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Two alternative adaptive landscapes observed in a coral snake Batesian mimicry complex. (a) No adaptive valley in Florida where coral snakes are highly abundant models. An a priori contrast showed no difference between the attack rate on the intermediate phenotype (interm.) versus the attack rate on cryptic and mimetic phenotypes. (b) Selection against intermediate phenotypes around southern North Carolina where coral snakes are rare. The intermediate phenotype is attacked at a higher rate than cryptic and mimetic phenotypes. Asterisk indicates statistical significance.
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In Batesian mimicry, a harmless species (the 'mimic') resembles a dangerous species (the 'model') and is thus protected from predators. It is often assumed that the mimetic phenotype evolves from a cryptic phenotype, but it is unclear how a population can transition through intermediate phenotypes; such intermediates may receive neither the benefit...
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Batesian mimicry is often imprecise. An underexplored explanation for imperfect mimicry is that predators might not be able to use all dimensions of prey phenotype to distinguish mimics from models and thus permit imperfect mimicry to persist. We conducted a field experiment to test whether or not predators can distinguish deadly coral snakes (Micr...
Citations
... For the coral snake mimicry complex in the southeastern United States, this research has documented the presence of mimics is dependent on the frequency of coral snakes (Pfennig et al., 2001), demonstrated that the precision of mimicry is dependent on predator cognition (Kikuchi et al., 2010b), and provided evidence that mimicry can generate reproductive isolation among mimic populations (Pfennig et al., 2015). This body of work has also shown that both sympatry and abundance of the model influences predation of coral snake mimics (Harper et al., 2007;Kikuchi et al., 2010a). In the tropics, where both coral snakes and coral snake mimics are at their peak richness, clay model studies have demonstrated that predators can avoid coral snake banding patterns (Smith, 1975;Brodie III, 1993;França et al., 2017). ...
Snakes have evolved extraordinary diversity in coloration, which is strongly linked to fitness and represents a major axis of phenotypic diversity in snakes. In this chapter, we discuss the integrative biology of snake coloration and identify future research targets in the field. First, we explore the ways that researchers define and quantify snake coloration, characterize interspecific diversity, and delimit intraspecific diversity (including ontogenetic color shifts, sexual dichromatism, geographic color variation, and color polymorphism). Second, we synthesize what is known about the mechanisms of the production of coloration in snakes, from identifying the sources of color (pigments or structural color) and color texture (matte and iridescence) to classifying the cells and tissues involved in color and color pattern and describing the quantitative and transmission genetics of snake coloration. Third, we discuss historical and contemporary approaches to studying the functional biology of snake coloration. We achieve this by considering snakes as both signalers and receivers of color information and discussing tradeoffs across the multiple functions of snake coloration, such as thermoregulation and predator defense. Fourth, we examine evidence for the drivers of color evolution by considering the role of neutral and selective forces that impact snake coloration, identifying the ecological agents of selection, and discussing potential evolutionary constraints on coloration in snakes. Finally, we explore macroevolutionary patterns of snake coloration, including phylogenetic tests of color variation, directionality of transitions and rates of change, and ecological correlates of coloration in snakes. Ultimately, future research that unites these conceptual approaches and data across disciplines will be crucial for understanding the factors that structure color variation across the snake tree of life.
... Such colour variants can thus present particularly fertile systems for ecological and evolutionary analysis (Bates, 1862;Joron & Mallet, 1998). In particular, researchers have sought to understand the genetic mechanisms by which seemingly intricate 'warning' colouration patterns can evolve repeatedly across independent lineages (Ferguson et al., 2011;Kunte et al., 2014) and the potential adaptive role of intermediate phenotypes, which have been thought to represent evolutionary 'stepping stones' (Kikuchi & Pfennig, 2010;Ruxton et al., 2019). Additionally, the rare occurrence of Batesian polymorphisms, in which only some members of a population resemble a noxious 'model' (Mallet & Joron, 1999;Tsurui-Sato et al., 2019), leads to questions regarding the potential key role of frequency-dependent selection as a driver of evolutionary diversification. ...
