Mimetic Traits Research Articles

An arachnid’s guide to being an ant: morphological and behavioral mimicry in ant-mimicking spiders

Abstract Batesian mimicry imposes several challenges to mimics and evokes adaptations in multiple sensory modalities. Myrmecomorphy, morphological and behavioral resemblance to ants, is seen in over 2000 arthropod species. Ant-like resemblance is observed in at least 13 spider families despite spiders having a distinct body plan compared to ants. Quantifying the extent to which spiders’ shape, size, and behavior resemble model ants will allow us to comprehend the evolutionary pressures that have facilitated myrmecomorphy. Myrmaplata plataleoides are thought to closely resemble weaver ants, Oecophylla smaragdina. In this study, we quantify the speed of movement of model, mimic, and non-mimetic jumping spiders. We use traditional and geometric morphometrics to quantify traits such as foreleg size and hindleg size, body shape between the model ant, mimic, and non-mimics. Our results suggest that while the mimics closely resemble the model ants in speed of movement, they occupy an intermediate morphological space compared to the model ants and non-mimics. Ant-mimicking spiders are better at mimicking ants’ locomotory movement than morphology and overall body shape. Some traits may compensate others, suggesting differential selection on these mimetic traits. Our study provides a framework to understand the multimodal nature of mimicry and helps discern the relative contributions of such traits that drive mimetic accuracy in ant-mimicking spiders.

Functional unit of supergene in female-limited Batesian mimicry of Papilio polytes.

Supergenes are sets of genes and genetic elements that are inherited like a single gene and control complex adaptive traits, but their functional roles and units are poorly understood. In Papilio polytes, female-limited Batesian mimicry is thought to be regulated by a ∼130 kb inversion region (highly diversified region: HDR) containing 3 genes, UXT, U3X, and doublesex (dsx) which switches non-mimetic and mimetic types. To determine the functional unit, we here performed electroporation-mediated RNAi analyses (and further Crispr/Cas9 for UXT) of genes within and flanking the HDR in pupal hindwings. We first clarified that non-mimetic dsx-h had a function to form the non-mimetic trait in female and only dsx-H isoform 3 had an important function in the formation of mimetic traits. Next, we found that UXT was involved in making mimetic-type pale-yellow spots and adjacent gene sir2 in making red spots in hindwings, both of which refine more elaborate mimicry. Furthermore, downstream gene networks of dsx, U3X, and UXT screened by RNA sequencing showed that U3X upregulated dsx-H expression and repressed UXT expression. These findings demonstrate that a set of multiple genes, not only inside but also flanking HDR, can function as supergene members, which extends the definition of supergene unit than we considered before. Also, our results indicate that dsx functions as the switching gene and some other genes such as UXT and sir2 within the supergene unit work as the modifier gene.

Mimetic accuracy and co-evolution of mimetic traits in ant-mimicking species

SummaryMyrmecomorphy is the most frequent type of Batesian mimicry. Myrmecomorphic species differ in the accuracy with which they resemble ants; however, the hypothesis of the co-evolution of mimetic traits has been rarely tested. Here, we measured dozens of traits of color, shape, size, and behavior, and quantified objectively the resemblance between dozens of arthropod mimics and ants. In all traits, the mimics were more similar to ants than to closely related non-myrmecomorphic species. We found that mimics resemble ants mainly in color and behavior, and less in size and body shape. We found that the mimetic accuracy in four trait categories demonstrate divergent co-evolutionary patterns. Mimetic accuracy in color was positively correlated with shape and size in insects but negatively in spiders, presumably reflecting developmental constraints. Accuracy in shape tend to be negatively related to movement in both insects and spiders supporting the motion-limited discrimination hypothesis.

