] 1 2 3 4 5 Cooper, J.M (May 1984). "Apostatic Selection on Prey that Match the Background". Biological Journal of the Linnean Society. 23 (2–3): 221–228. doi:10.1111/j.1095-8312.1984.tb00140.x.

[allen-4] Allen, J.A. (1988) Frequency-dependent selection by predators. Philos. T. Roy. Soc. B 319, 485–503

[5] Rutz, Christian (8 May 2012). "Predator Fitness Increases with Selectivity for Odd Prey". Current Biology. 22 (9): 820–824. doi: 10.1016/j.cub.2012.03.028 . PMID 22503502.

[suryan-6] 1 2 Suryan, R., Irons, D., & Benson, J. (2000). Prey Switching and Variable Foraging Strategies of Black-Legged Kittiwakes and the Effect on Reproductive Success. The Condor, 374–384.

[:0-7] 1 2 Bond, A.B (15 August 2007). "The Evolution of Color Polymorphism: Crypticity, Searching Images, and Apostatic Selection". Annual Review of Ecology, Evolution, and Systematics. 38: 489–514. doi:10.1146/annurev.ecolsys.38.091206.095728.

[8] Fraser, B.A; Hughes, K.A; Tosh, D.N; Rodd, F.H (October 2013). "The role of learning by a predator, Rivulus hartii, in the rare‐morph survival advantage in guppies". Journal of Evolutionary Biology. 26 (12): 2597–2605. doi:10.1111/jeb.12251. PMID 24118199.

[9] Dukas, Reuven, Kamil, Alan. (2000). Limited attention: the constraint underlying search image. Behavioral Ecology, 192–199.

[10] Tinbergen, L. (1960). The natural control of insects in pine woods. Factors influencing the intensity of predation by songbirds. Arch. Neerl. Zool. 13:265–343.

[paulson-11] 1 2 3 Paulson, D. (2013). Predator Polymorphism and Apostatic Selection. Society for the Study of Evolution, 269–277.

[12] Rand, A. S. (1967). Predator–prey interactions and the evolution of aspect diversity. Atas do Simposio sobre a Biota Amaz6nica 5 (Zool.): 73–83.

[:2-13] 1 2 3 4 Merilaita, Sami; Ruxton, Graeme (January 2009). "Optimal apostatic selection: how should predators adjust to variation in prey frequencies?". Animal Behaviour. 77: 239–245. doi:10.1016/j.anbehav.2008.09.032. S2CID 53175552.

[14] Horst, Jonathan; Venable, D.L (January 2018). "Frequency‐dependent seed predation by rodents on Sonoran Desert winter annual plants". Ecology. 99 (1): 196–203. doi: 10.1002/ecy.2066 . PMID 29083479.

[Bond-15] 1 2 Bond, A., & Kamil, A. (1998). Apostatic selection by blue jays produces balanced polymorphism in virtual prey. Nature, 594–596.

[fowlie-16] 1 2 Fowlie, M., & Kruger, O. (2003). The Evolution of plumage polymorphism in birds of prey and owls: the apostatic selection hypothesis revisited. Journal of Evolutionary Biology, 577–583.

[matthews-17] 1 2 Matthews, E. G. (1997). Signal-based frequency-dependent defense strategies and the evolution of mimicry. The American Naturalist, 213–222.

[18] Pfenning, D., Harper, G., Brumo, A., Harcombe, W., & Pfenning, K. (2007). Population differences in predation on batesian mimics in allopatry with their model. Behavioral Ecology and Sociobiology, 505–511.

[:3-19] 1 2 3 4 Allen, John A.; Clarke, Bryan (November 1968). "Evidence of Apostatic Selection by Wild Passerines". Nature. 220 (5166): 501–502. Bibcode:1968Natur.220..501A. doi:10.1038/220501a0. PMID 5686173. S2CID 4201444.

[20] Torres-Dowall, Julian; Golcher-Benavides, Jimena; Machado-Schiaffino, Gonzalo; Meyer, Axel (September 2017). "The role of rare morph advantage and conspicuousness in the stable gold‐dark colour polymorphism of a crater lake Midas cichlid fish". Journal of Animal Ecology. 86 (5): 1044–1053. doi: 10.1111/1365-2656.12693 . PMID 28502118.

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