Evolution Of Mimicry Research Articles

Genome of the early spider-orchid Ophrys sphegodes provides insights into sexual deception and pollinator adaptation

Pollinator-driven evolution of floral traits is thought to be a major driver of angiosperm speciation and diversification. Ophrys orchids mimic female insects to lure male pollinators into pseudocopulation. This strategy, called sexual deception, is species-specific, thereby providing strong premating reproductive isolation. Identifying the genomic architecture underlying pollinator adaptation and speciation may shed light on the mechanisms of angiosperm diversification. Here, we report the 5.2 Gb chromosome-scale genome sequence of Ophrys sphegodes. We find evidence for transposable element expansion that preceded the radiation of the O. sphegodes group, and for gene duplication having contributed to the evolution of chemical mimicry. We report a highly differentiated genomic candidate region for pollinator-mediated evolution on chromosome 2. The Ophrys genome will prove useful for investigations into the repeated evolution of sexual deception, pollinator adaptation and the genomic architectures that facilitate evolutionary radiations.

Integrating ecological niche modeling and rates of evolution to model geographic regions of mimetic color pattern selection

Geographic variation in natural selection derived from biotic sources is an important driver of trait evolution. The evolution of Müllerian mimicry is governed by dual biotic forces of frequency-dependent predator selection and densities of prey populations consisting of conspecifics or congeners. Difficulties in quantifying these biotic forces can lead to difficulties in delimiting and studying phenomena such as mimicry evolution. We explore the spatial distribution of morphotypes and identify areas of high mimetic selection using a novel combination of methods to generate maps of mimetic phenotype prevalence in Ranitomeya poison frogs, a group of frogs characterized by great phenotypic variation and multiple putative Müllerian mimic pairs. We categorized representative populations of all species into four major recurring color patterns observed in Ranitomeya: striped, spotted, redhead, and banded morphs. We calculated rates of phenotypic evolution for each of the 4 morphs separately and generated ecological niche models (ENMs) for all species. We then split our species-level ENMs on the basis of intraspecific variation in color pattern categorization, and weighted ENM layers by relative evolutionary rate to produce mimicry maps. Our phenotypic evolutionary rate analyses identified multiple significant shifts in rates of evolution for the spotted, redhead, and banded phenotypes. Our mimicry maps successfully identify all suspected and known areas of Müllerian mimicry selection in Ranitomeya from the literature and show geographic areas with a gradient of suitability for Müllerian mimicry surrounding mimic hotspots. This approach offers an effective hypothesis generation method for studying traits that are tied to geography by explicitly connecting evolutionary patterns of traits to trends in their geographic distribution, particularly in situations where there are unknowns about drivers of trait evolution.

Hybridization constrains the evolution of mimicry complexes in woodpeckers

The evolution of interspecific mimicry does not always result in perfect resemblance between mimics and models. Differences between members of a mimicry complex can be explained by genetic or developmental constraints. Alternatively, imperfect mimicry might be the outcome of a tradeoff between multiple selective pressures. In this study, we explored the evolutionary conflict between mimicry and hybridization in woodpeckers. Based on the selective tradeoff hypothesis, we expected that mimicry complexes will start to evolve once the constraint of maladaptive hybridization is relaxed. Hence, we predicted limited overlap in the divergence times between hybridizing species pairs and members of a mimicry complex. This prediction was supported by clear tipping point in the probability of hybridization and mimicry at ca 9 million years of divergence. Around this timepoint, the probability of hybridization approaches zero while the probability of belonging to a mimicry complex increases. This finding is only correlational and remains to be confirmed in other taxonomic groups. Nonetheless, our results suggest a selective tradeoff between evolving interspecific mimicry and avoiding maladaptive hybridization in woodpeckers.

The genomics and evolution of inter-sexual mimicry and female-limited polymorphisms in damselflies

Sex-limited morphs can provide profound insights into the evolution and genomic architecture of complex phenotypes. Inter-sexual mimicry is one particular type of sex-limited polymorphism in which a novel morph resembles the opposite sex. While inter-sexual mimics are known in both sexes and a diverse range of animals, their evolutionary origin is poorly understood. Here, we investigated the genomic basis of female-limited morphs and male mimicry in the common bluetail damselfly. Differential gene expression between morphs has been documented in damselflies, but no causal locus has been previously identified. We found that male mimicry originated in an ancestrally sexually dimorphic lineage in association with multiple structural changes, probably driven by transposable element activity. These changes resulted in ~900 kb of novel genomic content that is partly shared by male mimics in a close relative, indicating that male mimicry is a trans-species polymorphism. More recently, a third morph originated following the translocation of part of the male-mimicry sequence into a genomic position ~3.5 mb apart. We provide evidence of balancing selection maintaining male mimicry, in line with previous field population studies. Our results underscore how structural variants affecting a handful of potentially regulatory genes and morph-specific genes can give rise to novel and complex phenotypic polymorphisms.