Body size in Batesian mimicry

A variety of traits is available for predators to distinguish unpalatable prey from palatable Batesian mimics. Among them, body size has received little attention as a possible mimetic trait. Size should influence predator behaviour if it shows variation between models and mimics, is detectable by the predator in question, and is not overshadowed by other traits more salient to the predator. Simple predictions within mimetic populations are that perfect mimics receive the lowest predation rate. However, prey body size is typically tightly linked to the nutritional yield and handling time for a successful predator, as well as likely being correlated with a model’s levels of defence. In certain circumstances, these confounding factors might mean that (a) selection pressures on a mimic’s size either side of the model’s phenotype are not symmetrical, (b) the optimal body size for a mimic is not necessarily equal to that of the model, and/or (c) for predators, attacking better mimics of a model’s body size more readily is adaptive. I discuss promising avenues for improving our understanding of body size as a mimetic trait, including the importance of treatments that range in both directions from the model’s size. Further work is required to understand how body size ranks in saliency against other mimetic traits such as pattern. Comparative studies could investigate whether mimics are limited to resembling only models that are already similar in size.

Doublesex Controls Both Hindwing and Abdominal Mimicry Traits in the Female-Limited Batesian Mimicry of Papilio memnon.

Papilio butterflies are known to possess female-limited Batesian mimicry polymorphisms. In Papilio memnon, females have mimetic and non-mimetic forms, whereas males are monomorphic and non-mimetic. Mimetic females are characterized by color patterns and tails in the hindwing and yellow abdomens. Recently, an analysis of whole-genome sequences has shown that an approximately 160 kb region of chromosome 25 is responsible for mimicry and has high diversity between mimetic (A) and non-mimetic (a) alleles (highly diversified region: HDR). The HDR includes three genes, UXT, doublesex (dsx), and Nach-like, but the functions of these genes are unknown. Here, we investigated the function of dsx, a gene involved in sexual differentiation, which is expected to be functionally important for hindwing and abdominal mimetic traits in P. memnon. Expression analysis by reverse transcription quantitative PCR (RT-qPCR) and RNA sequencing showed that mimetic dsx (dsx-A) was highly expressed in the hindwings in the early pupal stage. In the abdomen, both dsx-A and dsx-a were highly expressed during the early pupal stage. When dsx was knocked down using small interfering RNAs (siRNAs) designed in the common region of dsx-A and dsx-a, a male-like pattern appeared on the hindwings of mimetic and non-mimetic females. Similarly, when dsx was knocked down in the abdomen, the yellow scales characteristic of mimetic females changed to black. Furthermore, when dsx-a was specifically knocked down, the color pattern of the hindwings changed, as in the case of dsx knockdown in non-mimetic females but not mimetic females. These results suggest that dsx-a is involved in color pattern formation on the hindwings of non-mimetic females, whereas dsx-A is involved in hindwing and abdominal mimetic traits. dsx was involved in abdominal and hindwing mimetic traits, but dsx expression patterns in the hindwing and abdomen were different, suggesting that different regulatory mechanisms may exist. Our study is the first to show that the same gene (dsx) regulates both the hindwing and abdominal mimetic traits. This is the first functional analysis of abdominal mimicry in butterflies.

Genomic architecture and functional unit of mimicry supergene in female limited Batesian mimic Papilio butterflies.

It has long been suggested that dimorphic female-limited Batesian mimicry of two closely related Papilio butterflies, Papilio memnon and Papilio polytes, is controlled by supergenes. Whole-genome sequencing, genome-wide association studies and functional analyses have recently identified mimicry supergenes, including the doublesex (dsx) gene. Although supergenes of both the species are composed of highly divergent regions between mimetic and non-mimetic alleles and are located at the same chromosomal locus, they show critical differences in genomic architecture, particularly with or without an inversion: P. polytes has an inversion, but P. memnon does not. This review introduces and compares the detailed genomic structure of mimicry supergenes in two Papilio species, including gene composition, repetitive sequence composition, breakpoint/boundary site structure, chromosomal inversion and linkage disequilibrium. Expression patterns and functional analyses of the respective genes within or flanking the supergene suggest that dsx and other genes are involved in mimetic traits. In addition, structural comparison of the corresponding region for the mimicry supergene among further Papilio species suggests three scenarios for the evolution of the mimicry supergene between the two Papilio species. The structural features revealed in the Papilio mimicry supergene provide insight into the formation, maintenance and evolution of supergenes. This article is part of the theme issue 'Genomic architecture of supergenes: causes and evolutionary consequences'.

