Pattern Mimicry Research Articles

Pervasive mimicry in flight behavior among aposematic butterflies

Flight was a key innovation in the adaptive radiation of insects. However, it is a complex trait influenced by a large number of interacting biotic and abiotic factors, making it difficult to unravel the evolutionary drivers. We investigate flight patterns in neotropical heliconiine butterflies, well known for mimicry of their aposematic wing color patterns. We quantify the flight patterns (wing beat frequency and wing angles) of 351 individuals representing 29 heliconiine and 9 ithomiine species belonging to ten color pattern mimicry groupings. For wing beat frequency and up wing angles, we show that heliconiine species group by color pattern mimicry affiliation. Convergence of down wing angles to mimicry groupings is less pronounced, indicating that distinct components of flight are under different selection pressures and constraints. The flight characteristics of the Tiger mimicry group are particularly divergent due to convergence with distantly related ithomiine species. Predator-driven selection for mimicry also explained variation in flight among subspecies, indicating that this convergence can occur over relatively short evolutionary timescales. Our results suggest that the flight convergence is driven by aposematic signaling rather than shared habitat between comimics. We demonstrate that behavioral mimicry can occur between lineages that have separated over evolutionary timescales ranging from <0.5 to 70 My.

Major patterns in the introgression history of Heliconius butterflies

Gene flow between species, although usually deleterious, is an important evolutionary process that can facilitate adaptation and lead to species diversification. It also makes estimation of species relationships difficult. Here, we use the full-likelihood multispecies coalescent (MSC) approach to estimate species phylogeny and major introgression events in Heliconius butterflies from whole-genome sequence data. We obtain a robust estimate of species branching order among major clades in the genus, including the ‘melpomene-silvaniform’ group, which shows extensive historical and ongoing gene flow. We obtain chromosome-level estimates of key parameters in the species phylogeny, including species divergence times, present-day and ancestral population sizes, as well as the direction, timing, and intensity of gene flow. Our analysis leads to a phylogeny with introgression events that differ from those obtained in previous studies. We find that Heliconius aoede most likely represents the earliest-branching lineage of the genus and that ‘silvaniform’ species are paraphyletic within the melpomene-silvaniform group. Our phylogeny provides new, parsimonious histories for the origins of key traits in Heliconius, including pollen feeding and an inversion involved in wing pattern mimicry. Our results demonstrate the power and feasibility of the full-likelihood MSC approach for estimating species phylogeny and key population parameters despite extensive gene flow. The methods used here should be useful for analysis of other difficult species groups with high rates of introgression.

Major patterns in the introgression history of Heliconius butterflies.

Gene flow between species, although usually deleterious, is an important evolutionary process that can facilitate adaptation and lead to species diversification. It also makes estimation of species relationships difficult. Here, we use the full-likelihood multispecies coalescent (MSC) approach to estimate species phylogeny and major introgression events in Heliconius butterflies from whole-genome sequence data. We obtain a robust estimate of species branching order among major clades in the genus, including the 'melpomene-silvaniform' group, which shows extensive historical and ongoing gene flow. We obtain chromosome-level estimates of key parameters in the species phylogeny, including species divergence times, present-day and ancestral population sizes, as well as the direction, timing, and intensity of gene flow. Our analysis leads to a phylogeny with introgression events that differ from those obtained in previous studies. We find that Heliconius aoede most likely represents the earliest-branching lineage of the genus and that 'silvaniform' species are paraphyletic within the melpomene-silvaniform group. Our phylogeny provides new, parsimonious histories for the origins of key traits in Heliconius, including pollen feeding and an inversion involved in wing pattern mimicry. Our results demonstrate the power and feasibility of the full-likelihood MSC approach for estimating species phylogeny and key population parameters despite extensive gene flow. The methods used here should be useful for analysis of other difficult species groups with high rates of introgression.

When perfection isn't enough: host egg signatures are an effective defence against high-fidelity African cuckoo mimicry.