When a glimpse is enough: Partial mimicry of jumping spiders by insects

Many flies and moths mimic the frontal appearance of jumping spiders. This type of mimicry, which we term as partial mimicry, can be distinguished from Batesian mimicry since the mimic has spider resembling patterns only in certain parts of the body, and not the entire body. The presence of spider-like patterns is obvious only at certain angles suggesting that the mimic is frequently targeted by its predators from particular angles. We tested this hypothesis using Deep Convolutional Neural Networks (DCNNs). First, we trained the network on images of forward facing jumping spiders, where features such as the large principal eyes, small lateral eyes and outstretched legs were evident. Then we tested the classifier on images of jumping spider mimicking flies and moths. A probability value according to the likelihood of the image being a jumping spider or not was assigned by the classifier. We show that the classifier was more likely to misidentify mimicking flies and moths as jumping spiders, but that this probability varied according to the species tested. We further tested it on images of flies from different angles and by taking into consideration the visual acuity of potential predators. Our results suggest that neural networks can be efficient tools for testing evolutionary hypotheses, and that partial mimicry may be a result of the effect of the signaling angle and orientation of the mimics in combination with the likelihood that predators may depend on cognitive shortcuts to identify insects as prey. Further experiments incorporating the properties of the visual system of predators (such as vision in ultraviolet) would result in a better understanding of the evolution of partial mimicry.

Model aversiveness and the evolution of imperfect Batesian mimics.

There are numerous examples of Batesian mimics that only imperfectly resemble their models. Given that inaccurate mimics are known to be predated more frequently than accurate ones, imperfect mimicry therefore poses something of a conundrum. One putative explanation, the relaxed selection hypothesis, predicts that when the cost of attacking a model is high relative to the benefit of consuming a mimic, selection against imperfect mimics will be relaxed, allowing mimics to be more imperfect for a given level of fitness. However, empirical support for this hypothesis is equivocal. Here, we report an experimental test of the relaxed selection hypothesis, in which human participants were tasked with discriminating between artificial stimuli representing models and mimics. In response to "attacking" a model (i.e., misclassifying it as palatable, or non-aversive) they received either a mild electric shock (high cost) or vibratory feedback (low cost). Consistent with the predictions of this hypothesis, we found that when the cost of attacking a model was high, mimetic phenotype could deviate more from the model (i.e., be more imperfect) for a given level of fitness than when the cost of attacking a model was low. Moreover, when the cost of attacking a model was high, participants showed an increased latency to attack. This finding shows that given sufficient costs, the relaxed selection hypothesis is a plausible explanation for the evolution of imperfect mimicry.

Ebony underpins Batesian mimicry in melanic stoneflies.

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.

High level of novelty under the hood of convergent evolution.

Little is known about the extent to which species use homologous regulatory architectures to achieve phenotypic convergence. By characterizing chromatin accessibility and gene expression in developing wing tissues, we compared the regulatory architecture of convergence between a pair of mimetic butterfly species. Although a handful of color pattern genes are known to be involved in their convergence, our data suggest that different mutational paths underlie the integration of these genes into wing pattern development. This is supported by a large fraction of accessible chromatin being exclusive to each species, including the de novo lineage-specific evolution of a modular optix enhancer. These findings may be explained by a high level of developmental drift and evolutionary contingency that occurs during the independent evolution of mimicry.

How the Easter Egg Weevils Got Their Spots: Phylogenomics Reveals Müllerian Mimicry in Pachyrhynchus (Coleoptera, Curculionidae).

The evolutionary origins of mimicry in the Easter egg weevil, Pachyrhynchus, have fascinated researchers since first noted more than a century ago by Alfred Russel Wallace. Müllerian mimicry, or mimicry in which 2 or more distasteful species look similar, is widespread throughout the animal kingdom. Given the varied but discrete color patterns in Pachyrhynchus, this genus presents one of the best opportunities to study the evolution of both perfect and imperfect mimicry. We analyzed more than 10,000 UCE loci using a novel partitioning strategy to resolve the relationships of closely related species in the genus. Our results indicate that many of the mimetic color patterns observed in sympatric species are due to convergent evolution. We suggest that this convergence is driven by positive frequency-dependent selection. [Biogeography, discrete traits, frequency-dependent selection, mimicry, partitioning, Philippines, polymorphic, UCE.].

Evolutionary origins of sexual dimorphism: Lessons from female-limited mimicry in butterflies.

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 favoring mimicry toward defended species could be higher in females because of their slower flight, and thus overcome developmental constraints favoring 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 hypothesize 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 Batesianmimics.

Phenotypic Plasticity of the Mimetic Swallowtail Butterfly Papilio polytes: Color Pattern Modifications and Their Implications in Mimicry Evolution.