On the evolution of mimicry in avian nestlings.

Batesian mimicry (BM), where a nontoxic species resembles a toxic species with aposematic coloring, has been recently described for a Neotropical species of the suboscine passerine (Laniocera hypopyrra). Understanding the order and series in which these characteristics evolved is unknown and requires character information from closely related taxa. Here, we trace the origin of mimetic traits and how they evolved by examining antipredator characteristics using images and other field‐collected trait data from nest and nestlings along with data available in the literature for the Laniisominae clade and closely related taxa. We found that morphological modifications of the downy feathers appeared first in the broader clade leading to the Laniisominae clade followed by further morphological and behavioral characteristics within the Laniisominae clade leading to the full BM. Images of nestlings in the Laniisominae and closely related clades demonstrated the extent of antipredator and camouflage characteristics. We found a complex set of behavioral and morphological traits in this clade for reducing predation from hiding to camouflage to mimicry. We further propose the evolution of two distinctive mimicry strategies in the Laniisominae clade: (1) Batesian Mimicry, as described above and (2) Masquerade, resemblance to inedible objects commonly found in their local environment. This complex set of antipredator traits shed light on the diversity of antipredator characteristics in avian nestlings, particularly in neotropical areas where the avian diversity is highest. Unfortunately, there are hundreds of species in the neotropics that lack basic natural history information on nesting traits, and therefore, we are likely missing critical information on the diversity of antipredator characteristics across avian nestlings.

Balanced polymorphisms and their divergence in a Heliconius butterfly.

The evolution of mimicry in similarly defended prey is well described by the Müllerian mimicry theory, which predicts the convergence of warning patterns in order to gain the most protection from predators. However, despite this prediction, we can find great diversity of color patterns among Müllerian mimics such as Heliconius butterflies in the neotropics. Furthermore, some species have evolved the ability to maintain multiple distinct warning patterns in single populations, a phenomenon known as polymorphic mimicry. The adaptive benefit of these polymorphisms is questionable since variation from the most common warning patterns is expected to be disadvantageous as novel signals are punished by predators naive to them. In this study, we use artificial butterfly models throughout Central and South America to characterize the selective pressures maintaining polymorphic mimicry in Heliconius doris. Our results highlight the complexity of positive frequency‐dependent selection, the principal selective pressure driving convergence among Müllerian mimics, and its impacts on interspecific variation of mimetic warning coloration. We further show how this selection regime can both limit and facilitate the diversification of mimetic traits.

Measuring mimicry: methods for quantifying visual similarity

The existence of substantial variation in the accuracy of resemblance of mimics to their models remains a fundamental evolutionary question, and the ability to quantify mimetic accuracy is key to addressing this question. Mimicry researchers have used a wide variety of methods to measure accuracy, which can be broadly grouped into (1) receiver responses, such as predator trials, and (2) trait measurements. While receiver responses are fundamental to mimicry research, logistical and ethical concerns mean that only a minority of studies include tests with relevant predator receivers. Trait measurement methods are therefore vital, both to supplement receiver response methods and as standalone methods for quantifying accuracy. Here, we collect and describe five methods for measuring the accuracy of visual mimicry. Three of the methods quantify the similarity of mimetic phenotypic traits: linear morphometrics, geometric morphometrics and biometric trait table. Two methods measure the responses of proxy receivers: machine learning and human assessment. These methods are applicable to any type of visual mimetic traits. We evaluate and compare the effectiveness and cost of these methods by assessing the accuracy of a variety of visual ant mimics to their ant models. The methods vary in the types and number of traits being measured, whether traits are measured directly (trait measurement methods) or indirectly (receiver responses) and in the effort and skills required for implementation. Despite the methods measuring different visual characteristics, the accuracy scores from all five methods were positively correlated when applied to ant mimics, suggesting some generality in how mimics rank in their accuracy. We provide practical advice on the use of these five methods and provide open-source implementations of the scripts used in our analysis. The scripts may be freely reused or used as the basis for new implementations. Our aim is to aid researchers to select and implement methods that are appropriate and suitable for future mimicry research.