Most mimicry systems involve imperfect mimicry, whereas perfect and high-fidelity mimicry are rare. When the fidelity of mimicry is high, mimics might be expected to have the upper hand against their antagonists. However, in coevolving systems, diversification of model phenotypes may provide an evolutionary escape, because mimics cannot simultaneously match all model individuals in the population. Here we investigate high-fidelity mimicry in a highly specialized, Afrotropical brood parasite-host system: the African cuckoo and fork-tailed drongo. Specifically, we test whether host egg polymorphisms are an effective defence against such mimicry. We show, using a combination of image analysis, field experiments and simulations, that: (1) egg colour and pattern mimicry of fork-tailed drongo eggs by African cuckoos is near-perfect on average; (2) drongos show fine-tuned rejection of foreign eggs, exploiting unpredictable pattern differences between parasitic eggs and their own; and (3) the high degree of interclutch variation (polymorphic egg 'signatures') exhibited by drongos gives them the upper hand in the arms race, with 93.7% of cuckoo eggs predicted to be rejected, despite cuckoos mimicking the full range of drongo egg phenotypes. These results demonstrate that model diversification is a highly effective defence against mimics, even when mimicry is highly accurate.

Common cuckoos do not mimic the size and shape of host eggs

AbstractOften considered a textbook example of coevolution, common cuckoo (Cuculus canorus) eggs are among the best-studied eggs in the world. Female cuckoos belong to genetically distinct host-races, each laying a specific egg type. When host species evolved to reject cuckoo eggs from their nests, cuckoos evolved better egg color and pattern mimicry. In this study, we asked: have cuckoos also evolved eggs that are well matched to host eggs in size and shape, and is the match better for highly discriminating hosts? We used digital image analysis to quantify the sizes and shapes of ~1230 eggs laid by ten European host species and their respective cuckoo host-races. We found that there is some variation in egg size and shape among host species. By contrast, different cuckoo host-races lay eggs that are—on average—similar in size and shape. This generic “one size and shape fits all” cuckoo egg morph is a poor match to most host egg sizes but a good match to most host egg shapes. Overall, we showed that host discrimination behavior was not correlated with the degree of egg size or shape similarity. We concluded that cuckoo females have not evolved egg size or shape mimicry. Alternative explanations for egg shape similarity include biophysical constraints associated with egg formation and selection for incubation efficiency. Finally, to place our results in a broader context, we compared the egg shapes of the common cuckoo and its hosts to those of three Australian parasitic cuckoo species and their hosts.

Egg Pattern Mimicry in Avian Brood Parasitism Assessed Using Local Image Descriptors and Human-Eyes

Egg pattern plays a critical role in avian brood parasitism where a brood parasite exploits a host's parental care by laying eggs in host nests relying on the host to rear the parasitic egg(s). It has been demonstrated that many hosts have evolved an ability to recognize and reject parasitic eggs, based on differences in egg patterns, as a defense against brood parasitism, while some parasites have evolved egg mimicry to counter the host defense. Egg pattern is a complex phenotype and its quantitative evaluation has been a focus of much research. In this paper, we propose a novel method for quantifying an egg pattern and assessing the degree of egg pattern mimicry—a measure of the similarity of a parasite egg to host eggs. Our approach is based on image analysis focused on local binary pattern (LBP) and its variant completed local binary pattern (CLBP) that captures the local structure of a pattern in an image. We compare the results obtained by LBP and CLBP with human-eye evaluation, a classical method widely used in previous studies. Both LBP and CLBP can successfully assess the similarity in egg pattern that is positively correlated with human-eye scores with a high accuracy rate. LBP tends to perform better than CLBP at small scales while CLBP performs better for a wide range of larger scales. Our method can be an effective alternative means of assessing the degree of egg pattern mimicry objectively, providing a useful tool for biologists studying avian brood parasitism. Many bird species have specific eggshell patterns (e.g. spots, blotches, lines) and it has been suggested that these patterns are an important functional trait, such as for camouflage against predators. We propose our method as a useful and objective tool for assessing egg patterns.

A model of octopus epidermis pattern mimicry mechanisms using inverse operation of the Turing reaction model.