The evolution of Batesian mimicry - whereby harmless species avoid predation through their resemblance to harmful species - has long intrigued biologists. In rare cases, Batesian mimicry is linked to intraspecific colour variation, in which only some individuals within a population resemble a noxious 'model'. Here, we assess intraspecific colour variation within a widespread New Zealand stonefly, wherein highly melanized individuals of Zelandoperla closely resemble a chemically defended aposematic stonefly, Austroperla cyrene. We assess convergence in the colour pattern of these two species, compare their relative palatability to predators, and use genome-wide association mapping to assess the genetic basis of this resemblance. Our analysis reveals that melanized Zelandoperla overlap significantly with Austroperla in colour space but are significantly more palatable to predators, implying that they are indeed Batesian mimics. Analysis of 194,773 genome-wide SNPs reveals an outlier locus (ebony) strongly differentiating melanic versus non-melanic Zelandoperla. Genotyping of 338 specimens from a single Zelandoperla population indicates that ebony explains nearly 70% of the observed variance in melanism. As ebony has a well-documented role in insect melanin biosynthesis, our findings indicate this locus has a conserved function across deeply divergent hexapod lineages. Distributional records suggest a link between the occurrence of melanic Zelandoperla and the forested ecosystems where the model Austroperla is abundant, suggesting the potential for adaptive shifts in this system underpinned by environmental change.
... Empirical studies (e.g. Dunn 1954, Sheppard 1959, Brower and Brower 1962, Pfennig et al. 2001, Harper and Pfennig 2007, Kikuchi and Pfennig 2010, Kikuchi et al. 2021) and simulations (e.g. Charlesworth and Charlesworth 1975, Turner et al. 1984 have found support for the frequency effect while others have questioned it (e.g. ...
We propose a feedback model for Batesian mimetic trophic system dynamics that integrates evolutionary and ecological processes including those not directly related to mimicry such as nutrient transfer. The proposed feedback circuit includes a previously overlooked link, specifically: selection for predation on the mimetic phenotype, which results when predators consume palatable mimics, and which perpetuates predation on the mimetic phenotype that drives mimicry. Preservation of variation throughout the feedback loop may also explain polymorphism, suboptimal mimicry, and other aspects of mimetic trophic system evolution.
... Undefended mimics can have a negative effect predator's learning (Lindström et al. 1997, Rowland et al. 2010, suggesting that Batesian mimicry could evolve and be maintained only in species with a low density compared to the model species. Moreover, a high abundance of the model species compared to the potential mimics also increases the protection of imperfect mimics allowing the evolution of gradual Batesian mimicry (Kikuchi & Pfennig 2010). The relative density between the focal and the model species is especially important when assuming reproductive interference, because the costs generated by heterospecific interactions depend on the proportion of heterospecific males encountered by females. ...
The striking female-limited mimicry observed in some butterfly species is a text-book example of sexually-dimorphic trait submitted to intense natural selection. Two main evolutionary hypotheses, based on natural and sexual selection respectively, have been proposed. Predation pressure favouring mimicry toward defended species could be higher in females because of their slower flight, and thus overcome developmental constraints favouring the ancestral trait that limits the evolution of mimicry in males but not in females. Alternatively, the evolution of mimicry in males could be limited by female preference for non-mimetic males. However, the evolutionary origin of female preference for non-mimetic males remains unclear. Here, we hypothesise that costly sexual interactions between individuals from distinct sympatric species might intensify because of mimicry, therefore promoting female preference for non-mimetic trait. Using a mathematical model, we compare the evolution of female-limited mimicry when assuming either alternative selective hypotheses. We show that the patterns of divergence of male and female trait from the ancestral traits can differ between these selection regimes. We specifically highlight that divergence in female trait is not a signature of the effect of natural selection. Our results also evidence why female-limited mimicry is more frequently observed in Batesian mimics. This article is protected by copyright. All rights reserved.
... Indeed, Müllerian mimicry, whereby different defended prey species living in sympatry share the same colour pattern, reduces the individual predation risk (Müller 1879). The protection gained by prey with a different level of conspicuousness then depends on the level of similarity of the colour pattern they displayed to the local mimicry rings, and on the generalization behaviour of predators (Kikuchi and Pfennig 2010, Merrill et al. 2012, Chouteau et al. 2016. ...