The first known riodinid ‘cuckoo’ butterfly reveals deep-time convergence and parallelism in ant social parasites

AbstractMutualistic interactions between butterflies and ants can evolve into complex social parasitism. ‘Cuckoo’ caterpillars, known only in the Lycaenidae, use multimodal mimetic traits to achieve social integration into ant societies. Here, we present the first known ‘cuckoo’ butterfly in the family Riodinidae. Aricoris arenarum remained in taxonomic limbo for > 80 years, relegated to nomen dubium and misidentified as Aricoris gauchoana. We located lost type material, designated lectotypes and documented the morphology and natural history of the immature stages. The multifaceted life cycle of A. arenarum can be summarized in three phases: (1) females lay eggs close to honeydew-producing hemipterans tended by specific Camponotus ants; (2) free-living caterpillars feed on liquids (honeydew and ant regurgitations); and (3) from the third instar onward, the caterpillars are fed and tended by ants as ‘cuckoos’ inside the ant nest. This life cycle is remarkably similar to that of the Asian lycaenid Niphanda fusca, despite divergence 90 Mya. Comparable eco-evolutionary pathways resulted in a suite of ecomorphological homoplasies through the ontogeny. This study shows that convergent interactions can be more important than phylogenetic proximity in shaping functional traits of social parasites.

Digest: The interplay between imprinting, mimicry, and multimodal signaling can lead to sympatric speciation†

Mimicry can directly affect the evolutionary history of models, mimics, and signal receivers. Mimics often use multimodal signaling to deceive receivers. Jamie etal. showed that brood parasitic birds display multimodal signaling of mimetic traits triggered by sexual and filial imprinting on host species. These resulting adaptations can interact with premating isolation barriers to strengthen reproductive isolation and potentially drive sympatric speciation.

The mimetic wing pattern of Papilio polytes butterflies is regulated by a doublesex-orchestrated gene network

The swallowtail butterfly Papilio polytes is sexually dimorphic and exhibits female-limited Batesian mimicry. This species also has two female forms, a non-mimetic form with male-like wing patterns, and a mimetic form resembling an unpalatable model, Pachliopta aristolochiae. The mimicry locus H constitutes a dimorphic Mendelian ‘supergene’, including a transcription factor gene doublesex (dsx). However, how the mimetic-type dsx (dsx-H) orchestrates the downstream gene network and causes the mimetic traits remains unclear. Here we performed RNA-seq-based gene screening and found that Wnt1 and Wnt6 are up-regulated by dsx-H during the early pupal stage and are involved in the red/white pigmentation and patterning of mimetic female wings. In contrast, a homeobox gene abdominal-A is repressed by dsx-H and involved in the non-mimetic colouration pattern. These findings suggest that dual regulation by dsx-H, induction of mimetic gene networks and repression of non-mimetic gene networks, is essential for the switch from non-mimetic to mimetic pattern in mimetic female wings.

Frequency dependence shapes the adaptive landscape of imperfect Batesian mimicry.

Despite more than a century of biological research on the evolution and maintenance of mimetic signals, the relative frequencies of models and mimics necessary to establish and maintain Batesian mimicry in natural populations remain understudied. Here we investigate the frequency-dependent dynamics of imperfect Batesian mimicry, using predation experiments involving artificial butterfly models. We use two geographically distinct populations of Adelpha butterflies that vary in their relative frequencies of a putatively defended model (Adelpha iphiclus) and Batesian mimic (Adelpha serpa). We found that in Costa Rica, where both species share similar abundances, Batesian mimicry breaks down, and predators more readily attack artificial butterfly models of the presumed mimic, A. serpa By contrast, in Ecuador, where A. iphiclus (model) is significantly more abundant than A. serpa (mimic), both species are equally protected from predation. Our results provide compelling experimental evidence that imperfect Batesian mimicry is frequency-dependent on the relative abundance of models and mimics in natural populations, and contribute to the growing body of evidence that complex dynamics, such as seasonality or the availability of alternative prey, influence the evolution of mimetic traits.