Many cephalopods such as octopi and squid can purposefully and rapidly change their skin color. Furthermore, it is widely known that some octopi have the ability to rapidly change the color and unevenness of their skin to mimic their surroundings. However, there has been little research published on the mechanisms by which an octopus recognizes its surrounding landscape and changes its skin pattern. We are unaware of any hypothetical model that explains this mimicry mechanism to date. In this study, the mechanism of octopus skin pattern change was assumed to be based on the Turing pattern model. Here, pattern formation using the Turing model was realized using an equivalent filter calculation model and a cellular automaton instead of directly solving the differential equations. It was shown that this model can create various patterns using two feature parameters. Furthermore, for visual recognition where two features are extracted from the Turing pattern image, a method that requires minimal calculation using the characteristics of the cellular Turing pattern model is proposed. These two calculations can be expressed in the same mathematical frame based on the cellular automaton model using a convolution filter. As a result, a model that is capable of extracting features from patterns and reconstructing those patterns rapidly can be created. This represents a basic model of the mimicry mechanism of octopi. Further, this study demonstrates the potential for creating a model with minimal learning calculation for application to machine learning.

Deep Convergence, Shared Ancestry, and Evolutionary Novelty in the Genetic Architecture of Heliconius Mimicry.

Convergent evolution can occur through different genetic mechanisms in different species. It is now clear that convergence at the genetic level is also widespread, and can be caused by either (i) parallel genetic evolution, where independently evolved convergent mutations arise in different populations or species, or (ii) collateral evolution in which shared ancestry results from either ancestral polymorphism or introgression among taxa. The adaptive radiation of Heliconius butterflies shows color pattern variation within species, as well as mimetic convergence between species. Using comparisons from across multiple hybrid zones, we use signals of shared ancestry to identify and refine multiple putative regulatory elements in Heliconius melpomene and its comimics, Heliconius elevatus and Heliconius besckei, around three known major color patterning genes: optix, WntA, and cortex While we find that convergence between H. melpomene and H. elevatus is caused by a complex history of collateral evolution via introgression in the Amazon, convergence between these species in the Guianas appears to have evolved independently. Thus, we find adaptive convergent genetic evolution to be a key driver of regulatory changes that lead to rapid phenotypic changes. Furthermore, we uncover evidence of parallel genetic evolution at some loci around optix and WntA in H. melpomene and its distant comimic Heliconius erato Ultimately, we show that all three of convergence, conservation, and novelty underlie the modular architecture of Heliconius color pattern mimicry.

Interplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing Patterns.

To what extent can we predict how evolution occurs? Do genetic architectures and developmental processes canalize the evolution of similar outcomes in a predictable manner? Or do historical contingencies impose alternative pathways to answer the same challenge? Examples of Müllerian mimicry between distantly related butterfly species provide natural replicates of evolution, allowing us to test whether identical wing patterns followed parallel or novel trajectories. Here, we explore the role that the signaling ligand WntA plays in generating mimetic wing patterns in Heliconius butterflies, a group with extraordinary mimicry-related wing pattern diversity. The radiation is relatively young, and numerous cases of wing pattern mimicry have evolved within the last 2.5-4.5 Ma. WntA is an important target of natural selection and is one of four major effect loci that underlie much of the pattern variation in the group. We used CRISPR/Cas9 targeted mutagenesis to generate WntA-deficient wings in 12 species and a further 10 intraspecific variants, including three co-mimetic pairs. In all tested butterflies, WntA knockouts affect pattern broadly and cause a shift among every possible scale cell type. Interestingly, the co-mimics lacking WntA were very different, suggesting that the gene networks that pattern a wing have diverged considerably among different lineages. Thus, although natural selection channeled phenotypic convergence, divergent developmental contexts between the two major Heliconius lineages opened different developmental routes to evolve resemblance. Consequently, even under very deterministic evolutionary scenarios, our results underscore a surprising unpredictability in the developmental paths underlying convergence in a recent radiation.