Variation in the conspicuousness of colour patterns is observed within and among defended prey species. The evolution of conspicuous colour pattern in defended species can be strongly impaired because of increased detectability by predators. Nevertheless, such evolution of the colour pattern can be favoured if changes in conspicuousness result in Müllerian mimicry with other defended prey. Here, we develop a model describing the population dynamics of a conspicuous defended prey species, and we assess the invasion conditions of derived phenotypes that differ from the ancestral phenotype by their conspicuousness. Such change in conspicuousness may then modify their level of mimicry with the local community of defended species. Derived colour pattern displayed in this focal population can therefore be either exactly similar, partially resembling or completely dissimilar to the local mimicry ring displaying the ancestral colour pattern. We assume that predation risk depends 1) on the number of individuals sharing a given colour pattern within the population, 2) on the occurrence of co‐mimetic defended species and 3) on the availability of alternative edible prey. Using a combination of analytical derivations and numerical simulations, we show that colour patterns that are less conspicuous than the ancestral one are generally favoured within mimicry rings, unless reduced conspicuousness impairs mimicry. By contrast, when a mutation affecting the colour pattern leads to a shift toward a better protected mimicry ring, a more conspicuous colour pattern can be favoured. The selected aposematic pattern then depends on the local communities of defended and edible prey, as well as on the detectability, memorability and level of mimicry of the colour patterns.
... As relatively common species, they were readily available as a model for alienopterid nymphs. Model-mimic evolution probably favoured body shapes of alienopterid nymphs corresponding to the most frequent and suitable models in the local environment, a phenomenon widespread in extant ecosystems (Ceccarelli and Crozier, 2007;Kikuchi and Pfennig, 2010;Quicke, 2017). ...
Alienopteridae are among the most perplexing fossil insects and once conspicuous members of Cretaceous Dictyoptera (now including cockroaches, termites and mantises). However, the precise nature of their life history, evolution, and phylogenetic affinities remained controversial and open to debate. Here we report new alienopterid nymphs from mid-Cretaceous Kachin amber (approximately 99 Ma) and define three nymphal morphotypes, along with proposed interpretations of their life style. We also re-evaluate the systematic position of Alienopteridae, and of the recently erected order Aethiocarenodea. Geometric morphometric analyses suggest that morphotype I nymphs exhibit distinct morphological specializations that were most likely associated with ant mimicry, like immature stages of some modern crown mantises. Remarkably, mimetic association between these nymphs and stem-group ants provides the earliest record of ant mimicry (myrmecomorphy), which is contemporary with the earliest ants and their eusociality. We discuss different interpretations of the life history of alienopterid adults, especially wasp mimicry, and conclude that Teyia was likely a wasp mimic. The nymphs (morphotype I) and adults of Teyia resemble different models, which provides the first fossil record of transformational mimicry, implying that this behaviour had already evolved by the mid-Cretaceous. In addition, one alienopterid nymph laden with pollen clumps provides evidence for gymnosperm pollination and a previously unknown gymnosperm-insect association. This suggests that extinct dictyopterans might have been among the earliest pollinators, with a hitherto undervalued role in pollination ecology. Our phylogenetic analysis provides evidence that Alienopteridae and Umenocoleidae together constitute a monophyletic group (Alienoptera), which is placed as sister taxon of Mantodea. Alienoptera including Umenocoleidae were supported as a separate lineage, and mainly characterized by sclerotized shell-like tegmina and unique leg structures, their main diversification probably occurred before the J/K boundary, and we suggest a common evolutionary origin during the Late Jurassic.
... In this situation, the phenotype of the lookalike is not dependent on the coral snake and therefore does not qualify as a Batesian mimic. The reasons for the different interpretations of these similarities include differing functions of the colour patterns (Brattstrom, 1955;Pough, 1976;Niskanen & Mappes, 2005;Allen et al., 2013;Titcomb et al., 2014), the high lethality of coral snake venom (Gans, 1961;Huheey, 1980;Brodie & Brodie, 1999;DuVal et al., 2006), the responses of predators when introduced to coral snakes (Livdahl, 1979;Brugger, 1989;Beckers et al., 1996;Kikuchi & Pfennig, 2010;Pfennig & Kikuchi, 2012;Akcali et al., 2019), and the geographical distribution of coral snakes and their lookalikes Harper & Pfennig, 2008;Kikuchi & Pfennig, 2009;Pfennig & Mullen, 2010;Pfennig & Kikuchi, 2012;Rabosky et al., 2016b;França et al., 2017;Akcali et al., 2018). ...