Aposematism and mimicry in soft‐bodied beetles of the superfamily Cleroidea (Insecta)

The evolution of animal life strategies is among the main themes of current evolutionary biology. Checkered beetles, soft‐winged flower beetles and their allies (superfamily Cleroidea), exhibit well‐known aposematic colour patterns, particularly in the family Cleridae, which participate in mimicry complexes mostly with unpalatable beetles, ants and velvet ants representing a Müllerian–Batesian continuum. Many cleroids also exhibit attenuated hardening of cuticular layers resulting in a soft‐bodied appearance. Here, a molecular phylogenetic analysis of the entire Cleroidea was performed using sequences of two nuclear and two mitochondrial loci of ~4 kb total length. Inferred phylogenies were used to reconstruct ancestral colour patterns and involvement in mimicry complexes. The hypothesis of a soft‐bodied ancestor of Cleridae and allies was tested. The phylogenetic analyses corroborated the expanded Cleroidea concept including Byturidae and Biphyllidae formerly classified as Cucujoidea. Character state optimization showed cryptic coloration was the ancestral state in Cleroidea, from which aposematic coloration originated several times in distant cleroid lineages. Within Cleridae, mimicry also arose from an ancestor that was cryptic, and multiple lineages that mimicked unpalatable beetles (Chrysomelidae, Meloidae, Lycidae) and stinging Hymenoptera evolved. Aposematic coloration was acquired in all major clerid lineages including Thanerocleridae, which are either the sister group of Chaetosomatidae or Cleridae. These findings suggest that mimetic traits in the clerid clade evolved at various times, possibly soon after the origin of soft‐bodiedness. The adaptive value of aposematism in cleroids is likely to be enhanced in soft‐bodied species, as this trait provides limited means of protection against predators, and therefore may promote the acquisition of aposematic and mimetic coloration in various ecological situations.

Number of genes controlling a quantitative trait in a hybrid zone of the aposematic frog Ranitomeya imitator.

The number of genes controlling mimetic traits has been a topic of much research and discussion. In this paper, we examine a mimetic, dendrobatid frog Ranitomeya imitator, which harbours extensive phenotypic variation with multiple mimetic morphs, not unlike the celebrated Heliconius system. However, the genetic basis for this polymorphism is unknown, and not easy to determine using standard experimental approaches, for this hard-to-breed species. To circumvent this problem, we first develop a new protocol for automatic quantification of complex colour pattern phenotypes from images. Using this method, which has the potential to be applied in many other systems, we define a phenotype associated with differences in colour pattern between different mimetic morphs. We then proceed to develop a maximum-likelihood method for estimating the number of genes affecting a quantitative trait segregating in a hybrid zone. This method takes advantage of estimates of admixture proportions obtained using genetic data, such as microsatellite markers, and is applicable to any other system where a phenotype has been quantified in an admixture/introgression zone. We evaluate the method using extensive simulations and apply it to the R. imitator system. We show that probably one or two, or at most three genes, control the mimetic phenotype segregating in a R. imitator hybrid zone identified using image analyses.

Batesian mimicry promotes pre- and postmating isolation in a snake mimicry complex.

We evaluated whether Batesian mimicry promotes early-stage reproductive isolation. Many Batesian mimics occur not only in sympatry with their model (as expected), but also in allopatry. As a consequence of local adaptation within both sympatry (where mimetic traits are favored) and allopatry (where nonmimetic traits are favored), divergent, predator-mediated natural selection should disfavor immigrants between these selective environments as well as any between-environment hybrids. This selection might form the basis for both pre- and postmating isolation, respectively. We tested for such selection in a snake mimicry complex by placing clay replicas of sympatric, allopatric, or hybrid phenotypes in both sympatry and allopatry and measuring predation attempts. As predicted, replicas with immigrant phenotypes were disfavored in both selective environments. Replicas with hybrid phenotypes were also disfavored, but only in a region of sympatry where previous studies have detected strong selection favoring precise mimicry. By fostering immigrant inviability and ecologically dependent selection against hybrids (at least in some habitats), Batesian mimicry might therefore promote reproductive isolation. Thus, although Batesian mimicry has long been viewed as a mechanism for convergent evolution, it might play an underappreciated role in fueling divergent evolution and possibly even the evolution of reproductive isolation and speciation.