Parallel evolution of ancient, pleiotropic enhancers underlies butterfly wing pattern mimicry

Color pattern mimicry in Heliconius butterflies is a classic case study of complex trait adaptation via selection on a few large effect genes. Association studies have linked color pattern variation to a handful of noncoding regions, yet the presumptive cis-regulatory elements (CREs) that control color patterning remain unknown. Here we combine chromatin assays, DNA sequence associations, and genome editing to functionally characterize 5 cis-regulatory elements of the color pattern gene optix We were surprised to find that the cis-regulatory architecture of optix is characterized by pleiotropy and regulatory fragility, where deletion of individual cis-regulatory elements has broad effects on both color pattern and wing vein development. Remarkably, we found orthologous cis-regulatory elements associate with wing pattern convergence of distantly related comimics, suggesting that parallel coevolution of ancestral elements facilitated pattern mimicry. Our results support a model of color pattern evolution in Heliconius where changes to ancient, multifunctional cis-regulatory elements underlie adaptive radiation.

Unsupervised machine learning reveals mimicry complexes in bumblebees occur along a perceptual continuum.

Müllerian mimicry theory states that frequency-dependent selection should favour geographical convergence of harmful species onto a shared colour pattern. As such, mimetic patterns are commonly circumscribed into discrete mimicry complexes, each containing a predominant phenotype. Outside a few examples in butterflies, the location of transition zones between mimicry complexes and the factors driving mimicry zones has rarely been examined. To infer the patterns and processes of Müllerian mimicry, we integrate large-scale data on the geographical distribution of colour patterns of social bumblebees across the contiguous United States and use these to quantify colour pattern mimicry using an innovative, unsupervised machine-learning approach based on computer vision. Our data suggest that bumblebees exhibit geographically clustered, but sometimes imperfect colour patterns, and that mimicry patterns gradually transition spatially rather than exhibit discrete boundaries. Additionally, examination of colour pattern transition zones of three comimicking, polymorphic species, where active selection is driving phenotype frequencies, revealed that their transition zones differ in location within a broad region of poor mimicry. Potential factors influencing mimicry transition zone dynamics are discussed.

Genome-wide introgression among distantly related Heliconius butterfly species.

BackgroundAlthough hybridization is thought to be relatively rare in animals, the raw genetic material introduced via introgression may play an important role in fueling adaptation and adaptive radiation. The butterfly genus Heliconius is an excellent system to study hybridization and introgression but most studies have focused on closely related species such as H. cydno and H. melpomene. Here we characterize genome-wide patterns of introgression between H. besckei, the only species with a red and yellow banded ‘postman’ wing pattern in the tiger-striped silvaniform clade, and co-mimetic H. melpomene nanna.ResultsWe find a pronounced signature of putative introgression from H. melpomene into H. besckei in the genomic region upstream of the gene optix, known to control red wing patterning, suggesting adaptive introgression of wing pattern mimicry between these two distantly related species. At least 39 additional genomic regions show signals of introgression as strong or stronger than this mimicry locus. Gene flow has been on-going, with evidence of gene exchange at multiple time points, and bidirectional, moving from the melpomene to the silvaniform clade and vice versa. The history of gene exchange has also been complex, with contributions from multiple silvaniform species in addition to H. besckei. We also detect a signature of ancient introgression of the entire Z chromosome between the silvaniform and melpomene/cydno clades.ConclusionsOur study provides a genome-wide portrait of introgression between distantly related butterfly species. We further propose a comprehensive and efficient workflow for gene flow identification in genomic data sets.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-0889-0) contains supplementary material, which is available to authorized users.

Rapid diversification associated with ecological specialization in Neotropical Adelpha butterflies.

Rapid diversification is often associated with morphological or ecological adaptations that allow organisms to radiate into novel niches. Neotropical Adelpha butterflies, which comprise over 200 species and subspecies, are characterized by extraordinary breadth in host plant use and wing colour patterns compared to their closest relatives. To examine the relationship between phenotypic and species diversification, we reconstructed the phylogenetic history of Adelpha and its temperate sister genus Limenitis using genomewide restriction-site-associated DNA (RAD) sequencing. Despite a declining fraction of shared markers with increasing evolutionary distance, the RAD-Seq data consistently generated well-supported trees using a variety of phylogenetic methods. These well-resolved phylogenies allow the identification of an ecologically important relationship with a toxic host plant family, as well as the confirmation of widespread, convergent wing pattern mimicry throughout the genus. Taken together, our results support the hypothesis that evolutionary innovations in both larvae and adults have permitted the colonization of novel host plants and fuelled adaptive diversification within this large butterfly radiation.