... As previously stated, there are various suggestions regarding why the allopatric distribution of these snakes is both persistent and remains feasible in a Batesian framework. For example, empirical field experiments using plasticine replicas were performed (Pfennig et al., 2001;Kikuchi & Pfennig, 2009;Akcali & Pfennig, 2017) in areas where coral snakes and their lookalikes exist together and in areas where only lookalikes exist. Predatory attacks on coral snake and mimetic replicas were found to occur more often in allopatric regions than in areas of sympatry, showing that as the abundance of the venomous coral snake decreases, the protection it provides via Batesian mimicry breaks down (Pfennig et al., 2001;Akcali & Pfennig, 2017). ...
Venomous coral snakes and non-venomous coral snake lookalikes are often regarded as a classic example of Batesian mimicry, whereby a harmless or palatable organism imitates a harmful or less palatable organism. However, the validity of this claim is questionable. The existing literature regarding coral snake mimicry presents a divisive stance on whether Batesian mimicry is occurring or whether the similarity between snakes is attributable to alternative factors. Here, we compile available literature on coral snake mimicry and assess the support for Batesian mimicry. We find that most of the recent relevant literature (after approximately 2000) supports the Batesian mimicry hypothesis. However, this is not strongly supported by empirical evidence. Potential considerations addressed here for both the Batesian and alternative hypotheses include the function of the colour pattern, predatory learning and the biogeographical distribution of similar snakes. The analyses performed previously by mimicry researchers show that the interpretation of the conditions for mimicry is not consistent throughout the scientific community when applied to coral snake systems. This review focuses on this division and stresses the need to reach an agreement about the adaptive significance of New World coral snakes and their lookalikes.
... spiders, flies, butterflies, snakes) showing stable occurrence suggesting that inaccurate mimics might be on the adaptive peak (Ruxton et al., 2019). A number of hypotheses have been proposed to explain the evolution and persistence of inaccurate mimics, such as (1) the imitation of a phenotype intermediate between several models (Edmunds, 2000); (2) the imitation of very noxious or very abundant models (Kikuchi & Pfennig, 2010;Lindström et al., 1997); (3) allopatric distribution with the model (Harper & Pfennig, 2008); (4) kin selection if the model is rare or weakly aversive and the mimics are closely related (e.g. Johnstone, 2002); (5) failure to classify mimics as precise due to human's perception biases (Dittrich et al., 1993); (6) relaxed selection on small body size due to unprofitability (Penney et al., 2012) or (7) the constraints hypothesis which holds that inaccurate mimics fail to evolve accuracy due to certain constraints (Kikuchi & Pfennig, 2013). ...
Aim
The evolution and maintenance of accurate Batesian mimicry has been explained by several hypotheses built upon relaxed selection. However, selection can be influenced by ecological factors, such as habitat type or geographical distribution, which have not been considered.
Location
Worldwide.
Taxon
Araneae.
Methods
I gathered data on body size, geographical area of distribution (temperate, subtropical, tropical), and habitat stratification (ground, low vegetation, bush, tree) from literature on more than 400 ant-mimicking (myrmecomorphic) spider species from 18 spider families. I ranked them into four accuracy levels based on morphology, from poor inaccurate mimics to very accurate ones. I used regression to study the effect of body size, distribution, and habitat on mimetic accuracy while controlling for phylogeny.
Results
Mimetic accuracy increased with spider body size but differently depending on habitat type. On the ground and in low vegetation, smaller species were inaccurate; whereas on shrubs and trees even smaller species were accurate. Accuracy increased from temperate to tropical locations, again differently depending on habitat. In the temperate zone, only species occurring on bushes were accurate, but in the tropical zone even ground-living species were accurate.
Main conclusions
Higher accuracy at lower latitudes is likely due to stronger predation pressure from visually hunting predators. Lower accuracy in species occurring near the ground is presumably due to predation pressure by non-visually hunting predators. Inaccurate myrmecomorphy in spiders appears to be further driven by smaller body size due to lower profitability to predators; and higher latitude due to increased occurrence of generalist predators.