Butterfly wing color patterns are sensitive to environmental stress, such as temperature shock, and this phenotypic plasticity plays an important role in color pattern evolution. However, the potential contributions of phenotypic plasticity to mimicry evolution have not been evaluated. Here, we focused on the swallowtail butterfly Papilio polytes, which has nonmimetic and mimetic forms in females, to examine its plastic phenotypes. In the nonmimetic form, medial white spots and submarginal reddish spots in the ventral hindwings were enlarged by cold shock but were mostly reduced in size by heat shock. These temperature-shock-induced color pattern modifications were partly similar to mimetic color patterns, and nonmimetic females were more sensitive than males and mimetic females. Unexpectedly, injection of tungstate, a known modification inducer in nymphalid and lycaenid butterflies, did not induce any modification, but fluorescent brightener 28, another inducer discovered recently, induced unique modifications. These results suggest that phenotypic plasticity in nonmimetic females might have provided a basis of natural selection for mimetic color patterns during evolution.

Mesozoic insect fossils reveal the early evolution of twig mimicry

Twig mimicry is common and diversified within Phasmatodea (stick and leaf insects). However, the fossil record of Phasmatodea is scant, especially evidence for the early evolution of twig mimicry. Herein, Yang et al. describe several stick insects from the Middle Jurassic (∼165 Ma) and mid-Cretaceous (∼99 Ma), and reconstruct the transitions in thoracic morphology relating to their overall twig form. Based on the phylogenetic relationships within Phasmatodea, the new findings suggest a possible evolutionary scenario for the phenomenon of twig mimicry.

Molecular Identification of an Avian Predator of Mimetic Salamanders

Natural field observations of salamander predation are uncommon, in some cases limiting the ability of scientists to study the evolution of toxicity, aposematism, and mimicry in these amphibians. Here, we document field observations of recently depredated salamanders: 1 Pseudotriton ruber (Red Salamander) and 2 Gyrinophilus porphyriticus (Spring Salamander), members of a putative Müllerian mimetic complex involving Notophthalmus viridescens (Eastern Newt). We used molecular methods to identify the likely avian predator of the Spring Salamanders and underscore the opportunities for future research enabled by the pairing of traditional natural history with modern molecular techniques.

Developing Behavioral Markers of Social Function in Aging: A Methodology Using Pitch Mimicry

The Covid pandemic brought to the forefront the crucial role of social interactions for society at large and in gerontological practice. Social interactions play a paramount role in preserving cognitive reserve in older adults. They rely on neurobehavioral processes that are complex (engage large parts of the brain and demand integrity of multiple perceptuomotor, attentional, cognitive and memory functions). Pitch mimicry is a well-known and spontaneously arising social phenomenon that requires the integrity of numerous processes of the brain, and we hypothesize that it constitutes a potentially sensitive behavioral marker of neurodegeneration in Alzheimer’s Disease and Related Dementias (ADRD). We developed and validated a series of algorithms to parse verbal exchanges between people and quantify the level of mimicry that each exhibit with their partners. Those algorithms are based on silence thresholding, carefully parametrized CEPSTRAL algorithms for automatic pitch estimation and Synchrosqueezing Transform for validation. We introduce a theoretical model to compare our estimates of pitch mimicry with model’s expectations based on the null hypothesis that its neurobehavioral pathways retain their integrity. Our method will allow researchers to study the evolution of pitch mimicry in aging individuals and its sensitivity to diverse social contexts, including those preserving lasting social engagement. Our method will also allow us to test the hypothesis that Pitch Mimicry is a sensitive behavioral marker of dementia, a condition characterized by a breakdown in social relatedness.

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.

Mapping the evolution of accurate Batesian mimicry of social wasps in hoverflies.

Hoverflies (Diptera: Syrphidae) provide an excellent opportunity to study the evolution of Batesian mimicry, where defenseless prey avoid predation by evolving to resemble defended "model" species. Although some hoverflies beautifully resemble their hymenopteran models, others seem to be poor mimics or are apparently nonmimetic. 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 nonmimics 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).

Quantifying plant mimesis in fossil insects using deep learning

ABSTRACT As an important combination of behaviour and pattern in animals to resemble benign objects, biolog ical mimesis can effectively avoid the detection of their prey and predators. It at least dates back to the Permian in fossil records. The recognition of mimesis within fossil, however, might be subjective and lack quantitative analysis being only based on few fossils with limited information. To compensate for this omission, we propose a new method using a Siamese network to measure the dissimilarity between hypothetical mimics and their models from images. It generates dissimilarity values between paired images of organisms by extracting feature vectors and calculating Euclidean distances. Additionally, the idea of ‘transfer learning’ is adopted to fine-tune the Siamese network, to overcome the limitations of available fossil image pairs. We use the processed Totally-Looks-Like, a large similar image data set, to pretrain the Siamese network and fine-tune it with a collected mimetic-image data set. Based on our results, we propose two recommended image dissimilarity thresholds for judging the mimicry of extant insects (0–0.4556) and fossil insects (0–0.4717). Deep learning algorithms are used to quantify the mimicry of fossil insects in this study, providing novel insights into exploring the early evolution of mimicry.

