Search Image‐Driven Apostatic Selection and the Evolution of Phenotypic Polymorphism
Authors: Weir Jamie C 
Published: May 2021

AbstractUnderstanding the mechanisms which actively maintain phenotypic variation in natural populations is an important consideration in evolutionary biology. Many cryptic prey species which rely upon avoiding visual detection by predators are also highly polymorphic, seemingly contradicting our expectation that selection would drive such a population towards a single, optimally concealed phenotype. When predators hunt for concealed prey in visually complex environments, they may filter what they see using a ‘search image’, consisting of the recalled phenotypic characters of previously encountered prey items. The use of search images can extend to phenotypically distinct morphs belonging to the same species, and in order to optimise a predator's foraging efficiency, they are more likely to be formed and retained for the most commonly encountered prey morphs. Hypothetically, common intraspecific colour morphs will therefore be subject to nonrandom and disproportionately high levels of predation, favouring the evolution of phenotypic diversity in otherwise cryptic prey species. A large but patchy, complex and often disconnected literature has developed which, although generally supportive of this mechanism, is far from conclusive.Animal colouration is frequently an adaptation both to the environment and the visual and perceptual systems of other organisms, through which that colour is perceived.Many cryptic species are also highly polymorphic, contrary to the expectation that selection would drive the population to an optimally concealed phenotype.Animals face limits on the quantity of visual information which can be processed by their nervous system, often far below the rate at which it is received from the environment.Animals must allocate their finite attention so as to make most efficient use of that incoming information, for example filtering visual information to increase foraging efficiency.Searching a visually complex, information‐rich environment for a well‐concealed object (which requires high levels of attention to discern) is a neurologically taxing process.By filtering their environment using the learned phenotypic characteristics of a desired object (a ‘search image’), animals can increase their likelihood of detecting it in spite of the constraints of their perceptual systems.Allocating much of their finite attention to one highly specific search task makes it more likely that animals will fail to perceive other visual stimuli.If predators search for one particular constituent morph of a polymorphic prey species, they are more likely to overlook other morphs which are phenotypically distinct.In order to optimise foraging efficiency, predators are unlikely to adopt search images of rare prey morphs for a prolonged period since this would be unprofitable.Predators hunting by search images therefore have the potential to exert a specific form of negative frequency‐dependent selection on prey colour morphs known as ‘apostatic selection’, such that their specific perceptual and behavioural mechanisms directly encourage phenotypic diversification among otherwise cryptic species.