Defining the colour pattern phenotype in bumble bees (Bombus): a new model for evo devo

Few insects exhibit the striking colour pattern radiation found in bumble bees (Bombus), which have diversified globally into a wide range of colours and patterns. Their potent sting is often advertised by conspicuous bands of contrasting colour commonly mimicked by scores of harmless (Batesian mimics) and noxious species (Mullerian co-mimics). Despite extensive documentation of colour pattern diversification, next to nothing is known about the genetic regulation of pattern formation in bumble bees, hindering progress toward a more general model of the evolution of colour pattern mimicry. A critical first step in understanding the colour pattern genotype is an unambiguous understanding of the phenotype under selection, which has not been objectively defined in bumble bees. Here, we quantitatively define the principal colour pattern elements that comprise the phenotype array across all species. Matrix analysis of meticulously scored colour patterns of ∼95% of described species indicates there are 12 discrete primary ‘ground plan’ elements in common among all species, many of which correspond to segmentation patterning. Additional secondary elements characterize individual species and geographical variants. The boundaries of these elements appear to correspond to expression patterns of Hox genes in Drosophila and Apis but also suggest novel post-Hox specialization of abdominal patterning. Our findings provide the first foundation for exploring candidate genes regulating adaptive pattern variation in bumble bees and broaden the framework for understanding common genetic mechanisms of pattern evolution in insects. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 384‐404.

Do Heliconius butterfly species exchange mimicry alleles?

Hybridization has the potential to transfer beneficial alleles across species boundaries, and there are a growing number of examples in which this has apparently occurred. Recent studies suggest that Heliconius butterflies have transferred wing pattern mimicry alleles between species via hybridization, but ancestral polymorphism could also produce a signature of shared ancestry around mimicry genes. To distinguish between these alternative hypotheses, we measured DNA sequence divergence around putatively introgressed mimicry loci and compared this with the rest of the genome. Our results reveal that putatively introgressed regions show strongly reduced sequence divergence between co-mimetic species, suggesting that their divergence times are younger than the rest of the genome. This is consistent with introgression and not ancestral variation. We further show that this signature of introgression occurs at sites throughout the genome, not just around mimicry genes.

Modularity of a leaf moth-wing pattern and a versatile characteristic of the wing-pattern ground plan

BackgroundOne of the most intriguing questions in evolutionary developmental biology is how an insect acquires a mimicry pattern within its body parts. A striking example of pattern mimicry is found in the pattern diversity of moth and butterfly wings, which is thought to evolve from preexisting elements illustrated by the nymphalid ground plan (NGP). Previous studies demonstrated that individuality of the NGP facilitates the decoupling of associated common elements, leading to divergence. In contrast, recent studies on the concept of modularity have argued the importance of a combination of coupling and decoupling of the constituent elements. Here, we examine the modularity of a mimicry wing pattern in a moth and explore an evolvable characteristic of the NGP.ResultsThis study examined the wings of the noctuid moth Oraesia excavata, which closely resemble leaves with a leaf venation pattern. Based on a comparative morphological procedure, we found that this leaf pattern was formed by the NGP common elements. Using geometric morphometrics combined with network analysis, we found that each of the modules in the leaf pattern integrates the constituent components of the leaf venation pattern (i.e., the main and lateral veins). Moreover, the detected modules were established by coupling different common elements and decoupling even a single element into different modules. The modules of the O. excavata wing pattern were associated with leaf mimicry, not with the individuality of the NGP common elements. For comparison, we also investigated the modularity of a nonmimetic pattern in the noctuid moth Thyas juno. Quantitative analysis demonstrated that the modules of the T. juno wing pattern regularly corresponded to the individuality of the NGP common elements, unlike those in the O. excavata wing pattern.ConclusionsThis study provides the first evidence for modularity in a leaf mimicry pattern. The results suggest that the evolution of this pattern involves coupling and decoupling processes to originate these modules, free from the individuality of the NGP system. We propose that this evolution has been facilitated by a versatile characteristic of the NGP, allowing the association of freely modifiable subordinate common elements to make modules.