Perspectives and Debates: Mimicry, Signalling and Co‐Evolution (Commentary on Wolfgang Wickler – Understanding Mimicry – With special reference to vocal mimicry)

AbstractIn his stimulating discussion, Wolfgang Wickler criticizes fuzzy usage of term mimicry by drawing attention to its original definition by H. Bates. Mimicry refers to functional ‘model–mimic–selecting agent’ trinity (with varying number of species involved) when the selecting agent (i.e. signal receiver) responds similarly to mimic and model to the advantage of the mimic. Concurring with Wickler I argue that convergence is neither necessary nor sufficient to support similarity as evidence for mimicry and that it is artificial and unproductive to classify mimicry with respect to ontogeny (innate vs. learned similarity) or model species identity (learning from conspecifics vs. heterospecifics). Using butterfly ‘eye’‐spots, I argue that just identifying each of the supposed model, the mimic and the selective agent, and even demonstrating that mimic‐model similarity affects the agent's behaviour, provides no conclusive evidence for mimicry. Even a demonstration that the mimic benefits from receiver response may not provide conclusive evidence for mimicry. Using avian brood parasite–host egg and nestling mimicry, I emphasize that without experimental manipulation of the hypothesized mimetic traits, it is impossible to test the mimicry hypothesis robustly. Due to fundamental constraints on human perception, some cases of mimicry may in fact be just a by‐product of human inability to perceive relevant differences between animal phenotypes (what is similar for human eye, nose or ear may not be viewed, smelled or heard as similar for relevant animal observers), whereas many cases of real mimicry may escape our attention from the same reason (‘hidden’ mimicry). Surprisingly, the same mimetic phenotype may show completely different effects on selective agents under different ecological circumstances. Finally, relatively dissimilar species may be more mimetic than highly similar model–mimic pairs because mimicry may be more fruitfully understood as a co‐evolutionary process rather than a similarity.

EVOLUTIONARY IMPLICATIONS OF THE FORM OF PREDATOR GENERALIZATION FOR APOSEMATIC SIGNALS AND MIMICRY IN PREY

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.

Female preferences drive the evolution of mimetic accuracy in male sexual displays

Males in many bird species mimic the vocalizations of other species during sexual displays, but the evolutionary and functional significance of interspecific vocal mimicry is unclear. Here we use spectrographic cross-correlation to compare mimetic calls produced by male satin bowerbirds (Ptilonorhynchus violaceus) in courtship with calls from several model species. We show that the accuracy of vocal mimicry and the number of model species mimicked are both independently related to male mating success. Multivariate analyses revealed that these mimetic traits were better predictors of male mating success than other male display traits previously shown to be important for male mating success. We suggest that preference-driven mimetic accuracy may be a widespread occurrence, and that mimetic accuracy may provide females with important information about male quality. Our findings support an alternative hypothesis to help explain a common element of male sexual displays.

Context‐Dependent Discrimination and the Evolution of Mimicry

Many mimetic organisms have evolved a close resemblance to their models, making it difficult to discriminate between them on the basis of appearance alone. However, if mimics and models differ slightly in their activity patterns, behavior, or use of microhabitats, the exact circumstances under which a signaler is encountered may provide additional clues to its identity. We employ an optimality model of mimetic discrimination in which signal receivers obtain information about the relative risk of encountering mimics and models by observing an external background cue and flexibly adjust their response thresholds. Although such flexibility on the part of signal receivers has been predicted by theory and is supported by empirical evidence in a range of biological settings, little is known about the effects it has on signalers. We show that the presence of external cues that partly reveal signaler identity may benefit models and harm mimics, harm both, or even benefit both, depending on ecological circumstances. Moreover, if mimetic traits are costly to express, or mimics are related to their neighbors, context-dependent discrimination can dramatically alter the outcome of mimetic evolution. We discuss context-dependent discrimination among signal receivers in relation to small-scale synchrony in model and mimic activity patterns.