Imperfect mimicry of host begging calls by a brood parasitic cuckoo: a cue for nestling rejection by hosts?

Coevolutionary interactions between avian brood parasites and their hosts often lead to the evolution of discrimination and rejection of parasite eggs or chicks by hosts based on visual cues, and the evolution of visual mimicry of host eggs or chicks by brood parasites. Hosts may also base rejection of brood parasite nestlings on vocal cues, which would in turn select for mimicry of host begging calls in brood parasite chicks. In cuckoos that exploit multiple hosts with different begging calls, call structure may be plastic, allowing nestlings to modify their calls to match those of their various hosts, or fixed, in which case we would predict either imperfect mimicry or divergence of the species into host-specific lineages. In our study of the little bronze-cuckoo (LBC) Chalcites minutillus and its primary host, the large-billed gerygone Gerygone magnirostris, we tested whether: (1) hosts use nestling vocalizations as a cue to discriminate cuckoo chicks; (2) cuckoo nestlings mimic the host begging calls throughout the nestling period; and (3) the cuckoo begging calls are plastic, thereby facilitating mimicry of the calls of different hosts. We found that the begging calls of LBCs are most similar to their gerygone hosts shortly after hatching (when rejection by hosts typically occurs) but become less similar as cuckoo chicks get older. Begging call structure may be used as a cue for rejection by hosts, and these results are consistent with gerygone defenses selecting for age-specific vocal mimicry in cuckoo chicks. We found no evidence that LBC begging calls were plastic.

Do floral and ecogeographic isolation allow the co-occurrence of two ecotypes of Anacamptis papilionacea (Orchidaceae)?

Ecotypes are relatively frequent in flowering plants and considered central in ecological speciation as local adaptation can promote the insurgence of reproductive isolation. Without geographic isolation, gene flow usually homogenizes the allopatrically generated phenotypic and ecological divergences, unless other forms of reproductive isolation keep them separated. Here, we investigated two orchid ecotypes with marked phenotypic floral divergence that coexist in contact zones. We found that the two ecotypes show different ecological habitat preferences with one being more climatically restricted than the other. The ecotypes remain clearly morphologically differentiated both in allopatry and in sympatry and differed in diverse floral traits. Despite only slightly different flowering times, the two ecotypes achieved floral isolation thanks to different pollination strategies. We found that both ecotypes attract a wide range of insects, but the ratio of male/female attracted by the two ecotypes was significantly different, with one ecotype mainly attracts male pollinators, while the other mainly attracts female pollinators. As a potential consequence, the two ecotypes show different pollen transfer efficiency. Experimental plots with pollen staining showed a higher proportion of intra‐ than interecotype movements confirming floral isolation between ecotypes in sympatry while crossing experiments excluded evident postmating barriers. Even if not completely halting the interecotypes pollen flow in sympatry, such incipient switch in pollination strategy between ecotypes may represent a first step on the path toward evolution of sexual mimicry in Orchidinae.

Evolutionary and ecological processes influencing chemical defense variation in an aposematic and mimetic Heliconius butterfly.

Chemical defences against predators underlie the evolution of aposematic coloration and mimicry, which are classic examples of adaptive evolution. Surprisingly little is known about the roles of ecological and evolutionary processes maintaining defence variation, and how they may feedback to shape the evolutionary dynamics of species. Cyanogenic Heliconius butterflies exhibit diverse warning color patterns and mimicry, thus providing a useful framework for investigating these questions. We studied intraspecific variation in de novo biosynthesized cyanogenic toxicity and its potential ecological and evolutionary sources in wild populations of Heliconius erato along environmental gradients, in common-garden broods and with feeding treatments. Our results demonstrate substantial intraspecific variation, including detectable variation among broods reared in a common garden. The latter estimate suggests considerable evolutionary potential in this trait, although predicting the response to selection is likely complicated due to the observed skewed distribution of toxicity values and the signatures of maternal contributions to the inheritance of toxicity. Larval diet contributed little to toxicity variation. Furthermore, toxicity profiles were similar along steep rainfall and altitudinal gradients, providing little evidence for these factors explaining variation in biosynthesized toxicity in natural populations. In contrast, there were striking differences in the chemical profiles of H. erato from geographically distant populations, implying potential local adaptation in the acquisition mechanisms and levels of defensive compounds. The results highlight the extensive variation and potential for adaptive evolution in defense traits for aposematic and mimetic species, which may contribute to the high diversity often found in these systems.