Introgression and fixation of mimicry genes

Sequencing the genome of Heliconius melpomene has enabled genome-scale analysis of introgression in Heliconius, which is a rapidly radiating genus of butterflies. This analysis has revealed a hybrid exchange of genes at genomic regions that control wing pattern mimicry, which is a protective mechanism whereby species mimic each others' warning signals to warn off predators. The authors infer that closely related Heliconius species exchange protective colour pattern genes promiscuously and that hybridization can aid adaptation by transferring beneficial traits between species.

Optix Drives the Repeated Convergent Evolution of Butterfly Wing Pattern Mimicry

Mimicry--whereby warning signals in different species evolve to look similar--has long served as a paradigm of convergent evolution. Little is known, however, about the genes that underlie the evolution of mimetic phenotypes or to what extent the same or different genes drive such convergence. Here, we characterize one of the major genes responsible for mimetic wing pattern evolution in Heliconius butterflies. Mapping, gene expression, and population genetic work all identify a single gene, optix, that controls extreme red wing pattern variation across multiple species of Heliconius. Our results show that the cis-regulatory evolution of a single transcription factor can repeatedly drive the convergent evolution of complex color patterns in distantly related species, thus blurring the distinction between convergence and homology.

AVIAN VISION AND THE EVOLUTION OF EGG COLOR MIMICRY IN THE COMMON CUCKOO

Coevolutionary arms races are a potent force in evolution, and brood parasite-host dynamics provide classical examples. Different host-races of the common cuckoo, Cuculus canorus, lay eggs in the nests of other species, leaving all parental care to hosts. Cuckoo eggs often (but not always) appear to match remarkably the color and pattern of host eggs, thus reducing detection by hosts. However, most studies of egg mimicry focus on human assessments or reflectance spectra, which fail to account for avian vision. Here, we use discrimination and tetrachromatic color space modeling of bird vision to quantify egg background and spot color mimicry in the common cuckoo and 11 of its principal hosts, and we relate this to egg rejection by different hosts. Egg background color and luminance are strongly mimicked by most cuckoo host-races, and mimicry is better when hosts show strong rejection. We introduce a novel measure of color mimicry-"color overlap"-and show that cuckoo and host background colors increasingly overlap in avian color space as hosts exhibit stronger rejection. Finally, cuckoos with better background color mimicry also have better pattern mimicry. Our findings reveal new information about egg mimicry that would be impossible to derive by the human eye.

Pattern mimicry of host eggs by the common cuckoo, as seen through a bird's eye

Cuckoo-host interactions provide classical examples of coevolution. Cuckoos place hosts under selection to detect and reject foreign eggs, while host defences result in the evolution of host-egg mimicry in cuckoos. Despite a long history of research, egg pattern mimicry has never been objectively quantified, and so its coevolution with host defences has not been properly assessed. Here, we use digital image analysis and modelling of avian vision to quantify the level of pattern mimicry in eight host species of the common cuckoo Cuculus canorus and their respective cuckoo host-races. We measure a range of pattern attributes, including marking size, diversity in size, contrast, coverage and dispersion. This new technique reveals hitherto unnoticed sophistication in egg pattern mimicry. We show that various features of host egg pattern are mimicked by the eggs of their respective cuckoo host-races, and that cuckoos have evolved better pattern mimicry for host species that exhibit stronger egg rejection. Pattern differs relatively more between eggs of different host species than between their respective cuckoo host-races. We suggest that cuckoos may have more 'average' markings in order to be able to use subsidiary hosts. Our study sheds new light on cuckoo-host coevolution and illustrates a new technique for quantifying animal markings with respect to the relevant animal visual system.