... In many mimicry rings, this fitness optimum may be shared among multiple species, providing independent tests of natural selection and phenotypic convergence or advergence. Many mimicry rings are amenable to experimental tests in the field and under laboratory conditions, which have been used abundantly to generate a rich understanding of predation, mutualism, parasitism, and natural selection in nature (Brodie & Brodie 1980;Brower 1960;Brower et al. 1960Brower et al. , 1963Finkbeiner et al. 2017Finkbeiner et al. , 2018Harper et al. 2007;Kikuchi & Pfennig 2010;Pfennig et al. 2001Pfennig et al. , 2007Rönkä et al. 2020). An increasing understanding of the genetic and developmental bases of mimetic resemblance (Figure 3) has provided a mechanistic understanding of mimetic adaptations (Deshmukh et al. 2018(Deshmukh et al. , 2020Hines et al. 2011;Kikuchi et al. 2014;Komata et al. 2016;Kunte et al. 2014;Reed et al. 2011;Ruttenberg et al. 2021;Timmermans et al. 2020). ...
... In their extended ranges, the mimics lose their mimetic advantage over nonmimics and are treated as ordinary edible prey by local predators Pfennig et al. 2001Pfennig et al. , 2007. Here, the mimetic pattern may either persist at low frequencies under drift or be eliminated in competition with nonmimetic phenotypes due to the conspicuousness of the mimetic form, even in the face of gene flow from mimetic populations (Harper & Pfennig 2008, Kikuchi & Pfennig 2010, Ries & Mullen 2008. ...
Mimicry rings are communities of mimetic organisms that are excellent models for ecological and evolutionary studies because the community composition, the nature of the species interactions, the phenotypes under selection, and the selective agents are well characterized. Here, we review how regional and ecological filtering, density- and frequency-dependent selection, toxicity of prey, and age of mimicry rings shape their assembly. We synthesize findings from theoretical and empirical studies to generate the following hypotheses: ( a) the degree of unpalatability and age of mimicry rings increase mimicry ring size and ( b) the degree of unpalatability, generalization of the aposematic signal, and availability of alternative prey are positively related to the breadth of the protection umbrella for an aposematic signal and negatively related to the degree of mimetic resemblance. We also provide a phylogenetic framework in which key aspects of mimicry ring diversification may be studied.
Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 52 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... However, neither of these studies explicitly considered hoverflies that are thought to be nonmimics. Studies examining mimicry in coral snakes have found that good Batesian mimicry could gradually evolve from nonmimetic ancestral species, and that maladaptive mimetic patterns can break down, resulting in poor mimics being deeply nested in a clade of good mimics (Kikuchi and Pfennig 2010;Hodson and Lehtinen 2017). However, life history traits that could be associated with the evolution of mimicry, such as diet or body size, were not considered in these analyses. ...
... Our results suggest that wasp mimicry has occasionally been lost deep within a clade of good wasp mimics; thus, to assume that conspicuous wasp-mimetic hoverflies always evolve from nonmimetic ancestral phenotypes may be inappropriate ( Fig. 3; see also Kikuchi and Pfennig 2010;Hodson and Lehtinen 2017). The loss of mimetic accuracy could result from an alteration in the selective environment, meaning that wasp mimicry was no longer an advantageous adaptation. ...
Hoverflies (Diptera: Syrphidae) provide an excellent opportunity to study the evolution of Batesian mimicry, where defenceless prey avoid predation by evolving to resemble defended ‘model’ species. While some hoverflies beautifully resemble their hymenopteran models, others seem to be poor mimics or are apparently non-mimetic. The reasons for this variation are still enigmatic despite decades of research. Here, we address this issue by mapping social-wasp mimicry across the phylogeny of Holarctic hoverflies. Using the ‘distance transform’ technique, we calculate an objective measure of the abdominal pattern similarity between 167 hoverfly species and a widespread putative model, the social wasp, Vespula germanica. We find that good wasp mimicry has evolved several times, and may have also been lost, leading to the presence of non-mimics deep within clades of good mimics. Body size was positively correlated with similarity to the model, supporting previous findings that smaller species are often poorer mimics. Additionally, univoltine species were less accurate wasp mimics than multivoltine and bivoltine species. Hence, variation in the accuracy of Batesian mimics may reflect variation in the opportunity for selection caused by differences in prey value or signal perception (influenced by body size) and phenology or generation time (influenced by voltinism).
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